@article {1443256, title = {Stability and manoeuvrability in animal movement: lessons from biology, modelling, and robotics}, journal = {Proceedings of the Royal Society, B}, volume = {289}, year = {2022}, pages = {1-5}, url = {https://doi.org/10.1098/rspb.2021.2492}, author = {Biewener, A. A. and Bomphrey, R. N. and Daley, M. A. and Isjpeert, A. J.} } @article {1443254, title = {Physiology {\textendash} Woodpecker skulls are not shock absorbers}, journal = {Current Biology}, volume = {32}, year = {2022}, pages = {R767-R769}, abstract = {Woodpeckers are well-known for their audible percussive wood drilling. A new study shows that these birds benefit from their small size and key skull features to safely hammer at wood for insect food and nesting excavations.}, url = {https://doi.org/10.1016/j.cub.2022.06.037}, author = {Biewener, A. A.} } @article {1443483, title = {Lower-limb muscle function is influenced by changing mechanical demands in cycling}, journal = {Journal of Experimental Biology}, volume = {224}, year = {2021}, abstract = {

ABSTRACT

Although cycling is a seemingly simple, reciprocal task, muscles must adapt their function to satisfy changes in mechanical demands induced by higher crank torques and faster pedalling cadences. We examined whether muscle function was sensitive to these changes in mechanical demands across a wide range of pedalling conditions. We collected experimental data of cycling where crank torque and pedalling cadence were independently varied from 13 to 44 N m and 60 to 140 rpm. These data were used in conjunction with musculoskeletal simulations and a recently developed functional index-based approach to characterise the role of human lower-limb muscles. We found that in muscles that generate most of the mechanical power and work during cycling, greater crank torque induced shifts towards greater muscle activation, greater positive muscle{\textendash}tendon unit (MTU) work and a more motor-like function, particularly in the limb extensors. Conversely, with faster pedalling cadence, the same muscles exhibited a phase advance in muscle activity prior to crank top dead centre, which led to greater negative MTU power and work and shifted the muscles to contract with more spring-like behaviour. Our results illustrate the capacity for muscles to adapt their function to satisfy the mechanical demands of the task, even during highly constrained reciprocal tasks such as cycling. Understanding how muscles shift their contractile performance under varied mechanical and environmental demands may inform decisions on how to optimise pedalling performance and to design targeted cycling rehabilitation therapies for muscle-specific injuries or deficits.

}, url = {https://journals.biologists.com/jeb/article/224/3/jeb228221/223443/Lower-limb-muscle-function-is-influenced-by}, author = {Lai, Adrian and Dick, T. J. M. and Brown, Nicholas A. T. and Biewener, A. A. and Wakeling, J. M.} } @article {1443478, title = {Task-dependent recruitment across ankle extensor muscles and between mechanical demands is driven by the metabolic cost of muscle contraction}, journal = {Journal of the Royal Society Interface}, volume = {18}, year = {2021}, abstract = {

Abstract

The nervous system is faced with numerous strategies for recruiting a large number of motor units within and among muscle synergists to produce and control body movement. This is challenging, considering multiple combinations of motor unit recruitment may result in the same movement. Yet vertebrates are capable of performing a wide range of movement tasks with different mechanical demands. In this study, we used an experimental human cycling paradigm and musculoskeletal simulations to test the theory that a strategy of prioritizing the minimization of the metabolic cost of muscle contraction, which improves mechanical efficiency, governs the recruitment of motor units within a muscle and the coordination among synergist muscles within the limb. Our results support our hypothesis, for which measured muscle activity and model-predicted muscle forces in soleus{\textemdash}the slower but stronger ankle plantarflexor{\textemdash}is favoured over the weaker but faster medial gastrocnemius (MG) to produce plantarflexor force to meet increased load demands. However, for faster-contracting speeds induced by faster-pedalling cadence, the faster MG is favoured. Similar recruitment patterns were observed for the slow and fast fibres within each muscle. By contrast, a commonly used modelling strategy that minimizes muscle excitations failed to predict force sharing and known physiological recruitment strategies, such as orderly motor unit recruitment. Our findings illustrate that this common strategy for recruiting motor units within muscles and coordination between muscles can explain the control of the plantarflexor muscles across a range of mechanical demands.

}, url = {https://royalsocietypublishing.org/doi/10.1098/rsif.2020.0765}, author = {Lai, Adrian and Dick, T. J. M. and Biewener, A. A. and Wakeling, J. M.} } @article {1443474, title = {Modeling muscle function using experimentally determined subject-specific muscle properties}, journal = {Journal of Biomechanics}, volume = {117}, year = {2021}, abstract = {

Abstract

Muscle models are commonly based on intrinsic properties pooled across a number of individuals, often from a different species, and rarely validated against directly measured muscle forces. Here we use a rich data set of rat medial\ gastrocnemius muscle\ forces recorded during\ in-situ\ and\ in-vivo\ isometric, isotonic, and cyclic contractions to test the accuracy of forces predicted using Hill-type muscle models. We identified force-length and force-velocity parameters for each individual, and used either these subject-specific intrinsic properties, or population-averaged properties within the models. The modeled forces for cyclic\ in-vivo\ and\ in-situ\ contractions matched with measured muscle-tendon forces with\ r2\ between 0.70 and 0.86, and root-mean square errors (RMSE) of 0.10 to 0.13 (values normalized to the maximum isometric force). The modeled forces were least accurate at the highest movement and cycle frequencies and did not show an improvement in\ r2\ when subject-specific intrinsic properties were used; however, there was a reduction in the RMSE with fewer predictions having higher errors. We additionally recorded and tested muscle models specific to proximal and distal regions of the muscle and compared them to measures and models from the whole muscle belly: there was no improvement in model performance when using data from specific anatomical regions. These results show that Hill-type muscle models can yield very good performance for cyclic contractions typical of locomotion, with small reductions in errors when subject-specific intrinsic properties are used.

}, url = {doi.org/10.1016/j.jbiomech.2021.110242}, author = {Biewener, A. A. and Wakeling, J. M. and N. Konow} } @article {1443263, title = {Effect of muscle stimulation intensity on the heterogeneous function of compartments within an architecturally complex muscle}, journal = {Journal of Applied Physiology}, volume = {130}, year = {2021}, pages = {941-951}, abstract = {

Skeletal muscle has fiber architectures ranging from simple to complex, alongside variations in fiber-type and neuro-anatomical compartmentalization. However, the functional implications of muscle subdivision into discrete functional units remain poorly understood. The rat medial gastrocnemius has well-characterized regions with distinct architectures and fiber type composition. Here, force-length and force-velocity contractions were performed for two stimulation intensities (supramaximal and submaximal) and for three structural units (whole muscle belly, proximal region, and distal region) to assess the effect of muscle compartmentalization on contractile force-length-velocity relationships and optimal speed for power production. Additionally, fiber strain, fiber rotation, pennation, and architectural gearing were quantified. Our results suggest that the proximal and distal muscle regions have fundamentally different physiological function. During supramaximal activation, the proximal region has shorter (8.4 {\textpm} 0.8 mm versus 10.9 {\textpm} 0.7 mm) fibers and steeper (28.7 {\textpm} 11.0{\textdegree} versus 19.6 {\textpm} 6.3{\textdegree}) fiber angles at optimum length, and operates over a larger (17.9 {\textpm} 3.8\% versus 12.6 {\textpm} 2.7\%) range of its force-length curve. The proximal region also exhibits larger changes in pennation angle (5.6 {\textpm} 2.2{\textdegree}/mm versus 2.4 {\textpm} 1.5{\textdegree}/mm muscle shortening) and architectural gearing (1.82 {\textpm} 0.53 versus 1.25 {\textpm} 0.24), whereas the distal region exhibits greater peak shortening speed (96.0 mm/s versus 81.3 mm/s) and 18-27\% greater optimal speed. Overall, similar patterns were observed during submaximal activation. These regional differences in physiological function with respect to the whole muscle highlight how variation in motor recruitment could fundamentally shift regional functional patterns within a single muscle, which likely has important implications for whole muscle force and work output in vivo.

NEW \& NOTEWORTHY We show that muscle compartmentalization can influence whole muscle contractile properties, with slower-fibered proximal rat medial gastrocnemius undergoing larger changes in pennation angle and architectural gearing, whereas the faster-fibered distal region achieves greater peak and optimal shortening velocity, and power output. Consequently, regional variation in motor recruitment can fundamentally influence functional patterns within a single muscle.

}, url = {https://doi.org/10.1152/japplphysiol.00514.2020}, author = {C. Tijs and Konow, N and Biewener, A. A.} } @article {1408144, title = {Added mass in rat plantaris muscle causes a reduction in mechanical work}, journal = {Journal of Experimental Biology}, volume = {223}, year = {2020}, abstract = {Most of what we know about whole muscle behaviour comes from experiments on single fibres or small muscles that are scaled up in size without considering the effects of the additional muscle mass. Previous modelling studies have shown that tissue inertia acts to slow the rate of force development and maximum velocity of muscle during shortening contractions and decreases the work and power per cycle during cyclic contractions; however, these results have not yet been confirmed by experiments on living tissue. Therefore, in this study we conducted\ in situ\ work-loop experiments on rat plantaris muscle to determine the effects of increasing the mass of muscle on mechanical work during cyclic contractions. We additionally simulated these experimental contractions using a mass-enhanced Hill-type model to validate our previous modelling work. We found that greater added mass resulted in lower mechanical work per cycle relative to the unloaded trials in which no mass was added to the muscle (P=0.041 for both 85 and 123\% increases in muscle mass). We additionally found that greater strain resulted in lower work per cycle relative to unloaded trials at the same strain to control for length change and velocity effects on the work output, possibly due to greater accelerations of the muscle mass at higher strains. These results confirm that tissue mass reduces muscle mechanical work at larger muscle sizes, and that this effect is likely amplified for lower activations.}, url = {https://journals.biologists.com/jeb/article/223/19/jeb224410/225839/Added-mass-in-rat-plantaris-muscle-causes-a}, author = {Ross, S. A. and Rimkus, B. and N. Konow and Biewener, A. A. and Wakeling, J. M.} } @article {1408143, title = {Aquatic and terrestrial takeoffs require different hindlimb kinematics and muscle function in mallard ducks}, journal = {Journal of Experimental Biology}, volume = {223}, year = {2020}, abstract = {

Mallard ducks are capable of performing a wide range of behaviors including nearly vertical takeoffs from both terrestrial and aquatic habitats. The hindlimb plays a key role during takeoffs from both media. However, because force generation differs in water versus on land, hindlimb kinematics and muscle function are likely modulated between these environments. Specifically, we hypothesize that hindlimb joint motion and muscle shortening are faster during aquatic takeoffs, but greater hindlimb muscle forces are generated during terrestrial takeoffs. In this study, we examined the hindlimb kinematics and\ in vivo\ contractile function of the lateral gastrocnemius (LG), a major ankle extensor and knee flexor, during takeoffs from water versus land in mallard ducks. In contrast to our hypothesis, we observed no change in ankle angular velocity between media. However, the hip and metatarsophalangeal joints underwent large excursions during terrestrial takeoffs but exhibited almost no motion during aquatic takeoffs. The knee extended during terrestrial takeoffs but flexed during aquatic takeoffs. Correspondingly, LG fascicle shortening strain, shortening velocity and pennation angle change were greater during aquatic takeoffs than during terrestrial takeoffs because of the differences in knee motion. Nevertheless, we observed no significant differences in LG stress or work, but did see an increase in muscle power output during aquatic takeoffs. Because differences in the physical properties of aquatic and terrestrial media require differing hindlimb kinematics and muscle function, animals such as mallards may be challenged to tune their muscle properties for movement across differing environments.

}, url = {https://journals.biologists.com/jeb/article/223/16/jeb223743/223634/Aquatic-and-terrestrial-takeoffs-require-different}, author = {Taylor-Burt, K. R. and Biewener, A. A.} } @article {1408141, title = {Functional morphology of the ankle extensor muscle-tendon units in the springhare Pedetes capensis shows convergent evolution with macropods for bipedal hopping locomotion}, journal = {Journal of Anatomy}, volume = {237}, year = {2020}, pages = {568-578}, abstract = {This study assesses the functional morphology of the ankle extensor muscle-tendon units of the springhare\ Pedetes capensis, an African bipedal hopping rodent, to test for convergent evolution with the Australian bipedal hopping macropods. We dissect and measure the gastrocnemius, soleus, plantaris, and flexor digitorum longus in 10 adult springhares and compare them against similar-sized macropods using phylogenetically informed scaling analyses. We show that springhares align reasonably well with macropod predictions, being statistically indistinguishable with respect to the ankle extensor mean weighted muscle moment arm (1.63 vs. 1.65\ cm, respectively), total muscle mass (41.1 vs. 29.2\ g), total muscle physiological cross-sectional area (22.9 vs. 19.3 cm2), mean peak tendon stress (26.2 vs. 35.2\ MPa), mean tendon safety factor (4.7 vs. 3.6), and total tendon strain energy return capacity (1.81 vs. 1.82\ J). However, total tendon cross-sectional area is significantly larger in springhares than predicted for a similar-sized macropod (0.26 vs. 0.17 cm2, respectively), primarily due to a greater plantaris tendon thickness (0.084 vs. 0.048 cm2), and secondarily because the soleus muscle-tendon unit is present in springhares but is vestigial in macropods. The overall similarities between springhares and macropods indicate that evolution has favored comparable lower hindlimb body plans for bipedal hopping locomotion in the two groups of mammals that last shared a common ancestor ~160 million years ago. The springhare{\textquoteright}s relatively thick plantaris tendon may facilitate rapid transfer of force from muscle to skeleton, enabling fast and accelerative hopping, which could help to outpace and outmaneuver predators.}, author = {Veiga, Gabriela N. and Biewener, A. A. and Fuller, A. and van de Ven, T. M. F. N. and McGowan, C. P. and Panaino, W. and Snelling, E. P.} } @article {1408139, title = {Tuning of feedforward control enables stable muscle force-length dynamics after loss of autogenic proprioceptive feedback}, journal = {eLife}, year = {2020}, abstract = {Animals must integrate feedforward, feedback and intrinsic mechanical control mechanisms to maintain stable locomotion. Recent studies of guinea fowl (Numida meleagris) revealed that the distal leg muscles rapidly modulate force and work output to minimize perturbations in uneven terrain. Here we probe the role of reflexes in the rapid perturbation responses of muscle by studying the effects of proprioceptive loss. We induced bilateral loss of autogenic proprioception in the lateral gastrocnemius muscle (LG) using self-reinnervation. We compared in vivo muscle dynamics and ankle kinematics in birds with reinnervated and intact LG. Reinnervated and intact LG exhibit similar steady state mechanical function and similar work modulation in response to obstacle encounters. Reinnervated LG exhibits 23ms earlier steady-state activation, consistent with feedforward tuning of activation phase to compensate for lost proprioception. Modulation of activity duration is impaired in rLG, confirming the role of reflex feedback in regulating force duration in intact muscle.}, url = {https://elifesciences.org/articles/53908}, author = {Gordon, J. C. and Holt, N. C. and Biewener, A. A. and Daley, M. A.} } @article {1306771, title = {Skeletal Muscle Shape Change in Relation to Varying Force Requirements Across Locomotor Conditions}, journal = {Frontiers in Physiology}, volume = {11}, year = {2020}, abstract = {Contractions of skeletal muscles to generate\ in vivo\ movement involve dynamic changes in contractile and elastic tissue strains that likely interact to influence the force and work of a muscle. However, studies of the\ in vivo\ dynamics of skeletal muscle and tendon strains remain largely limited to bipedal animals, and rarely cover the broad spectra of movement requirements met by muscles that operate as motors, struts, or brakes across the various gaits that animals commonly use and conditions they encounter. Using high-speed bi-planar fluoromicrometry, we analyze\ in vivo\ strains within the rat medial gastrocnemius (MG) across a range of gait and slope conditions. These conditions require changes in muscle force ranging from decline walk (low) to incline gallop (high). Measurements are made from implanted (0.5{\textendash}0.8 mm) tantalum spheres marking MG mid-belly width, mid-belly thickness, as well as strains of distal fascicles, the muscle belly, and the Achilles tendon. During stance, as the muscle contracts, muscle force increases linearly with respect to gait{\textendash}slope combinations, and both shortening and lengthening fiber strains increase from approximately 5 to 15\% resting length. Contractile change in muscle thickness (thickness strain) decreases (r2\ = 0.86;\ p\ = 0.001); whereas, the change in muscle width (width strain) increases (r2\ = 0.88;\ p\ = 0.001) and tendon strain increases (r2\ = 0.77;\ p\ = 0.015). Our results demonstrate force-dependency of contractile and tendinous tissue strains with compensatory changes in shape for a key locomotor muscle in the hind limb of a small quadruped. These dynamic changes are linked to the ability of a muscle to tune its force and work output as requirements change with locomotor speed and environmental conditions.}, url = {https://www.frontiersin.org/articles/10.3389/fphys.2020.00143/full}, author = {Konow, N and Collias, A and Biewener, A. A.} } @article {1306758, title = {Elastic recoil action amplifies jaw closure in an aquatic-feeding salamander}, journal = {Proceedings of the Royal Society Ser. B}, volume = {287}, year = {2020}, url = {https://royalsocietypublishing.org/doi/10.1098/rspb.2020.0428}, author = {Rull, M and Solomon, J and Konow, N} } @article {1306755, title = {Post-activation muscle potentiation and its relevance to cyclical behaviours}, journal = {Biol. Letters}, volume = {16}, year = {2020}, pages = {1-6}, abstract = {Muscle can experience post-activation potentiation (PAP), a temporary increase in force and rate of force development, when contractions are closely timed; therefore, cyclical behaviours are likely affected by PAP, as succeeding contraction cycles can lead to potentiation over several subsequent cycles. Here, we examined PAP during\ in situ\ cyclical contractions of the mallard lateral gastrocnemius (LG). Surface swimming, a cyclical behaviour, was mimicked with work-loops using\ in vivo\ LG length change and stimulation parameters. Tests were performed at mallards{\textquoteright} preferred cycle frequency as well as at lower and higher frequencies. Like muscles from mammals, anurans and arthropods, the mallard LG exhibited PAP with increases in peak force, average force rate and net work. Staircase potentiation occurred over two or more work-loop cycles, resulting in gradual increases in PAP. The number of cycles needed to reach maximum work varied with cycle frequency, requiring more cycles at higher cycle frequencies. PAP occurred under\ in vivo-like stimulation parameters, suggesting a potentially important role of PAP in animal locomotion, especially in cyclical behaviours.}, url = {https://royalsocietypublishing.org/doi/10.1098/rsbl.2020.0255}, author = {Taylor-Burt, K and Konow, N and Biewener, A. A.} } @article {1280396, title = {The Reliability of Foot and Ankle Bone and Joint Kinematics Measured With Biplanar Videoradiography and Manual Scientific Rotoscoping}, journal = {Frontiers in Bioengineering and Biotechnology}, year = {2020}, abstract = {The intricate motion of the small bones of the feet are critical for its diverse function. Accurately measuring the 3-dimensional (3D) motion of these bones has attracted much attention over the years and until recently, was limited to invasive techniques or quantification of functional segments using multi-segment foot models. Biplanar videoradiography and model-based scientific rotoscoping offers an exciting alternative that allows us to focus on the intricate motion of individual bones in the foot. However, scientific rotoscoping, the process of rotating and translating a 3D bone model so that it aligns with the captured x-ray images, is either semi- or completely manual and it is unknown how much human error affects tracking results. Thus, the aim of this study was to quantify the inter- and intra-operator reliability of manually rotoscoping\ in vivo\ bone motion of the tibia, talus, and calcaneus during running. Three-dimensional CT bone volumes and high-speed biplanar videoradiography images of the foot were acquired on six participants. The six-degree-of-freedom motions of the tibia, talus, and calcaneus were determined using a manual markerless registration algorithm. Two operators performed the tracking, and additionally, the first operator re-tracked all bones, to test for intra-operator effects. Mean RMS errors were 1.86 mm and 1.90{\textdegree} for intra-operator comparisons and 2.30 mm and 2.60{\textdegree} for inter-operator comparisons across all bones and planes. The moderate to strong similarity values indicate that tracking bones and joint kinematics between sessions and operators is reliable for running. These errors are likely acceptable for defining gross joint angles. However, this magnitude of error may limit the capacity to perform advanced analyses of joint interactions, particularly those that require precise (sub-millimeter) estimates of bone position and orientation. Optimizing the view and image quality of the biplanar videoradiography system as well as the automated tracking algorithms for rotoscoping bones in the foot are required to reduce these errors and the time burden associated with the manual processing.}, url = {https://www.frontiersin.org/articles/10.3389/fbioe.2020.00106/full}, author = {Jayshini, N M and Kessler, S and Rainbow, M J and D{\textquoteright}Andrea, S E and Konow, N and Kelly, L and Lichtwark, G A} } @article {1280395, title = {A salamander that chews with complex, three-dimensional mandible movements }, journal = {Journal of Experimental Biology}, year = {2020}, abstract = {It is generally accepted that most non-mammal tetrapods have a hinge-like jaw operation restricted to vertical opening and closing movements. Many mammal jaw joints, by contrast, operate in more complex, three-dimensional ways, involving not only vertical, but also propalinal (rostro-caudal) and transverse (lateral) movements. Data on intraoral food processing in lissamphibians and sauropsids has prompted a generally accepted view that these groups mostly swallow food unreduced, and that in those cases where lissamphibians and sauropsids chew, they mostly use simple vertical jaw movements for food processing. The exception to that generally accepted view being some propalinal chewing in sauropsids. We combined 3D kinematics and morphological analyses from biplanar high-speed video fluoroscopy and micro-CT to determine how the paedomorphic salamander Siren intermedia treats captured food. We discovered that S. intermedia not only uses intraoral food processing, but that the elaborated morphology of its jaw joint facilitates mandibular motions in all three planes, resulting in complex three-dimensional chewing. Thus, our data challenge the commonly held view that complex three-dimensional chewing movements are exclusive to mammals, by suggesting that complex chewing mechanisms might evolved early in tetrapod evolution.}, url = {https://jeb.biologists.org/content/early/2020/01/25/jeb.220749}, author = {Schwarz, D and Konow, N and Roba, Y T and Heiss, E.} } @article {1280386, title = {Modulation of Flight Muscle Recruitment and Wing Rotation Enables Hummingbirds to Mitigate Aerial Roll Perturbations}, journal = {Current Biology}, volume = {30}, year = {2020}, pages = {187-195.e4}, abstract = {Both biological and artificial fliers must contend with aerial perturbations that are ubiquitous in the outdoor environment. Flapping fliers are generally least stable, but also the most maneuverable in roll, yet roll control in biological fliers remains less well understood. Hummingbirds are suitable models for linking aerodynamic perturbations to flight control strategies, as these small, powerful fliers are capable of remaining airborne even in adverse airflows. We challenged hummingbirds to fly within a longitudinally oriented vortex that imposed a continuous roll perturbation, measured wing kinematics and neuromotor activation of the major flight muscles with synchronized high-speed video and electromyography and used computational fluid dynamics (CFD) to estimate the aerodynamic forces generated by wing motions. Hummingbirds responded to the perturbation using bilaterally different activation of the main flight muscles and maintained symmetry in most major aspects of wing motion including stroke amplitude, stroke plane angle, and flapping frequency. However, hummingbirds also displayed consistent bilateral differences in subtle wing kinematics traits, including wing rotation and elevation. CFD modeling implicate asymmetric responses in wing rotation as important for generating the necessary stabilizing torques, suggesting that intrinsic wing muscles play a critical role in aerodynamic control. The birds also augment flight stabilization by adjusting body and tail posture to expose greater surface area to upwash than to the undesirable downwash. Our results provide insight into the remarkable capacity of hummingbirds to maintain flight control and bio-inspiration for simple yet effective control strategies for robotic fliers to contend with unfamiliar and challenging real-word aerial conditions.}, url = {https://www.sciencedirect.com/science/article/pii/S0960982219314642?via\%3Dihub}, author = {Ravi, Sridhar and Noda, Ryusuke and Gagliardi, Susie and Kolomenskiy, Dmitry and Combes, Stacey and Liu, Hao and Biewener, Andrew and Konow, Nicolai} } @article {1280383, title = {Broad similarities in shoulder muscle architecture and organization across two amniotes: implications for reconstructing non-mammalian synapsids}, journal = {PeerJ}, volume = {8}, year = {2020}, abstract = {The evolution of upright limb posture in mammals may have enabled modifications of the forelimb for diverse locomotor ecologies. A rich fossil record of non-mammalian synapsids holds the key to unraveling the transition from {\textquotedblleft}sprawling{\textquotedblright} to {\textquotedblleft}erect{\textquotedblright} limb function in the precursors to mammals, but a detailed understanding of muscle functional anatomy is a necessary prerequisite to reconstructing postural evolution in fossils. Here we characterize the gross morphology and internal architecture of muscles crossing the shoulder joint in two morphologically-conservative extant amniotes that form a phylogenetic and morpho-functional bracket for non-mammalian synapsids: the Argentine black and white tegu Salvator merianae and the Virginia opossum Didelphis virginiana. By combining traditional physical dissection of cadavers with nondestructive three-dimensional digital dissection, we find striking similarities in muscle organization and architectural parameters. Despite the wide phylogenetic gap between our study species, distal muscle attachments are notably similar, while differences in proximal muscle attachments are driven by modifications to the skeletal anatomy of the pectoral girdle that are well-documented in transitional synapsid fossils. Further, correlates for force production, physiological cross-sectional area (PCSA), muscle gearing (pennation), and working range (fascicle length) are statistically indistinguishable for an unexpected number of muscles. Functional tradeoffs between force production and working range reveal muscle specializations that may facilitate increased girdle mobility, weight support, and active stabilization of the shoulder in the opossum{\textemdash}a possible signal of postural transformation. Together, these results create a foundation for reconstructing the musculoskeletal anatomy of the non-mammalian synapsid pectoral girdle with greater confidence, as we demonstrate by inferring shoulder muscle PCSAs in the fossil non-mammalian cynodont Massetognathus pascua}, url = {https://doi.org/10.7717/peerj.8556}, author = {Fahn-Lai, Philip and Biewener, Andrew A and Pierce, Stephanie E} } @article {1280389, title = {Goats Decrease Hindlimb Stiffness When Walking Over Compliant Surfaces}, journal = {Journal of Experimental Biology}, year = {2019}, abstract = {Leg stiffness, commonly estimated as the {\textquoteright}compression{\textquoteright} of a defined leg element in response to a load, has long been used to characterize terrestrial locomotion. This study investigated how goats adjust the stiffness of their hindlimbs to accommodate surfaces of different stiffness. Goats provide a compelling animal model for studying leg stiffness modulation, because they skillfully ambulate over a range of substrates that vary in compliance. To investigate the adjustments that goats make when walking over such substrates, ground reaction forces and three-dimensional trajectories of hindlimb markers were recorded as goats walked on rigid, rubber and foam surfaces. Net joint moments, power and work at the hip, knee, ankle and metatarsophalangeal joints were estimated throughout stance via inverse dynamics. Hindlimb stiffness was estimated from plots of total leg force versus total leg length, and individual joint stiffness was estimated from plots of joint moment versus joint angle. Our results support the hypothesis that goats modulate hindlimb stiffness in response to surface stiffness; specifically, hindlimb stiffness decreased on the more compliant surfaces (P\<0.002). Estimates of joint stiffness identified hip and ankle muscles as the primary drivers of these adjustments. When humans run on compliant surfaces, they generally increase leg stiffness to preserve their center-of-mass mechanics. We did not estimate center-of-mass mechanics in this study; nevertheless, our estimates of hindlimb stiffness suggest that goats exhibit a different behavior. This study offers new insight into mechanisms that allow quadrupeds to modulate their gait mechanics when walking on surfaces of variable compliance.}, author = {Clites, T. R. and Arnold, A. S. and Singh, N. M. and Kline, E. and H.Chen and Tugman, C. and Billadeau, B. and Biewener, A. A. and Herr, H. M.} } @article {1280388, title = {In vivo force{\textendash}length and activation dynamics of two distal rat hindlimb muscles in relation to gait and grade}, journal = {Journal of Experimental Biology}, year = {2019}, abstract = {Muscle function changes to meet the varying mechanical demands of locomotion across different gait and grade conditions. A muscle{\textquoteright}s work output is determined by time-varying patterns of neuromuscular activation, muscle force and muscle length change, but how these patterns change under different conditions in small animals is not well defined. Here, we report the first integrated in vivo force{\textendash}length and activation patterns in rats, a commonly used small animal model, to evaluate the dynamics of two distal hindlimb muscles (medial gastrocnemius and plantaris) across a range of gait (walk, trot and gallop) and grade (level and incline) conditions. We use these data to explore how the pattern of force production, muscle activation and muscle length changes across conditions in a small quadrupedal mammal. As hypothesized, we found that the rat muscles show limited fascicle strains during active force generation in stance across gaits and grades, indicating that these distal rat muscles generate force economically but perform little work, similar to patterns observed in larger animals during level locomotion. Additionally, given differences in fiber type composition and variation in motor unit recruitment across the gait and grade conditions examined here for these muscles, the in vivo force{\textendash}length behavior and neuromuscular activation data reported here can be used to validate improved two-element Hill-type muscle models.}, url = {https://jeb.biologists.org/content/222/24/jeb205559.abstract}, author = {Eng, Carolyn M and Konow, Nicolai and Tijs, Chris and Holt, Natalie C and Biewener, Andrew A} } @article {1224399, title = {Muscle-specific indices to characterise the functional behavior of human lower-limb muscles during locomotion }, journal = {Journal of Biomechanics}, volume = {89}, year = {2019}, pages = {134-138}, url = {https://www.sciencedirect.com/science/article/pii/S002192901930291X?via\%3Dihub}, author = {Lai, A. and Biewener, A. A. and Wakeling, J. M.} } @article {1224391, title = {The evolution of a single toe in horses: causes, consequences, and the way forward}, journal = {Integrative \& Compartive Biology}, volume = {icz050}, year = {2019}, pages = {1-18}, url = {https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icz050/5498567}, author = {McHorse, B. K. and Biewener, A. A. and Pierce, S. E.} } @article {1223563, title = {A Direct Comparison of Biplanar Videoradiography and Optical Motion Capture for Foot and Ankle Kinematics}, journal = {Frontiers in Bioengineering and Biotechnology }, volume = {7}, year = {2019}, pages = {1-10}, abstract = {Measuring motion of the human foot presents a unique challenge due to the large number of closely packed bones with congruent articulating surfaces. Optical motion capture (OMC) and multi-segment models can be used to infer foot motion, but might be affected by soft tissue artifact (STA). Biplanar videoradiography (BVR) is a relatively new tool that allows direct, non-invasive measurement of bone motion using high-speed, dynamic x-ray images to track individual bones. It is unknown whether OMC and BVR can be used interchangeably to analyse multi-segment foot motion. Therefore, the aim of this study was to determine the agreement in kinematic measures of dynamic activities. Nine healthy participants performed three walking and three running trials while BVR was recorded with synchronous OMC. Bone position and orientation was determined through manual scientific-rotoscoping. The OMC and BVR kinematics were co-registered to the same coordinate system, and BVR tracking was used to create virtual markers for comparison to OMC during dynamic trials. Root mean square (RMS) differences in marker positions and joint angles as well as a linear fit method (LFM) was used to compare the outputs of both methods. When comparing BVR and OMC, sagittal plane angles were in good agreement (ankle: R2 = 0.947, 0.939; Medial Longitudinal Arch (MLA) Angle: R2 = 0.713, 0.703, walking and running, respectively). When examining the ankle, there was a moderate agreement between the systems in the frontal plane (R2 = 0.322, 0.452, walking and running, respectively), with a weak to moderate correlation for the transverse plane (R2 = 0.178, 0.326, walking and running, respectively). However, root mean squared error (RMSE) showed angular errors ranging from 1.06 to 8.31{\textdegree} across the planes (frontal: 3.57{\textdegree}, 3.67{\textdegree}, transverse: 4.28{\textdegree}, 4.70{\textdegree}, sagittal: 2.45{\textdegree}, 2.67{\textdegree}, walking and running, respectively). Root mean square (RMS) differences between OMC and BVR marker trajectories were task dependent with the largest differences in the shank (6.0 {\textpm} 2.01 mm) for running, and metatarsals (3.97 {\textpm} 0.81 mm) for walking. Based on the results, we suggest BVR and OMC provide comparable solutions to foot motion in the sagittal plane, however, interpretations of out-of-plane movement should be made carefully.}, url = {https://www.frontiersin.org/articles/10.3389/fbioe.2019.00199/full$\#$h1}, author = {Kessler, S E and Rainbow, M J and Lichtwark, G A and Cresswell, A G and D{\textquoteright}Andrea, S E and Konow, N and Kelly, L A} } @article {1223560, title = {Eye Movements in Frogs and Salamanders{\textemdash}Testing the Palatal Buccal Pump Hypothesis}, journal = {Integrative Organismal Biology }, volume = {1}, year = {2019}, abstract = {In frogs and salamanders, movements of the eyeballs in association with an open palate have often been proposed to play a functional role in lung breathing. In this {\textquotedblleft}palatal buccal pump,{\textquotedblright} the eyeballs are elevated during the lowering of the buccal floor to suck air in through the nares, and the eyeballs are lowered during elevation of the buccal floor to help press air into the lungs. Here, we used X-Ray Reconstruction of Moving Morphology to investigate eye movements during lung breathing and feeding in bullfrogs and axolotls. Our data do not show eye movements that would be in accordance with the palatal buccal pump. On the contrary, there is a small passive elevation of the eyeballs when the buccal floor is raised. Inward drawing of the eyeballs occurs only during body motion and for prey transport in bullfrogs, but this was not observed in axolotls. Each eye movement in bullfrogs has a vertical, a mediolateral, and an anteroposterior component. Considering the surprisingly weak posterior motion component of the eyeballs, their main role in prey transport might be fixing the prey by pressing it against the buccal floor. The retraction of the buccal floor would then contribute to the posterior push of the prey. Because our study provides no evidence for a palatal buccal pump in frogs and salamanders, there is also no experimental support for the idea of a palatal buccal pump in extinct temnospondyl amphibians, in contrast to earlier suggestions.}, url = {https://academic.oup.com/iob/article/1/1/obz011/5512359}, author = {Witzmann, F and Brainerd, E. L. and Konow, N} } @article {1166605, title = {Evidence of a tunable biological spring: Elastic energy storage in aponeuroses varies with transverse strain in vivo}, journal = {Proceedings of Royal Society Series B}, volume = {286}, year = {2019}, pages = {20182764}, url = {https://royalsocietypublishing.org/doi/10.1098/rspb.2018.2764}, author = {Arellano, C. and N. Konow and Gidmark, N. and Roberts, T. J.} } @article {1166600, title = {How moles destroy your lawn: the forelimb kinematics of Eastern moles in loose and compact substrates}, journal = {Journal of Experimental Biology}, volume = {222}, year = {2019}, url = {http://jeb.biologists.org/content/222/4/jeb182436}, author = {Lin, Y. and N. Konow and Dumont, E. R.} } @article {1166599, title = {Chewing or not? Intraoral food processing in a salamandrid newt}, journal = {Journal of Experimental Biology}, volume = {222}, year = {2019}, note = {PhysOrg, TDnews, ScienceDaily, InnovationsReport, Stern (DE), Eurekalert. Featured Article: InsideJEB}, url = {http://jeb.biologists.org/content/222/6/jeb189886}, author = {Heiss, E. and Schwartz, D. and N. Konow} } @article {1166598, title = {Goats decrease hindlimb stiffness when walking over compliant surfaces}, journal = {Journal of Experimental Biology}, volume = {222}, year = {2019}, url = {http://jeb.biologists.org/content/222/10/jeb198325}, author = {Clites, T. R. and Arnold, A. S. and Singh, N. M. and H.Chen and Tugman, C. and Billadeau, B. and Biewener, A. A. and Herr, H. M.} } @article {1166404, title = {Muscle-specific indices to characterise the functional behaviours of human lower limb muscles during locomotion}, journal = {Journal of Biomechanics}, volume = {89}, year = {2019}, pages = {134-138}, author = {Lai, A. and Biewener, A. A. and Wakeling, J. M.} } @article {1157963, title = {Animal Locomotion: Near-Ground Low-Cost Flights}, journal = {Curr. Biol.}, volume = {28}, year = {2018}, pages = {R1348-R1349}, url = {https://www.sciencedirect.com/science/article/pii/S0960982218313423?via\%3Dihub}, author = {Biewener, A. A.} } @article {1157962, title = {Metabolic cost underlies task-dependent variations in motor unit recruitment}, journal = {J. Roy. Soc. Interface}, volume = {15}, year = {2018}, url = {https://royalsocietypublishing.org/doi/10.1098/rsif.2018.0541}, author = {Lai, A. and Biewener, A. A. and Wakeling, J. M.} } @article {1157958, title = {Foot-propelled swimming kinematics and turning strategies in common loons}, journal = {J. exp. Biol.}, volume = {221}, year = {2018}, pages = {1-11}, url = {http://jeb.biologists.org/content/221/19/jeb168831}, author = {Clifton, G. T. and Biewener, A. A.} } @article {1157955, title = {Different segments within vertebrate muscles can operate on different regions of their force-length relationships}, journal = {Int. Comp. Biol.}, volume = {58}, year = {2018}, pages = {219-231}, url = {https://academic.oup.com/icb/article/58/2/219/5034474}, author = {Ahn, A. N. and N. Konow and C. Tijs and Biewener, A. A.} } @article {1157326, title = {Evolutionary race as predators hunt prey}, journal = {Nature}, volume = {554}, year = {2018}, pages = {176-178}, url = {https://www.nature.com/magazine-assets/d41586-018-01278-w/d41586-018-01278-w.pdf}, author = {Biewener, A. A.} } @article {1125742, title = {Three-dimensional mobility and muscle attachments in the pectoral limb of the Triassic cynodont Massetognathus pascuali (Romer, 1967)}, journal = {Journal of Anatomy}, volume = {232}, year = {2018}, pages = {383-406}, abstract = {The musculoskeletal configuration of the mammalian pectoral limb has been heralded as a key anatomical feature leading to the adaptive radiation of mammals, but limb function in the non-mammaliaform cynodont outgroup remains unresolved. Conflicting reconstructions of abducted and adducted posture are based on mutually incompatible interpretations of ambiguous osteology. We reconstruct the pectoral limb of the Triassic non-mammaliaform cynodont Massetognathus pascuali in three dimensions, by combining skeletal morphology from micro-computed tomography with muscle anatomy from an extended extant phylogenetic bracket. Conservative tests of maximum range of motion suggest a degree of girdle mobility, as well as substantial freedom at the shoulder and the elbow joints. The glenoid fossa supports a neutral pose in which the distal end of the humerus points 45{\textdegree} posterolaterally from the body wall, intermediate between classically {\textquoteleft}sprawling{\textquoteright} and {\textquoteleft}parasagittal{\textquoteright} limb postures. Massetognathus pascuali is reconstructed as having a near-mammalian complement of shoulder muscles, including an incipient rotator cuff (m.\ subscapularis, m.\ infraspinatus, m.\ supraspinatus, and m.\ teres minor). Based on close inspection of the morphology of the glenoid fossa, we hypothesize a posture-driven scenario for the evolution of the therian ball-and-socket shoulder joint. The musculoskeletal reconstruction presented here provides the anatomical scaffolding for more detailed examination of locomotor evolution in the precursors to mammals.}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/joa.12766 }, author = {Lai, Phil H. and Biewener, Andrew A and Pierce, SE} } @article {1114907, title = {Does a two-element muscle model offer advantages when estimating ankle plantar flexor forces during human cycling?}, journal = {Journal of Biomechanics}, volume = {68}, year = {2018}, pages = {6-13}, abstract = {Traditional Hill-type muscle models, parameterized using high-quality experimental data, are often {\textquotedblleft}too weak{\textquotedblright} to reproduce the joint torques generated by healthy adults during rapid, high force tasks. This study investigated whether the failure of these models to account for different types of motor units contributes to this apparent weakness; if so, muscle-driven simulations may rely on excessively high muscle excitations to generate a given force. We ran a series of forward simulations that reproduced measured ankle mechanics during cycling at five cadences ranging from 60 to 140 RPM. We generated both {\textquotedblleft}nominal{\textquotedblright} simulations, in which an abstract ankle model was actuated by a 1-element Hill-type plantar flexor with a single contractile element (CE), and {\textquotedblleft}test{\textquotedblright} simulations, in which the same model was actuated by a 2-element plantar flexor with two CEs that accounted for the force-generating properties of slower and faster motor units. We varied the total excitation applied to the 2-element plantar flexor between 60 and 105\% of the excitation from each nominal simulation, and we varied the amount distributed to each CE between 0 and 100\% of the total. Within this test space, we identified the excitation level and distribution, at each cadence, that best reproduced the plantar flexor forces generated in the nominal simulations. Our comparisons revealed that the 2-element model required substantially less total excitation than the 1-element model to generate comparable forces, especially at higher cadences. For instance, at 140 RPM, the required excitation was reduced by 23\%. These results suggest that a 2-element model, in which contractile properties are {\textquotedblleft}tuned{\textquotedblright} to represent slower and faster motor units, can increase the apparent strength and perhaps improve the fidelity of simulations of tasks with varying mechanical demands.}, url = {http://www.jbiomech.com/article/S0021-9290(17)30725-X/fulltext}, author = {Lai, Adrian and Arnold, Allison and Biewener, Andrew A and Dick, Taylor and Wakeling, James M} } @article {1078431, title = {Why are antagonist muscles co-activated in my simulation? A musculoskeletal model for analyzing human locomotor tasks}, journal = {Annals of Biomedical Engineering}, volume = {45}, year = {2017}, pages = {2762-2774}, abstract = {Existing "off-the-shelf" musculoskeletal models are problematic when simulating movements that involve substantial hip and knee flexion, such as the upstroke of pedalling, because they tend to generate excessive passive fibre force. The goal of this study was to develop a refined musculoskeletal model capable of simulating pedalling and fast running, in addition to walking, which predicts the activation patterns of muscles better than existing models. Specifically, we tested whether the anomalous co-activation of antagonist muscles, commonly observed in simulations, could be resolved if the passive forces generated by the underlying model were diminished. We refined the OpenSim{\texttrademark} model published by Rajagopal et al. (IEEE Trans Biomed Eng 63:1-1, 2016) by increasing the model{\textquoteright}s range of knee flexion, updating the paths of the knee muscles, and modifying the force-generating properties of eleven muscles. Simulations of pedalling, running and walking based on this model reproduced measured EMG activity better than simulations based on the existing model-even when both models tracked the same subject-specific kinematics. Improvements in the predicted activations were associated with decreases in the net passive moments; for example, the net passive knee moment during the upstroke of pedalling decreased from 36.9\ N\ m (existing model) to 6.3\ N\ m (refined model), resulting in a dramatic decrease in the co-activation of knee flexors. The refined model is available from SimTK.org and is suitable for analysing movements with up to 120{\textdegree} of hip flexion and 140{\textdegree} of knee flexion.}, url = {https://link.springer.com/article/10.1007/s10439-017-1920-7}, author = {Lai, AKM and Arnold, A. S. and Wakeling, J. M.} } @article {1076476, title = {Experimental determination of three-dimensional cervical joint mobility in the avian neck}, journal = {Frontiers in Zoology}, volume = {14}, year = {2017}, pages = {1-15}, abstract = {

Background

Birds have highly mobile necks, but neither the details of how they realize complex poses nor the evolution of this complex musculoskeletal system is well-understood. Most previous work on avian neck function has focused on dorsoventral flexion, with few studies quantifying lateroflexion or axial rotation. Such data are critical for understanding joint function, as musculoskeletal movements incorporate motion around multiple degrees of freedom simultaneously. Here we use biplanar X-rays on wild turkeys to quantify three-dimensional cervical joint range of motion in an avian neck to determine patterns of mobility along the cranial-caudal axis.

Results

Range of motion can be generalized to a three-region model: cranial joints are ventroflexed with high axial and lateral mobility, caudal joints are dorsiflexed with little axial rotation but high lateroflexion, and middle joints show varying amounts axial rotation and a low degree of lateroflexion. Nonetheless, variation within and between regions is high. To attain complex poses, substantial axial rotation can occur at joints caudal to the atlas/axis complex and zygapophyseal joints can reduce their overlap almost to osteological disarticulation. Degrees of freedom interact at cervical joints; maximum lateroflexion occurs at different dorsoventral flexion angles at different joints, and axial rotation and lateroflexion are strongly coupled. Further, patterns of joint mobility are strongly predicted by cervical morphology.

Conclusion

Birds attain complex neck poses through a combination of mobile intervertebral joints, coupled rotations, and highly flexible zygapophyseal joints. Cranial-caudal patterns of joint mobility are tightly linked to cervical morphology, such that function can be predicted by form. The technique employed here provides a repeatable protocol for studying neck function in a broad array of taxa that will be directly comparable. It also serves as a foundation for future work on the evolution of neck mobility along the line from non-avian theropod dinosaurs to birds.

Electronic supplementary material

The online version of this article (doi:10.1186/s12983-017-0223-z) contains supplementary material, which is available to authorized users.

Keywords: Function, Mobility, XROMM, Avian, Bird, Anatomy, Cervical, Neck, X-ray, Motion, Morphology
}, author = {Kambic, R. E. and Biewener, A. A. and Pierce, S. E.} } @article {1076471, title = {High-speed surface reconstruction of a flying bird using structured-light}, journal = {J. Exp. Biol.}, volume = {220}, year = {2017}, pages = {1956-1961}, abstract = {Birds fly effectively and maneuver nimbly by dynamically changing the shape of their wings during each wingbeat. These shape changes have yet to be quantified automatically at high temporal and spatial resolution. Therefore, we developed a custom 3D surface reconstruction method, which uses a high-speed camera to identify spatially encoded binary striped patterns that are projected on a flying bird. This non-invasive structured-light method allows automated 3D reconstruction of each stand-alone frame and can be extended to multiple views. We demonstrate this new technique by automatically reconstructing the dorsal surface of a parrotlet wing at 3200 fps during flapping flight. From this shape we analyze key parameters such as wing twist and angle of attack distribution. While our binary {\textquoteleft}single-shot{\textquoteright} algorithm is demonstrated by quantifying dynamic shape changes of a flying bird, it is generally applicable to moving animals, plants and deforming objects.}, author = {Deetjen, M. E. and Biewener, A. A. and Lentink, D.} } @article {1076466, title = {Mechanics of evolutionary digit reduction in fossil horses }, journal = {Proc. Roy. Soc. B.}, volume = {284}, year = {2017}, pages = {1-8}, abstract = {Digit reduction is a major trend that characterizes horse evolution, but its causes and consequences have rarely been quantitatively tested. Using beam analysis on fossilized centre metapodials, we tested how locomotor bone stresses changed with digit reduction and increasing body size across the horse lineage. Internal bone geometry was captured from 13 fossil horse genera that covered the breadth of the equid phylogeny and the spectrum of digit reduction and body sizes, from Hyracotherium to Equus. To account for the load-bearing role of side digits, a novel, continuous measure of digit reduction was also established{\textemdash}toe reduction index (TRI). Our results show that without accounting for side digits, three-toed horses as late as Parahippus would have experienced physiologically untenable bone stresses. Conversely, when side digits are modelled as load-bearing, species at the base of the horse radiation through Equus probably maintained a similar safety factor to fracture stress. We conclude that the centre metapodial compensated for evolutionary digit reduction and body mass increases by becoming more resistant to bending through substantial positive allometry in internal geometry. These results lend support to two historical hypotheses: that increasing body mass selected for a single, robust metapodial rather than several smaller ones; and that, as horse limbs became elongated, the cost of inertia from the side toes outweighed their utility for stabilization or load-bearing.}, author = {McHorse, B. K. and Biewener, A. A. and Pierce, S. E.} } @article {1076461, title = {Comparison of human gastrocnemius forces predicted by Hill-type muscle models and estimated from ultrasound images}, journal = {Journal of Experimental Biology}, volume = {220}, year = {2017}, pages = {1643-1653}, abstract = {Hill-type models are ubiquitous in the field of biomechanics, providing estimates of a muscle{\textquoteright}s force as a function of its activation state and its assumed force-length and force-velocity properties. However, despite their routine use, the accuracy with which Hill-type models predict the forces generated by muscles during submaximal, dynamic tasks remains largely unknown. This study compared human gastrocnemii forces predicted by Hill-type models to the forces estimated from ultrasound-based measures of tendon length changes and stiffness during cycling, over a range of loads and cadences. We tested both a traditional model, with one contractile element, and a differential model, with two contractile elements that accounted for independent contributions of slow and fast muscle fibres. Both models were driven by subject-specific, ultrasound-based measures of fascicle lengths, velocities, and pennation angles and by activation patterns of slow and fast muscle fibres derived from surface electromyographic recordings. The models predicted on average, 54 \% the time-varying gastrocnemii forces estimated from the ultrasound-based methods. However, differences between predicted and estimated forces were smaller under low speed-high activation conditions, with models able to predict nearly 80 \% of the gastrocnemii force over a complete pedal cycle. Additionally, the predictions from the Hill-type muscle models tested here showed that a similar pattern of force production could be achieved for most conditions with and without accounting for the independent contributions of different muscle fibre types.}, author = {Dick, T. J. M. and Biewener, A. A. and Wakeling, J. M.} } @article {1076451, title = {Rules to fly by: pigeons navigating horizontal obstacles limit steering by selecting gaps most aligned to their bearing}, journal = {Roy. Soc. Interface Focus}, volume = {7}, year = {2017}, abstract = {Flying animals must successfully contend with obstacles in their natural
environments. Inspired by the robust manoeuvring abilities of flying animals,
unmanned aerial systems are being developed and tested to improve flight
control through cluttered environments. We previously examined steering
strategies that pigeons adopt to fly through an array of vertical obstacles
(VOs). Modelling VO flight guidance revealed that pigeons steer towards
larger visual gaps when making fast steering decisions. In the present experiments,
we recorded three-dimensional flight kinematics of pigeons as they
flew through randomized arrays of horizontal obstacles (HOs). We found
that pigeons still decelerated upon approach but flew faster through a
denser array of HOs compared with the VO array previously tested. Pigeons
exhibited limited steering and chose gaps between obstacles most aligned to
their immediate flight direction, in contrast to VO navigation that favoured
widest gap steering. In addition, pigeons navigated past the HOs with more
variable and decreased wing stroke span and adjusted their wing stroke
plane to reduce contact with the obstacles. Variability in wing extension,
stroke plane and wing stroke path was greater during HO flight. Pigeons
also exhibited pronounced head movements when negotiating HOs, which
potentially serve a visual function. These head-bobbing-like movements
were most pronounced in the horizontal (flight direction) and vertical directions,
consistent with engaging motion vision mechanisms for obstacle
detection. These results show that pigeons exhibit a keen kinesthetic sense of
their body and wings in relation to obstacles. Together with aerodynamic flapping
flight mechanics that favours vertical manoeuvring, pigeons are able to
navigate HOs using simple rules, with remarkable success.}, author = {Ros, I. G. and Bhagavatula, P. S. and Lin, H. T. and Biewener, A. A.} } @article {1076156, title = {Vertical leaping mechanics of the Lesser Egyptian Jerboa reveal specialization for maneuverability rather than elastic energy storage}, journal = {Frontiers in Zoology}, volume = {14}, year = {2017}, pages = {1-12}, abstract = {

Background

Numerous historical descriptions of the Lesser Egyptian jerboa, Jaculus jaculus, a small bipedal mammal with elongate hindlimbs, make special note of their extraordinary leaping ability. We observed jerboa locomotion in a laboratory setting and performed inverse dynamics analysis to understand how this small rodent generates such impressive leaps. We combined kinematic data from video, kinetic data from a force platform, and morphometric data from dissections to calculate the relative contributions of each hindlimb muscle and tendon to the total movement.

Results

Jerboas leapt in excess of 10 times their hip height. At the maximum recorded leap height (not the maximum observed leap height), peak moments for metatarso-phalangeal, ankle, knee, and hip joints were 13.1, 58.4, 65.1, and 66.9 Nmm, respectively. Muscles acting at the ankle joint contributed the most work (mean 231.6 mJ / kg Body Mass) to produce the energy of vertical leaping, while muscles acting at the metatarso-phalangeal joint produced the most stress (peak 317.1 kPa). The plantaris, digital flexors, and gastrocnemius tendons encountered peak stresses of 25.6, 19.1, and 6.0 MPa, respectively, transmitting the forces of their corresponding muscles (peak force 3.3, 2.0, and 3.8 N, respectively). Notably, we found that the mean elastic energy recovered in the primary tendons of both hindlimbs comprised on average only 4.4\% of the energy of the associated leap.

Conclusions

The limited use of tendon elastic energy storage in the jerboa parallels the morphologically similar heteromyid kangaroo rat, Dipodomys spectabilis. When compared to larger saltatory kangaroos and wallabies that sustain hopping over longer periods of time, these small saltatory rodents store and recover less elastic strain energy in their tendons. The large contribution of muscle work, rather than elastic strain energy, to the vertical leap suggests that the fitness benefit of rapid acceleration for predator avoidance dominated over the need to enhance locomotor economy in the evolutionary history of jerboas.

Electronic supplementary material

The online version of this article (doi:10.1186/s12983-017-0215-z) contains supplementary material, which is available to authorized users.

Keywords: Jerboa, Inverse dynamics, Muscle-tendon stresses, Ricochetal bipedal locomotion
}, author = {Moore, T. Y. and Rivera, A. M. and Biewener, A. A.} } @article {1076126, title = {Unpredictability of escape trajectory explains predator evasion ability and microhabitat preference of desert rodents}, journal = {Nature Communications}, volume = {8}, year = {2017}, pages = {1-9}, abstract = {Mechanistically linking movement behaviors and ecology is key to understanding the adaptive evolution of locomotion. Predator evasion, a behavior that enhances fitness, may depend upon short bursts or complex patterns of locomotion. However, such movements are poorly characterized by existing biomechanical metrics. We present methods based on the entropy measure of randomness from Information Theory to quantitatively characterize the unpredictability of non-steady-state locomotion. We then apply the method by examining sympatric rodent species whose escape trajectories differ in dimensionality. Unlike the speed-regulated gait use of cursorial animals to enhance locomotor economy, bipedal jerboa (family Dipodidae) gait transitions likely enhance maneuverability. In field-based observations, jerboa trajectories are significantly less predictable than those of quadrupedal rodents, likely increasing predator evasion ability. Consistent with this hypothesis, jerboas exhibit lower anxiety in open fields than quadrupedal rodents, a behavior that varies inversely with predator evasion ability. Our unpredictability metric expands the scope of quantitative biomechanical studies to include non-steady-state locomotion in a variety of evolutionary and ecologically significant contexts.}, url = {https://www.nature.com/articles/s41467-017-00373-2}, author = {Moore, T. Y. and Cooper, K. L. and Biewener, A. A. and Vasudevan, R.} } @article {1076496, title = {Foraging at the edge of the world: low-altitude, high-speed maneuvering in barn swallows}, journal = {Phil. Trans. Roy. Soc.}, volume = {371}, year = {2016}, abstract = {While prior studies of swallow manoeuvering have focused on slow-speed flight and obstacle avoidance in still air, swallows survive by foraging at high speeds in windy environments. Recent advances in field-portable, high-speed video systems, coupled with precise anemometry, permit measures of high-speed aerial performance of birds in a natural state. We undertook the present study to test: (i) the manner in which barn swallows (Hirundo rustica) may exploit wind dynamics and ground effect while foraging and (ii) the relative importance of flapping versus gliding for accomplishing high-speed manoeuvers. Using multi-camera videography synchronized with wind-velocity measurements, we tracked coursing manoeuvers in pursuit of prey. Wind speed averaged 1.3{\textendash}2.0 m s-1 across the atmospheric boundary layer, exhibiting a shear gradient greater than expected, with instantaneous speeds of 0.02{\textendash}6.1 m s-1. While barn swallows tended to flap throughout turns, they exhibited reduced wingbeat frequency, relying on glides and partial bounds during maximal manoeuvers. Further, the birds capitalized on the near-earth wind speed gradient to gain kinetic and potential energy during both flapping and gliding turns; providing evidence that such behaviour is not limited to large, fixed-wing soaring seabirds and that exploitation of wind gradients by small aerial insectivores may be a significant aspect of their aeroecology.}, author = {Warrick, D. R. and Hedrick, T. L. and Biewener, A. A. and Crandell, K. E. and Tobalske, B. W.} } @article {1076491, title = {Optic flow stabilizes flight in ruby-throated hummingbirds}, journal = {J. Exp. Biol}, volume = {219}, year = {2016}, pages = {2443-2448}, abstract = {Flying birds rely on visual cues for retinal image stabilization by negating rotation-induced optic flow, the motion of the visual panorama across the retina, through corrective eye and head movements. In combination with vestibular and proprioceptive feedback, birds may also use visual cues to stabilize their body during flight. Here, we test whether artificially induced wide-field motion generated through projected visual patterns elicits maneuvers in body orientation and flight position, in addition to stabilizing vision. To test this hypothesis, we present hummingbirds flying freely within a 1.2 m cylindrical visual arena with a virtual surround rotated at different speeds about its vertical axis. The birds responded robustly to these visual perturbations by rotating their heads and bodies with the moving visual surround, and by adjusting their flight trajectories, following the surround. Thus, similar to insects, hummingbirds appear to use optic flow cues to control flight maneuvers as well as to stabilize their visual inputs.}, author = {Ros, I. G. and Biewener, A. A.} } @article {1076481, title = {Locomotion as an emergent property of muscle contractile dynamics}, journal = {J. Exp. Biol.}, volume = {219}, year = {2016}, pages = {285-294}, abstract = {Skeletal muscles share many common, highly conserved features of organization at the molecular and myofilament levels, giving skeletal muscle fibers generally similar and characteristic mechanical and energetic properties; properties well described by classical studies of muscle mechanics and energetics. However, skeletal muscles can differ considerably in architectural design (fiber length, pinnation, and connective tissue organization), as well as fiber type, and how they contract in relation to the timing of neuromotor activation and in vivo length change. The in vivo dynamics of muscle contraction is, therefore, crucial to assessing muscle design and the roles that muscles play in animal movement. Architectural differences in muscle{\textendash}tendon organization combined with differences in the phase of activation and resulting fiber length changes greatly affect the time-varying force and work that muscles produce, as well as the energetic cost of force generation. Intrinsic force{\textendash}length and force{\textendash}velocity properties of muscles, together with their architecture, also play important roles in the control of movement, facilitating rapid adjustments to changing motor demands. Such adjustments complement slower, reflex-mediated neural feedback control of motor recruitment. Understanding how individual fiber forces are integrated to whole-muscle forces, which are transmitted to the skeleton for producing and controlling locomotor movement, is therefore essential for assessing muscle design in relation to the dynamics of movement.}, author = {Biewener, A. A.} } @article {548496, title = {Hummingbird flight stability and control in freestream turbulent winds}, journal = {J Exp Biol}, year = {2015}, note = {

Ravi, SridharCrall, James DMcNeilly, LucasGagliardi, Susan FBiewener, Andrew ACombes, Stacey AENG2015/03/15 06:00J Exp Biol. 2015 Mar 12. pii: jeb.114553.

}, month = {Mar 12}, abstract = {

Airflow conditions close to the Earth{\textquoteright}s surface are often complex, posing challenges to flight stability and control for volant taxa. Relatively little is known about how well flying animals can contend with complex, adverse air flows, or about the flight-control mechanisms employed by animals to mitigate wind disturbances. Several recent studies have examined flight in the unsteady von Karman vortex streets that form behind cylinders, generating flow disturbances that are predictable in space and time; these structures are relatively rare in nature, as they occur only the immediate, downstream vicinity of an object. In contrast, freestream turbulence is characterized by rapid, unpredictable flow disturbances across a wide range of spatial and temporal scales, and is nearly ubiquitous in natural habitats. Hummingbirds are ideal organisms for studying the influence of freestream turbulence on flight, as they forage in a variety of aerial conditions and are powerful flyers. We filmed ruby-throated hummingbirds (A. colubris) maintaining position at a feeder in laminar and strongly turbulent (intensity approximately 15\%) airflow environments within a wind tunnel, and compared their mean head, body, tail and wing kinematics, as well as variability in these parameters. Hummingbirds exhibited remarkably stable head position and orientation in both smooth and turbulent flow while maintaining position at the feeder. However, the hummingbird{\textquoteright}s body was less stable in turbulent flow and appeared to be most sensitive to disturbances along the mediolateral axis, displaying large lateral accelerations, translations, and rolling motions during flight. The hummingbirds mitigated these disturbances by increasing mean wing stroke amplitude and stroke plane angle, and by varying these parameters asymmetrically between the wings, and from one stroke to the next. They also actively varied the orientation and fan angle of the tail, maintaining a larger mean fan angle when flying in turbulent flow; this may improve their passive stability, but likely incurs an energetic cost due to increased drag. Overall, we observed many of the same kinematic changes noted previously for hummingbirds flying in a von Karman vortex street, but we also observed kinematic changes associated with high force production, similar to those seen during load-lifting or high-speed flight. These findings suggest that flight may be particularly costly in fully mixed, freestream turbulence, the flow condition that hummingbirds are likely to encounter most frequently in natural habitats.

}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Ravi, S. and Crall, J. D. and McNeilly, L. and Gagliardi, S. F. and Biewener, A. A. and Combes, S.A.} } @article {548511, title = {Pigeons produce aerodynamic torques through changes in wing trajectory during low speed aerial turns}, journal = {J Exp Biol}, volume = {218}, number = {Pt 3}, year = {2015}, note = {

Ros, Ivo GBadger, Marc APierson, Alyssa NBassman, Lori CBiewener, Andrew AengEngland2014/12/03 06:00J Exp Biol. 2015 Feb 1;218(Pt 3):480-90. doi: 10.1242/jeb.104141. Epub 2014 Dec 1.

}, month = {Feb 1}, pages = {480-90}, abstract = {

The complexity of low speed maneuvering flight is apparent from the combination of two critical aspects of this behavior: high power and precise control. To understand how such control is achieved, we examined the underlying kinematics and resulting aerodynamic mechanisms of low speed turning flight in the pigeon (Columba livia). Three birds were trained to perform 90 deg level turns in a stereotypical fashion and detailed three-dimensional (3D) kinematics were recorded at high speeds. Applying the angular momentum principle, we used mechanical modeling based on time-varying 3D inertia properties of individual sections of the pigeon{\textquoteright}s body to separate angular accelerations of the torso based on aerodynamics from those based on inertial effects. Directly measured angular accelerations of the torso were predicted by aerodynamic torques, justifying inferences of aerodynamic torque generation based on inside wing versus outside wing kinematics. Surprisingly, contralateral asymmetries in wing speed did not appear to underlie the 90 deg aerial turns, nor did contralateral differences in wing area, angle of attack, wingbeat amplitude or timing. Instead, torso angular accelerations into the turn were associated with the outside wing sweeping more anteriorly compared with a more laterally directed inside wing. In addition to moving through a relatively more retracted path, the inside wing was also more strongly pronated about its long axis compared with the outside wing, offsetting any difference in aerodynamic angle of attack that might arise from the observed asymmetry in wing trajectories. Therefore, to generate roll and pitch torques into the turn, pigeons simply reorient their wing trajectories toward the desired flight direction. As a result, by acting above the center of mass, the net aerodynamic force produced by the wings is directed inward, generating the necessary torques for turning.

}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Ros, I. G. and Badger, M. A. and Pierson, A. N. and Bassman, L. C. and Biewener, A. A.} } @article {548576, title = {Pigeons trade efficiency for stability in response to level of challenge during confined flight}, journal = {Proc Natl Acad Sci U S A}, volume = {112}, number = {11}, year = {2015}, note = {

Williams, C DavidBiewener, Andrew Aeng2015/03/04 06:00Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):3392-6. doi: 10.1073/pnas.1407298112. Epub 2015 Mar 2.

}, month = {Mar 17}, pages = {3392-6}, abstract = {

Individuals traversing challenging obstacles are faced with a decision: they can adopt traversal strategies that minimally disrupt their normal locomotion patterns or they can adopt strategies that substantially alter their gait, conferring new advantages and disadvantages. We flew pigeons (Columba livia) through an array of vertical obstacles in a flight arena, presenting them with this choice. The pigeons selected either a strategy involving only a slight pause in the normal wing beat cycle, or a wings-folded posture granting reduced efficiency but greater stability should a misjudgment lead to collision. The more stable but less efficient flight strategy was not used to traverse easy obstacles with wide gaps for passage but came to dominate the postures used as obstacle challenge increased with narrower gaps and there was a greater chance of a collision. These results indicate that birds weigh potential obstacle negotiation strategies and estimate task difficulty during locomotor pattern selection.

}, isbn = {1091-6490 (Electronic)0027-8424 (Linking)}, author = {Williams, C. D. and Biewener, A. A.} } @article {548486, title = {A constitutive description of the anisotropic response of the fascia lata}, journal = {J Mech Behav Biomed MaterJ Mech Behav Biomed MaterJ Mech Behav Biomed Mater}, volume = {30}, year = {2014}, note = {Pancheri, F QEng, C MLieberman, D EBiewener, A ADorfmann, LengNetherlands2013/12/24 06:00J Mech Behav Biomed Mater. 2014 Feb;30:306-23. doi: 10.1016/j.jmbbm.2013.12.002. Epub 2013 Dec 9.}, month = {Feb}, pages = {306-23}, abstract = {In this paper we propose a constitutive model to analyze in-plane extension of goat fascia lata. We first perform a histological analysis of the fascia that shows a well-organized bi-layered arrangement of undulated collagen fascicles oriented along two well defined directions. To develop a model consistent with the tissue structure we identify the absolute and relative thickness of each layer and the orientation of the preferred directions. New data are presented showing the mechanical response in uniaxial and planar biaxial extension. The paper proposes a constitutive relation to describe the mechanical response. We provide a summary of the main ingredients of the nonlinear theory of elasticity and introduce a suitable strain-energy function to describe the anisotropic response of the fascia. We validate the model by showing good fit of the numerical results and the experimental data. Comments are included about differences and analogies between goat fascia lata and the human iliotibial band.}, keywords = {*Fascia Lata/cytology, *Materials Testing, *Mechanical Processes, Anisotropy, Biomechanical Phenomena, Elasticity, Humans, Models, Biological, Molecular Imaging, Stress, Mechanical}, isbn = {1878-0180 (Electronic)1878-0180 (Linking)}, author = {Pancheri, F. Q. and Eng, C. M. and Lieberman, D. E. and Biewener, A. A. and Dorfmann, L.} } @article {548421, title = {Through the eyes of a bird: modelling visually guided obstacle flight}, journal = {J R Soc InterfaceJ R Soc InterfaceJ R Soc Interface}, volume = {11}, number = {96}, year = {2014}, note = {Lin, Huai-TiRos, Ivo GBiewener, Andrew AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2014/05/09 06:00J R Soc Interface. 2014 May 8;11(96):20140239. doi: 10.1098/rsif.2014.0239. Print 2014 Jul 6.}, month = {Jul 6}, pages = {20140239}, abstract = {Various flight navigation strategies for birds have been identified at the large spatial scales of migratory and homing behaviours. However, relatively little is known about close-range obstacle negotiation through cluttered environments. To examine obstacle flight guidance, we tracked pigeons (Columba livia) flying through an artificial forest of vertical poles. Interestingly, pigeons adjusted their flight path only approximately 1.5 m from the forest entry, suggesting a reactive mode of path planning. Combining flight trajectories with obstacle pole positions, we reconstructed the visual experience of the pigeons throughout obstacle flights. Assuming proportional-derivative control with a constant delay, we searched the relevant parameter space of steering gains and visuomotor delays that best explained the observed steering. We found that a pigeon{\textquoteright}s steering resembles proportional control driven by the error angle between the flight direction and the desired opening, or gap, between obstacles. Using this pigeon steering controller, we simulated obstacle flights and showed that pigeons do not simply steer to the nearest opening in the direction of flight or destination. Pigeons bias their flight direction towards larger visual gaps when making fast steering decisions. The proposed behavioural modelling method converts the obstacle avoidance behaviour into a (piecewise) target-aiming behaviour, which is better defined and understood. This study demonstrates how such an approach decomposes open-loop free-flight behaviours into components that can be independently evaluated.}, keywords = {*Flight, Animal, *Models, Biological, *Visual Perception, Animals, Birds, Columbidae/*physiology, Depth Perception, Eye, Homing Behavior}, isbn = {1742-5662 (Electronic)1742-5662 (Linking)}, author = {Lin, H. T. and Ros, I. G. and Biewener, A. A.} } @article {548361, title = {The effect of fast and slow motor unit activation on whole-muscle mechanical performance: the size principle may not pose a mechanical paradox}, journal = {Proc Biol SciProc Biol SciProc Biol Sci}, volume = {281}, number = {1783}, year = {2014}, note = {Holt, N CWakeling, J MBiewener, A AengAR055648/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralEngland2014/04/04 06:00Proc Biol Sci. 2014 Apr 2;281(1783):20140002. doi: 10.1098/rspb.2014.0002. Print 2014 May 22.}, month = {May 22}, pages = {20140002}, abstract = {The output of skeletal muscle can be varied by selectively recruiting different motor units. However, our knowledge of muscle function is largely derived from muscle in which all motor units are activated. This discrepancy may limit our understanding of in vivo muscle function. Hence, this study aimed to characterize the mechanical properties of muscle with different motor unit activation. We determined the isometric properties and isotonic force-velocity relationship of rat plantaris muscles in situ with all of the muscle active, 30\% of the muscle containing predominately slower motor units active or 20\% of the muscle containing predominately faster motor units active. There was a significant effect of active motor unit type on isometric force rise time (p < 0.001) and the force-velocity relationship (p < 0.001). Surprisingly, force rise time was longer and maximum shortening velocity higher when all motor units were active than when either fast or slow motor units were selectively activated. We propose this is due to the greater relative effects of factors such as series compliance and muscle resistance to shortening during sub-maximal contractions. The findings presented here suggest that recruitment according to the size principle, where slow motor units are activated first and faster ones recruited as demand increases, may not pose a mechanical paradox, as has been previously suggested.}, keywords = {*Isometric Contraction, *Recruitment, Neurophysiological, Animals, Electromyography, Male, Muscle, Skeletal/*physiology, Rats, Rats, Sprague-Dawley, Time Factors}, isbn = {1471-2954 (Electronic)0962-8452 (Linking)}, author = {Holt, N. C. and Wakeling, J. M. and Biewener, A. A.} } @article {548391, title = {Scaling of the spring in the leg during bouncing gaits of mammals}, journal = {Integr Comp BiolIntegr Comp BiolIntegr Comp Biol}, volume = {54}, number = {6}, year = {2014}, note = {Lee, David VIsaacs, Michael RHiggins, Trevor EBiewener, Andrew AMcGowan, Craig PengP20 GM103408/GM/NIGMS NIH HHS/P20 RR016454/RR/NCRR NIH HHS/P20GM103440/GM/NIGMS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2014/10/12 06:00Integr Comp Biol. 2014 Dec;54(6):1099-108. doi: 10.1093/icb/icu114. Epub 2014 Oct 9.}, month = {Dec}, pages = {1099-108}, abstract = {Trotting, bipedal running, and especially hopping have long been considered the principal bouncing gaits of legged animals. We use the radial-leg spring constant [Formula: see text] to quantify the stiffness of the physical leg during bouncing gaits. The radial-leg is modeled as an extensible strut between the hip and the ground and [Formula: see text] is determined from the force and deflection of this strut in each instance of stance. A Hookean spring is modeled in-series with a linear actuator and the stiffness of this spring [Formula: see text] is determined by minimizing the work of the actuator while reproducing the measured force-deflection dynamics of an individual leg during trotting or running, and of the paired legs during hopping. Prior studies have estimated leg stiffness using [Formula: see text], a metric that imagines a virtual-leg connected to the center of mass. While [Formula: see text] has been applied extensively in human and comparative biomechanics, we show that [Formula: see text] more accurately models the spring in the leg when actuation is allowed, as is the case in biological and robotic systems. Our allometric analysis of [Formula: see text] in the kangaroo rat, tammar wallaby, dog, goat, and human during hopping, trotting, or running show that [Formula: see text] scales as body mass to the two-third power, which is consistent with the predictions of dynamic similarity and with the scaling of [Formula: see text]. Hence, two-third scaling of locomotor spring constants among mammals is supported by both the radial-leg and virtual-leg models, yet the scaling of [Formula: see text] emerges from work-minimization in the radial-leg model instead of being a defacto result of the ratio of force to length used to compute [Formula: see text]. Another key distinction between the virtual-leg and radial-leg is that [Formula: see text] is substantially greater than [Formula: see text], as indicated by a 30-37\% greater scaling coefficient for [Formula: see text]. We also show that the legs of goats are on average twice as stiff as those of dogs of the same mass and that goats increase the stiffness of their legs, in part, by more nearly aligning their distal limb-joints with the ground reaction force vector. This study is the first allometric analysis of leg spring constants in two decades. By means of an independent model, our findings reinforce the two-third scaling of spring constants with body mass, while showing that springs in-series with actuators are stiffer than those predicted by energy-conservative models of the leg.}, isbn = {1557-7023 (Electronic)1540-7063 (Linking)}, author = {Lee, D. V. and Isaacs, M. R. and Higgins, T. E. and Biewener, A. A. and McGowan, C. P.} } @article {548276, title = {Directional differences in the biaxial material properties of fascia lata and the implications for fascia function}, journal = {Ann Biomed EngAnn Biomed EngAnn Biomed Eng}, volume = {42}, number = {6}, year = {2014}, note = {Eng, Carolyn MPancheri, Francesco QLieberman, Daniel EBiewener, Andrew ADorfmann, LuisengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2014/03/22 06:00Ann Biomed Eng. 2014 Jun;42(6):1224-37. doi: 10.1007/s10439-014-0999-3. Epub 2014 Mar 20.}, month = {Jun}, pages = {1224-37}, abstract = {Fascia is a highly organized collagenous tissue that is ubiquitous in the body, but whose function is not well understood. Because fascia has a sheet-like structure attaching to muscles and bones at multiple sites, it is exposed to different states of multi- or biaxial strain. In order to measure how biaxial strain affects fascia material behavior, planar biaxial tests with strain control were performed on longitudinal and transversely oriented samples of goat fascia lata (FL). Cruciform samples were cycled to multiple strain levels while the perpendicular direction was held at a constant strain. Structural differences among FL layers were examined using histology and SEM. Results show that FL stiffness, hysteresis, and strain energy density are greater in the longitudinal vs. transverse direction. Increased stiffness in the longitudinal layer is likely due to its greater thickness and greater average fibril diameter compared to the transverse layer(s). Perpendicular strain did not affect FL material behavior. Differential loading in the longitudinal vs. transverse directions may lead to structural changes, enhancing the ability of the longitudinal FL to transmit force, store energy, or stabilize the limb during locomotion. The relative compliance of the transverse fibers may allow expansion of underlying muscles when they contract.}, keywords = {*Stress, Mechanical, Animals, Collagen/chemistry/metabolism, Fascia Lata/*chemistry/metabolism, Goats, Hindlimb/physiology, Locomotion/physiology, Weight-Bearing/physiology}, isbn = {1573-9686 (Electronic)0090-6964 (Linking)}, author = {Eng, C. M. and Pancheri, F. Q. and Lieberman, D. E. and Biewener, A. A. and Dorfmann, L.} } @article {548211, title = {Validation of Hill-type muscle models in relation to neuromuscular recruitment and force-velocity properties: predicting patterns of in vivo muscle force}, journal = {Integr Comp BiolIntegr Comp BiolIntegr Comp Biol}, volume = {54}, number = {6}, year = {2014}, note = {Biewener, Andrew AWakeling, James MLee, Sabrina SArnold, Allison SengR01AR055648/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralEngland2014/06/15 06:00Integr Comp Biol. 2014 Dec;54(6):1072-83. doi: 10.1093/icb/icu070. Epub 2014 Jun 12.}, month = {Dec}, pages = {1072-83}, abstract = {We review here the use and reliability of Hill-type muscle models to predict muscle performance under varying conditions, ranging from in situ production of isometric force to in vivo dynamics of muscle length change and force in response to activation. Muscle models are frequently used in musculoskeletal simulations of movement, particularly when applied to studies of human motor performance in which surgically implanted transducers have limited use. Musculoskeletal simulations of different animal species also are being developed to evaluate comparative and evolutionary aspects of locomotor performance. However, such models are rarely validated against direct measures of fascicle strain or recordings of muscle-tendon force. Historically, Hill-type models simplify properties of whole muscle by scaling salient properties of single fibers to whole muscles, typically accounting for a muscle{\textquoteright}s architecture and series elasticity. Activation of the model{\textquoteright}s single contractile element (assigned the properties of homogenous fibers) is also simplified and is often based on temporal features of myoelectric (EMG) activation recorded from the muscle. Comparison of standard one-element models with a novel two-element model and with in situ and in vivo measures of EMG, fascicle strain, and force recorded from the gastrocnemius muscles of goats shows that a two-element Hill-type model, which allows independent recruitment of slow and fast units, better predicts temporal patterns of in situ and in vivo force. Recruitment patterns of slow/fast units based on wavelet decomposition of EMG activity in frequency-time space are generally correlated with the intensity spectra of the EMG signals, the strain rates of the fascicles, and the muscle-tendon forces measured in vivo, with faster units linked to greater strain rates and to more rapid forces. Using direct measures of muscle performance to further test Hill-type models, whether traditional or more complex, remains critical for establishing their accuracy and essential for verifying their applicability to scientific and clinical studies of musculoskeletal function.}, isbn = {1557-7023 (Electronic)1540-7063 (Linking)}, author = {Biewener, A. A. and Wakeling, J. M. and Lee, S. S. and Arnold, A. S.} } @article {548406, title = {Recruitment of faster motor units is associated with greater rates of fascicle strain and rapid changes in muscle force during locomotion}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {216}, number = {Pt 2}, year = {2013}, note = {Lee, Sabrina S Mde Boef Miara, MariaArnold, Allison SBiewener, Andrew AWakeling, James MengR01 AR055648/AR/NIAMS NIH HHS/R01AR055648/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralEngland2012/09/14 06:00J Exp Biol. 2013 Jan 15;216(Pt 2):198-207. doi: 10.1242/jeb.072637. Epub 2012 Sep 12.}, month = {Jan 15}, pages = {198-207}, abstract = {Animals modulate the power output needed for different locomotor tasks by changing muscle forces and fascicle strain rates. To generate the necessary forces, appropriate motor units must be recruited. Faster motor units have faster activation-deactivation rates than slower motor units, and they contract at higher strain rates; therefore, recruitment of faster motor units may be advantageous for tasks that involve rapid movements or high rates of work. This study identified motor unit recruitment patterns in the gastrocnemii muscles of goats and examined whether faster motor units are recruited when locomotor speed is increased. The study also examined whether locomotor tasks that elicit faster (or slower) motor units are associated with increased (or decreased) in vivo tendon forces, force rise and relaxation rates, fascicle strains and/or strain rates. Electromyography (EMG), sonomicrometry and muscle-tendon force data were collected from the lateral and medial gastrocnemius muscles of goats during level walking, trotting and galloping and during inclined walking and trotting. EMG signals were analyzed using wavelet and principal component analyses to quantify changes in the EMG frequency spectra across the different locomotor conditions. Fascicle strain and strain rate were calculated from the sonomicrometric data, and force rise and relaxation rates were determined from the tendon force data. The results of this study showed that faster motor units were recruited as goats increased their locomotor speeds from level walking to galloping. Slow inclined walking elicited EMG intensities similar to those of fast level galloping but different EMG frequency spectra, indicating that recruitment of the different motor unit types depended, in part, on characteristics of the task. For the locomotor tasks and muscles analyzed here, recruitment patterns were generally associated with in vivo fascicle strain rates, EMG intensity and tendon force. Together, these data provide new evidence that changes in motor unit recruitment have an underlying mechanical basis, at least for certain locomotor tasks.}, keywords = {*Locomotion, Animals, Biomechanical Phenomena, Electromyography, Female, Goats/*physiology, Male, Muscle Contraction, Muscle Fibers, Fast-Twitch/physiology, Muscle, Skeletal/*physiology, Tendons/*physiology}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Lee, S. S. and de Boef Miara, M. and Arnold, A. S. and Biewener, A. A. and Wakeling, J. M.} } @article {548401, title = {Accuracy of gastrocnemius muscles forces in walking and running goats predicted by one-element and two-element Hill-type models}, journal = {J BiomechJ BiomechJ Biomech}, volume = {46}, number = {13}, year = {2013}, note = {Lee, Sabrina S MArnold, Allison SMiara, Maria de BoefBiewener, Andrew AWakeling, James MengR01 AR055648/AR/NIAMS NIH HHS/R01AR055648/AR/NIAMS NIH HHS/Research Support, N.I.H., Extramural2013/07/23 06:00J Biomech. 2013 Sep 3;46(13):2288-95. doi: 10.1016/j.jbiomech.2013.06.001. Epub 2013 Jul 18.}, month = {Sep 3}, pages = {2288-95}, abstract = {Hill-type models are commonly used to estimate muscle forces during human and animal movement-yet the accuracy of the forces estimated during walking, running, and other tasks remains largely unknown. Further, most Hill-type models assume a single contractile element, despite evidence that faster and slower motor units, which have different activation-deactivation dynamics, may be independently or collectively excited. This study evaluated a novel, two-element Hill-type model with "differential" activation of fast and slow contractile elements. Model performance was assessed using a comprehensive data set (including measures of EMG intensity, fascicle length, and tendon force) collected from the gastrocnemius muscles of goats during locomotor experiments. Muscle forces predicted by the new two-element model were compared to the forces estimated using traditional one-element models and to the forces measured in vivo using tendon buckle transducers. Overall, the two-element model resulted in the best predictions of in vivo gastrocnemius force. The coefficient of determination, r(2), was up to 26.9\% higher and the root mean square error, RMSE, was up to 37.4\% lower for the two-element model than for the one-element models tested. All models captured salient features of the measured muscle force during walking, trotting, and galloping (r(2)=0.26-0.51), and all exhibited some errors (RMSE=9.63-32.2\% of the maximum in vivo force). These comparisons provide important insight into the accuracy of Hill-type models. The results also show that incorporation of fast and slow contractile elements within muscle models can improve estimates of time-varying, whole muscle force during locomotor tasks.}, keywords = {*Models, Biological, Animals, Electromyography, Female, Goats, Male, Muscle Contraction/physiology, Muscle, Skeletal/*physiology, Reproducibility of Results, Running/*physiology, Walking/*physiology}, isbn = {1873-2380 (Electronic)0021-9290 (Linking)}, author = {Lee, S. S. and Arnold, A. S. and Miara Mde, B. and Biewener, A. A. and Wakeling, J. M.} } @article {548016, title = {Modulation of joint moments and work in the goat hindlimb with locomotor speed and surface grade}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {216}, number = {Pt 12}, year = {2013}, note = {Arnold, Allison SLee, David VBiewener, Andrew AengR01 AR047679/AR/NIAMS NIH HHS/R01 AR055648/AR/NIAMS NIH HHS/R01-AR47679/AR/NIAMS NIH HHS/R01-AR55648S/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralEngland2013/03/09 06:00J Exp Biol. 2013 Jun 15;216(Pt 12):2201-12. doi: 10.1242/jeb.082495. Epub 2013 Mar 7.}, month = {Jun 15}, pages = {2201-12}, abstract = {Goats and other quadrupeds must modulate the work output of their muscles to accommodate the changing mechanical demands associated with locomotion in their natural environments. This study examined which hindlimb joint moments goats use to generate and absorb mechanical energy on level and sloped surfaces over a range of locomotor speeds. Ground reaction forces and the three-dimensional locations of joint markers were recorded as goats walked, trotted and galloped over 0, +15 and -15 deg sloped surfaces. Net joint moments, powers and work were estimated at the goats{\textquoteright} hip, knee, ankle and metatarsophalangeal joints throughout the stance phase via inverse dynamics calculations. Differences in locomotor speed on the level, inclined and declined surfaces were characterized and accounted for by fitting regression equations to the joint moment, power and work data plotted versus non-dimensionalized speed. During level locomotion, the net work generated by moments at each of the hindlimb joints was small (less than 0.1 J kg(-1) body mass) and did not vary substantially with gait or locomotor speed. During uphill running, by contrast, mechanical energy was generated at the hip, knee and ankle, and the net work at each of these joints increased dramatically with speed (P<0.05). The greatest increases in positive joint work occurred at the hip and ankle. During downhill running, mechanical energy was decreased in two main ways: goats generated larger knee extension moments in the first half of stance, absorbing energy as the knee flexed, and goats generated smaller ankle extension moments in the second half of stance, delivering less energy. The goats{\textquoteright} hip extension moment in mid-stance was also diminished, contributing to the decrease in energy. These analyses offer new insight into quadrupedal locomotion, clarifying how the moments generated by hindlimb muscles modulate mechanical energy at different locomotor speeds and grades, as needed to accommodate the demands of variable terrain.}, keywords = {*Gait, *Locomotion, Animals, Biomechanical Phenomena, Female, Goats/*physiology, Hindlimb/*physiology, Joints/*physiology, Male}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Arnold, A. S. and Lee, D. V. and Biewener, A. A.} } @article {548566, title = {A muscle{\textquoteright}s force depends on the recruitment patterns of its fibers}, journal = {Ann Biomed EngAnn Biomed EngAnn Biomed Eng}, volume = {40}, number = {8}, year = {2012}, note = {Wakeling, James MLee, Sabrina S MArnold, Allison Sde Boef Miara, MariaBiewener, Andrew AengR01 AR055648/AR/NIAMS NIH HHS/R01 AR055648-01A1/AR/NIAMS NIH HHS/R01AR055648/AR/NIAMS NIH HHS/Research Support, N.I.H., Extramural2012/02/22 06:00Ann Biomed Eng. 2012 Aug;40(8):1708-20. doi: 10.1007/s10439-012-0531-6. Epub 2012 Feb 17.}, month = {Aug}, pages = {1708-20}, abstract = {Biomechanical models of whole muscles commonly used in simulations of musculoskeletal function and movement typically assume that the muscle generates force as a scaled-up muscle fiber. However, muscles are comprised of motor units that have different intrinsic properties and that can be activated at different times. This study tested whether a muscle model comprised of motor units that could be independently activated resulted in more accurate predictions of force than traditional Hill-type models. Forces predicted by the models were evaluated by direct comparison with the muscle forces measured in situ from the gastrocnemii in goats. The muscle was stimulated tetanically at a range of frequencies, muscle fiber strains were measured using sonomicrometry, and the activation patterns of the different types of motor unit were calculated from electromyographic recordings. Activation patterns were input into five different muscle models. Four models were traditional Hill-type models with different intrinsic speeds and fiber-type properties. The fifth model incorporated differential groups of fast and slow motor units. For all goats, muscles and stimulation frequencies the differential model resulted in the best predictions of muscle force. The in situ muscle output was shown to depend on the recruitment of different motor units within the muscle.}, keywords = {*Models, Biological, Animals, Electromyography, Goats, Humans, Muscle Contraction/*physiology, Muscle Fibers, Skeletal/*physiology, Muscle Strength/*physiology}, isbn = {1573-9686 (Electronic)0090-6964 (Linking)}, author = {Wakeling, J. M. and Lee, S. S. and Arnold, A. S. and de Boef Miara, M. and Biewener, A. A.} } @article {548506, title = {Muscle function during takeoff and landing flight in the pigeon (Columba livia)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {215}, number = {Pt 23}, year = {2012}, note = {Robertson, Angela M BergBiewener, Andrew AengComparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2012/09/14 06:00J Exp Biol. 2012 Dec 1;215(Pt 23):4104-14. doi: 10.1242/jeb.075275. Epub 2012 Sep 12.}, month = {Dec 1}, pages = {4104-14}, abstract = {This study explored the muscle strain and activation patterns of several key flight muscles of the pigeon (Columba livia) during takeoff and landing flight. Using electromyography (EMG) to measure muscle activation, and sonomicrometry to quantify muscle strain, we evaluated the muscle function patterns of the pectoralis, biceps, humerotriceps and scapulotriceps as pigeons flew between two perches. These recordings were analyzed in the context of three-dimensional wing kinematics. To understand the different requirements of takeoff, midflight and landing, we compared the activity and strain of these muscles among the three flight modes. The pectoralis and biceps exhibited greater fascicle strain rates during takeoff than during midflight or landing. However, the triceps muscles did not exhibit notable differences in strain among flight modes. All observed strain, activation and kinematics were consistent with hypothesized muscle functions. The biceps contracted to stabilize and flex the elbow during the downstroke. The humerotriceps contracted to extend the elbow at the upstroke-downstroke transition, followed by scapulotriceps contraction to maintain elbow extension during the downstroke. The scapulotriceps also appeared to contribute to humeral elevation. Greater muscle activation intensity was observed during takeoff, compared with mid-flight and landing, in all muscles except the scapulotriceps. The timing patterns of muscle activation and length change differed among flight modes, yet demonstrated that pigeons do not change the basic mechanical actions of key flight muscles as they shift from flight activities that demand energy production, such as takeoff and midflight, to maneuvers that require absorption of energy, such as landing. Similarly, joint kinematics were consistent among flight modes. The stereotypy of these neuromuscular and joint kinematic patterns is consistent with previously observed stereotypy of wing kinematics relative to the pigeon{\textquoteright}s body (in the local body frame) across these flight behaviors. Taken together, these observations suggest that the control of takeoff and landing flight primarily involves modulation of overall body pitch to effect changes in stroke plane angle and resulting wing aerodynamics.}, keywords = {*Acceleration, *Flight, Animal, Analysis of Variance, Animals, Biomechanical Phenomena, Columbidae/*physiology, Deceleration, Electromyography, Muscle Contraction, Muscle, Skeletal/*physiology, Pectoralis Muscles/physiology, Videotape Recording, Wing/physiology}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Robertson, A. M. and Biewener, A. A.} } @article {548321, title = {Morphological and kinematic basis of the hummingbird flight stroke: scaling of flight muscle transmission ratio}, journal = {Proc Biol SciProc Biol SciProc Biol Sci}, volume = {279}, number = {1735}, year = {2012}, note = {Hedrick, Tyson LTobalske, Bret WRos, Ivo GWarrick, Douglas RBiewener, Andrew AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2011/12/16 06:00Proc Biol Sci. 2012 May 22;279(1735):1986-92. doi: 10.1098/rspb.2011.2238. Epub 2011 Dec 14.}, month = {May 22}, pages = {1986-92}, abstract = {Hummingbirds (Trochilidae) are widely known for their insect-like flight strokes characterized by high wing beat frequency, small muscle strains and a highly supinated wing orientation during upstroke that allows for lift production in both halves of the stroke cycle. Here, we show that hummingbirds achieve these functional traits within the limits imposed by a vertebrate endoskeleton and muscle physiology by accentuating a wing inversion mechanism found in other birds and using long-axis rotational movement of the humerus. In hummingbirds, long-axis rotation of the humerus creates additional wing translational movement, supplementing that produced by the humeral elevation and depression movements of a typical avian flight stroke. This adaptation increases the wing-to-muscle-transmission ratio, and is emblematic of a widespread scaling trend among flying animals whereby wing-to-muscle-transmission ratio varies inversely with mass, allowing animals of vastly different sizes to accommodate aerodynamic, biomechanical and physiological constraints on muscle-powered flapping flight.}, keywords = {*Flight, Animal, Animals, Biomechanical Phenomena, Birds/anatomy \& histology/*physiology, Female, Male, Muscle, Skeletal/*physiology, Video Recording, Wing/anatomy \& histology/physiology/radiography}, isbn = {1471-2954 (Electronic)0962-8452 (Linking)}, author = {Hedrick, T. L. and Tobalske, B. W. and Ros, I. G. and Warrick, D. R. and Biewener, A. A.} } @article {548156, title = {Editorial policy on computational, simulation and/or robotic papers}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {215}, number = {Pt 23}, year = {2012}, note = {Biewener, Andrew ADickinson, Michael HLauder, George VengEditorialEngland2012/11/09 06:00J Exp Biol. 2012 Dec 1;215(Pt 23):4051. doi: 10.1242/jeb.081794.}, month = {Dec 1}, pages = {4051}, keywords = {*Computer Simulation, *Editorial Policies, *Robotics, Computational Biology, Periodicals as Topic}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Biewener, A. A. and Dickinson, M. H. and Lauder, G. V.} } @article {548516, title = {Pigeons steer like helicopters and generate down- and upstroke lift during low speed turns}, journal = {Proc Natl Acad Sci U S AProc Natl Acad Sci U S AProc Natl Acad Sci U S A}, volume = {108}, number = {50}, year = {2011}, note = {Ros, Ivo GBassman, Lori CBadger, Marc APierson, Alyssa NBiewener, Andrew AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2011/11/30 06:00Proc Natl Acad Sci U S A. 2011 Dec 13;108(50):19990-5. doi: 10.1073/pnas.1107519108. Epub 2011 Nov 28.}, month = {Dec 13}, pages = {19990-5}, abstract = {Turning is crucial for animals, particularly during predator-prey interactions and to avoid obstacles. For flying animals, turning consists of changes in (i) flight trajectory, or path of travel, and (ii) body orientation, or 3D angular position. Changes in flight trajectory can only be achieved by modulating aerodynamic forces relative to gravity. How birds coordinate aerodynamic force production relative to changes in body orientation during turns is key to understanding the control strategies used in avian maneuvering flight. We hypothesized that pigeons produce aerodynamic forces in a uniform direction relative to their bodies, requiring changes in body orientation to redirect those forces to turn. Using detailed 3D kinematics and body mass distributions, we examined net aerodynamic forces and body orientations in slowly flying pigeons (Columba livia) executing level 90 degrees turns. The net aerodynamic force averaged over the downstroke was maintained in a fixed direction relative to the body throughout the turn, even though the body orientation of the birds varied substantially. Early in the turn, changes in body orientation primarily redirected the downstroke aerodynamic force, affecting the bird{\textquoteright}s flight trajectory. Subsequently, the pigeon mainly reacquired the body orientation used in forward flight without affecting its flight trajectory. Surprisingly, the pigeon{\textquoteright}s upstroke generated aerodynamic forces that were approximately 50\% of those generated during the downstroke, nearly matching the relative upstroke forces produced by hummingbirds. Thus, pigeons achieve low speed turns much like helicopters, by using whole-body rotations to alter the direction of aerodynamic force production to change their flight trajectory.}, keywords = {*Aircraft, Animals, Biomechanical Phenomena, Columbidae/*physiology, Flight, Animal/*physiology, Models, Biological, Movement/*physiology, Rotation}, isbn = {1091-6490 (Electronic)0027-8424 (Linking)}, author = {Ros, I. G. and Bassman, L. C. and Badger, M. A. and Pierson, A. N. and Biewener, A. A.} } @article {548411, title = {EMG analysis tuned for determining the timing and level of activation in different motor units}, journal = {J Electromyogr KinesiolJ Electromyogr KinesiolJ Electromyogr Kinesiol}, volume = {21}, number = {4}, year = {2011}, note = {Lee, Sabrina S MMiara, Maria de BoefArnold, Allison SBiewener, Andrew AWakeling, James MengR01 AR055648/AR/NIAMS NIH HHS/R01 AR055648-03/AR/NIAMS NIH HHS/R01AR055648/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralEngland2011/05/17 06:00J Electromyogr Kinesiol. 2011 Aug;21(4):557-65. doi: 10.1016/j.jelekin.2011.04.003. Epub 2011 May 12.}, month = {Aug}, pages = {557-65}, abstract = {Recruitment patterns and activation dynamics of different motor units greatly influence the temporal pattern and magnitude of muscle force development, yet these features are not often considered in muscle models. The purpose of this study was to characterize the recruitment and activation dynamics of slow and fast motor units from electromyographic (EMG) recordings and twitch force profiles recorded directly from animal muscles. EMG and force data from the gastrocnemius muscles of seven goats were recorded during in vivo tendon-tap reflex and in situ nerve stimulation experiments. These experiments elicited EMG signals with significant differences in frequency content (p<0.001). The frequency content was characterized using wavelet and principal components analysis, and optimized wavelets with centre frequencies, 149.94 Hz and 323.13 Hz, were obtained. The optimized wavelets were used to calculate the EMG intensities and, with the reconstructed twitch force profiles, to derive transfer functions for slow and fast motor units that estimate the activation state of the muscle from the EMG signal. The resulting activation-deactivation time constants gave r values of 0.98-0.99 between the activation state and the force profiles. This work establishes a framework for developing improved muscle models that consider the intrinsic properties of slow and fast fibres within a mixed muscle, and that can more accurately predict muscle force output from EMG.}, keywords = {*Electromyography, *Recruitment, Neurophysiological, Animals, Goats, Motor Neurons/*physiology, Muscle, Skeletal/*physiology}, isbn = {1873-5711 (Electronic)1050-6411 (Linking)}, author = {Lee, S. S. and Miara Mde, B. and Arnold, A. S. and Biewener, A. A. and Wakeling, J. M.} } @article {548386, title = {BigDog-inspired studies in the locomotion of goats and dogs}, journal = {Integr Comp BiolIntegr Comp BiolIntegr Comp Biol}, volume = {51}, number = {1}, year = {2011}, note = {Lee, David VBiewener, Andrew AengComparative StudyResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2011/06/11 06:00Integr Comp Biol. 2011 Jul;51(1):190-202. doi: 10.1093/icb/icr061. Epub 2011 Jun 9.}, month = {Jul}, pages = {190-202}, abstract = {Collision-based expenditure of mechanical energy and the compliance and geometry of the leg are fundamental, interrelated considerations in the mechanical design of legged runners. This article provides a basic context and rationale for experiments designed to inform each of these key areas in Boston Dynamic{\textquoteright}s BigDog robot. Although these principles have been investigated throughout the past few decades within different academic disciplines, BigDog required that they be considered together and in concert with an impressive set of control algorithms that are not discussed here. Although collision reduction is an important strategy for reducing mechanical cost of transport in the slowest and fastest quadrupedal gaits, walking and galloping, BigDog employed an intermediate-speed trotting gait without collision reduction. Trotting, instead, uses a spring-loaded inverted pendulum mechanism with potential for storage and return of elastic strain energy in appropriately compliant structures. Rather than tuning BigDog{\textquoteright}s built-in leg springs according to a spring-mass model-based virtual leg-spring constant , a much stiffer distal leg spring together with actuation of the adjacent joint provided good trotting dynamics and avoided functional limitations that might have been imposed by too much compliance in real-world terrain. Adjusting the directional compliance of the legs by adopting a knee-forward, elbow-back geometry led to more robust trotting dynamics by reducing perturbations about the pitch axis of the robot{\textquoteright}s center of mass (CoM). BigDog is the most successful large-scale, all-terrain trotting machine built to date and it continues to stimulate our understanding of legged locomotion in comparative biomechanics as well as in robotics.}, keywords = {Animals, Biomechanical Phenomena, Dogs/*physiology, Gait/physiology, Goats/*physiology, Locomotion/*physiology, Lower Extremity/*physiology, Models, Theoretical, Robotics/instrumentation/*methods}, isbn = {1557-7023 (Electronic)1540-7063 (Linking)}, author = {Lee, D. V. and Biewener, A. A.} } @article {548381, title = {A collisional perspective on quadrupedal gait dynamics}, journal = {J R Soc InterfaceJ R Soc InterfaceJ R Soc Interface}, volume = {8}, number = {63}, year = {2011}, note = {Lee, David VBertram, John E AAnttonen, Jennifer TRos, Ivo GHarris, Sarah LBiewener, Andrew AengEngland2011/04/08 06:00J R Soc Interface. 2011 Oct 7;8(63):1480-6. doi: 10.1098/rsif.2011.0019. Epub 2011 Apr 6.}, month = {Oct 7}, pages = {1480-6}, abstract = {The analysis of terrestrial locomotion over the past half century has focused largely on strategies of mechanical energy recovery used during walking and running. In contrast, we describe the underlying mechanics of legged locomotion as a collision-like interaction that redirects the centre of mass (CoM). We introduce the collision angle, determined by the angle between the CoM force and velocity vectors, and show by computing the collision fraction, a ratio of actual to potential collision, that the quadrupedal walk and gallop employ collision-reduction strategies while the trot permits greater collisions. We provide the first experimental evidence that a collision-based approach can differentiate quadrupedal gaits and quantify interspecific differences. Furthermore, we show that this approach explains the physical basis of a commonly used locomotion metric, the mechanical cost of transport. Collision angle and collision fraction provide a unifying analysis of legged locomotion which can be applied broadly across animal size, leg number and gait.}, keywords = {Animals, Biomechanical Phenomena, Dogs/*physiology, Gait/*physiology, Goats/*physiology, Locomotion/*physiology}, isbn = {1742-5662 (Electronic)1742-5662 (Linking)}, author = {Lee, D. V. and Bertram, J. E. and Anttonen, J. T. and Ros, I. G. and Harris, S. L. and Biewener, A. A.} } @article {548346, title = {Functional and architectural complexity within and between muscles: regional variation and intermuscular force transmission}, journal = {Philos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol Sci}, volume = {366}, number = {1570}, year = {2011}, note = {Higham, Timothy EBiewener, Andrew AengReviewEngland2011/04/20 06:00Philos Trans R Soc Lond B Biol Sci. 2011 May 27;366(1570):1477-87. doi: 10.1098/rstb.2010.0359.}, month = {May 27}, pages = {1477-87}, abstract = {Over the past 30 years, studies of single muscles have revealed complex patterns of regional variation in muscle architecture, activation, strain and force. In addition, muscles are often functionally integrated with other muscles in parallel or in series. Understanding the extent of this complexity and the interactions between muscles will profoundly influence how we think of muscles in relation to organismal function, and will allow us to address questions regarding the functional benefits (or lack thereof) and dynamics of this complexity under in vivo conditions. This paper has two main objectives. First, we present a cohesive and integrative review of regional variation in function within muscles, and discuss the functional ramifications that can stem from this variation. This involves splitting regional variation into passive and active components. Second, we assess the functional integration of muscles between different limb segments by presenting new data involving in vivo measurements of activation and strain from the medial gastrocnemius, iliotibialis cranialis and iliotibialis lateralis pars preacetabularis of the helmeted guinea fowl (Numida meleagris) during level running on a motorized treadmill. Future research directions for both of these objectives are presented.}, keywords = {Animals, Biomechanical Phenomena, Extremities/*physiology, Galliformes/*physiology, Locomotion/*physiology, Models, Biological, Muscle Contraction/*physiology, Muscle Fatigue/*physiology, Muscle, Skeletal/*physiology}, isbn = {1471-2970 (Electronic)0962-8436 (Linking)}, author = {Higham, T. E. and Biewener, A. A.} } @article {548351, title = {Mechanics, modulation and modelling: how muscles actuate and control movement}, journal = {Philos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol Sci}, volume = {366}, number = {1570}, year = {2011}, note = {Higham, Timothy EBiewener, Andrew ADelp, Scott LengIntroductoryEngland2011/04/20 06:00Philos Trans R Soc Lond B Biol Sci. 2011 May 27;366(1570):1463-5. doi: 10.1098/rstb.2010.0354.}, month = {May 27}, pages = {1463-5}, abstract = {Animal movement is often complex, unsteady and variable. The critical role of muscles in animal movement has captivated scientists for over 300 years. Despite this, emerging techniques and ideas are still shaping and advancing the field. For example, sonomicrometry and ultrasound techniques have enhanced our ability to quantify muscle length changes under in vivo conditions. Robotics and musculoskeletal models have benefited from improved computational tools and have enhanced our ability to understand muscle function in relation to movement by allowing one to simulate muscle-tendon dynamics under realistic conditions. The past decade, in particular, has seen a rapid advancement in technology and shifts in paradigms related to muscle function. In addition, there has been an increased focus on muscle function in relation to the complex locomotor behaviours, rather than relatively simple (and steady) behaviours. Thus, this Theme Issue will explore integrative aspects of muscle function in relation to diverse locomotor behaviours such as swimming, jumping, hopping, running, flying, moving over obstacles and transitioning between environments. Studies of walking and running have particular relevance to clinical aspects of human movement and sport. This Theme Issue includes contributions from scientists working on diverse taxa, ranging from humans to insects. In addition to contributions addressing locomotion in various taxa, several manuscripts will focus on recent advances in neuromuscular control and modulation during complex behaviours. Finally, some of the contributions address recent advances in biomechanical modelling and powered prostheses. We hope that our comprehensive and integrative Theme Issue will form the foundation for future work in the fields of neuromuscular mechanics and locomotion.}, keywords = {*Models, Biological, Animals, Biomechanical Phenomena, Locomotion/*physiology, Muscle Contraction/*physiology, Muscle, Skeletal/anatomy \& histology/*physiology}, isbn = {1471-2970 (Electronic)0962-8436 (Linking)}, author = {Higham, T. E. and Biewener, A. A. and Delp, S. L.} } @article {548256, title = {Leg muscles that mediate stability: mechanics and control of two distal extensor muscles during obstacle negotiation in the guinea fowl}, journal = {Philos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol Sci}, volume = {366}, number = {1570}, year = {2011}, note = {Daley, Monica ABiewener, Andrew AengAR047679/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2011/04/20 06:00Philos Trans R Soc Lond B Biol Sci. 2011 May 27;366(1570):1580-91. doi: 10.1098/rstb.2010.0338.}, month = {May 27}, pages = {1580-91}, abstract = {Here, we used an obstacle treadmill experiment to investigate the neuromuscular control of locomotion in uneven terrain. We measured in vivo function of two distal muscles of the guinea fowl, lateral gastrocnemius (LG) and digital flexor-IV (DF), during level running, and two uneven terrains, with 5 and 7 cm obstacles. Uneven terrain required one step onto an obstacle every four to five strides. We compared both perturbed and unperturbed strides in uneven terrain to level terrain. When the bird stepped onto an obstacle, the leg became crouched, both muscles acted at longer lengths and produced greater work, and body height increased. Muscle activation increased on obstacle strides in the LG, but not the DF, suggesting a greater reflex contribution to LG. In unperturbed strides in uneven terrain, swing pre-activation of DF increased by 5 per cent compared with level terrain, suggesting feed-forward tuning of leg impedance. Across conditions, the neuromechanical factors in work output differed between the two muscles, probably due to differences in muscle-tendon architecture. LG work depended primarily on fascicle length, whereas DF work depended on both length and velocity during loading. These distal muscles appear to play a critical role in stability by rapidly sensing and responding to altered leg-ground interaction.}, keywords = {Analysis of Variance, Animals, Biomechanical Phenomena, Electromyography, Gait/*physiology, Galliformes/*physiology, Hindlimb/*physiology, Locomotion/*physiology, Muscle, Skeletal/anatomy \& histology/innervation/*physiology, Transducers}, isbn = {1471-2970 (Electronic)0962-8436 (Linking)}, author = {Daley, M. A. and Biewener, A. A.} } @article {548111, title = {Muscle function in avian flight: achieving power and control}, journal = {Philos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol Sci}, volume = {366}, number = {1570}, year = {2011}, note = {Biewener, Andrew AengComparative StudyResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.ReviewEngland2011/04/20 06:00Philos Trans R Soc Lond B Biol Sci. 2011 May 27;366(1570):1496-506. doi: 10.1098/rstb.2010.0353.}, month = {May 27}, pages = {1496-506}, abstract = {Flapping flight places strenuous requirements on the physiological performance of an animal. Bird flight muscles, particularly at smaller body sizes, generally contract at high frequencies and do substantial work in order to produce the aerodynamic power needed to support the animal{\textquoteright}s weight in the air and to overcome drag. This is in contrast to terrestrial locomotion, which offers mechanisms for minimizing energy losses associated with body movement combined with elastic energy savings to reduce the skeletal muscles{\textquoteright} work requirements. Muscles also produce substantial power during swimming, but this is mainly to overcome body drag rather than to support the animal{\textquoteright}s weight. Here, I review the function and architecture of key flight muscles related to how these muscles contribute to producing the power required for flapping flight, how the muscles are recruited to control wing motion and how they are used in manoeuvring. An emergent property of the primary flight muscles, consistent with their need to produce considerable work by moving the wings through large excursions during each wing stroke, is that the pectoralis and supracoracoideus muscles shorten over a large fraction of their resting fibre length (33-42\%). Both muscles are activated while being lengthened or undergoing nearly isometric force development, enhancing the work they perform during subsequent shortening. Two smaller muscles, the triceps and biceps, operate over a smaller range of contractile strains (12-23\%), reflecting their role in controlling wing shape through elbow flexion and extension. Remarkably, pigeons adjust their wing stroke plane mainly via changes in whole-body pitch during take-off and landing, relative to level flight, allowing their wing muscles to operate with little change in activation timing, strain magnitude and pattern.}, keywords = {Animals, Biomechanical Phenomena, Birds/*physiology, Flight, Animal/*physiology, Muscle Contraction/*physiology, Muscle, Skeletal/*anatomy \& histology/*physiology, Species Specificity}, isbn = {1471-2970 (Electronic)0962-8436 (Linking)}, author = {Biewener, A. A.} } @article {548021, title = {There is always a trade-off between speed and force in a lever system: comment on McHenry (2010)}, journal = {Biol LettBiol LettBiol Lett}, volume = {7}, number = {6}, year = {2011}, note = {Arnold, Allison SRichards, Christopher TRos, Ivo GBiewener, Andrew AengCommentEngland2011/09/02 06:00Biol Lett. 2011 Dec 23;7(6):878-9; discussion 880-1. doi: 10.1098/rsbl.2011.0431. Epub 2011 Aug 31.}, month = {Dec 23}, pages = {878-9; discussion 880-1}, keywords = {*Models, Biological, Animals, Grasshoppers/*physiology}, isbn = {1744-957X (Electronic)1744-9561 (Linking)}, author = {Arnold, A. S. and Richards, C. T. and Ros, I. G. and Biewener, A. A.} } @article {548541, title = {Effects of flight speed upon muscle activity in hummingbirds}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {213}, number = {Pt 14}, year = {2010}, note = {Tobalske, Bret WBiewener, Andrew AWarrick, Douglas RHedrick, Tyson LPowers, Donald RengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2010/06/29 06:00J Exp Biol. 2010 Jul 15;213(Pt 14):2515-23. doi: 10.1242/jeb.043844.}, month = {Jul 15}, pages = {2515-23}, abstract = {Hummingbirds have the smallest body size and highest wingbeat frequencies of all flying vertebrates, so they represent one endpoint for evaluating the effects of body size on sustained muscle function and flight performance. Other bird species vary neuromuscular recruitment and contractile behavior to accomplish flight over a wide range of speeds, typically exhibiting a U-shaped curve with maxima at the slowest and fastest flight speeds. To test whether the high wingbeat frequencies and aerodynamically active upstroke of hummingbirds lead to different patterns, we flew rufous hummingbirds (Selasphorus rufus, 3 g body mass, 42 Hz wingbeat frequency) in a variable-speed wind tunnel (0-10 m s(-1)). We measured neuromuscular activity in the pectoralis (PECT) and supracoracoideus (SUPRA) muscles using electromyography (EMG, N=4 birds), and we measured changes in PECT length using sonomicrometry (N=1). Differing markedly from the pattern in other birds, PECT deactivation occurred before the start of downstroke and the SUPRA was deactivated before the start of upstroke. The relative amplitude of EMG signal in the PECT and SUPRA varied according to a U-shaped curve with flight speed; additionally, the onset of SUPRA activity became relatively later in the wingbeat at intermediate flight speeds (4 and 6 m s(-1)). Variation in the relative amplitude of EMG was comparable with that observed in other birds but the timing of muscle activity was different. These data indicate the high wingbeat frequency of hummingbirds limits the time available for flight muscle relaxation before the next half stroke of a wingbeat. Unlike in a previous study that reported single-twitch EMG signals in the PECT of hovering hummingbirds, across all flight speeds we observed 2.9+/-0.8 spikes per contraction in the PECT and 3.8+/-0.8 spikes per contraction in the SUPRA. Muscle strain in the PECT was 10.8+/-0.5\%, the lowest reported for a flying bird, and average strain rate was 7.4+/-0.2 muscle lengths s(-1). Among species of birds, PECT strain scales proportional to body mass to the 0.2 power (infinityM(b)(0.2)) using species data and infinityM(b)(0.3) using independent contrasts. This positive scaling is probably a physiological response to an adverse scaling of mass-specific power available for flight.}, keywords = {Animals, Biomechanical Phenomena, Birds/anatomy \& histology/*physiology, Electromyography, Female, Flight, Animal/*physiology, Muscle Contraction/physiology, Pectoralis Muscles/*physiology, Periodicity, Wing/*physiology}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Tobalske, B. W. and Biewener, A. A. and Warrick, D. R. and Hedrick, T. L. and Powers, D. R.} } @article {548416, title = {Nature-inspired flight--beyond the leap}, journal = {Bioinspir BiomimBioinspir BiomimBioinspir Biomim}, volume = {5}, number = {4}, year = {2010}, note = {Lentink, DavidBiewener, Andrew AengEditorialIntroductoryEngland2010/11/26 06:00Bioinspir Biomim. 2010 Dec;5(4):040201. doi: 10.1088/1748-3182/5/4/040201. Epub 2010 Nov 24.}, month = {Dec}, pages = {040201}, keywords = {*Aircraft, *Biomimetic Materials, *Models, Biological, Animals, Biomimetics/*instrumentation/*methods, Flight, Animal/*physiology, Wing/*physiology}, isbn = {1748-3190 (Electronic)1748-3182 (Linking)}, author = {Lentink, D. and Biewener, A. A.} } @article {548031, title = {Wing and body kinematics of takeoff and landing flight in the pigeon (Columba livia)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {213}, number = {Pt 10}, year = {2010}, note = {Berg, Angela MBiewener, Andrew AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2010/05/04 06:00J Exp Biol. 2010 May;213(Pt 10):1651-8. doi: 10.1242/jeb.038109.}, month = {May}, pages = {1651-8}, abstract = {Takeoff and landing are critical phases in a flight. To better understand the functional importance of the kinematic adjustments birds use to execute these flight modes, we studied the wing and body movements of pigeons (Columba livia) during short-distance free-flights between two perches. The greatest accelerations were observed during the second wingbeat of takeoff. The wings were responsible for the majority of acceleration during takeoff and landing, with the legs contributing only one-quarter of the acceleration. Parameters relating to aerodynamic power output such as downstroke amplitude, wingbeat frequency and downstroke velocity were all greatest during takeoff flight and decreased with each successive takeoff wingbeat. This pattern indicates that downstroke velocity must be greater for accelerating flight to increase the amount of air accelerated by the wings. Pigeons used multiple mechanisms to adjust thrust and drag to accelerate during takeoff and decelerate during landing. Body angle, tail angle and wing plane angles all shifted from more horizontal orientations during takeoff to near-vertical orientations during landing, thereby reducing drag during takeoff and increasing drag during landing. The stroke plane was tilted steeply downward throughout takeoff (increasing from -60+/-5 deg. to -47+/-1 deg.), supporting our hypothesis that a downward-tilted stroke plane pushes more air rearward to accelerate the bird forward. Similarly, the stroke plane tilted upward during landing (increasing from -1+/-2 deg. to 17+/-7 deg.), implying that an upward-tilted stroke plane pushes more air forward to slow the bird down. Rotations of the stroke plane, wing planes and tail were all strongly correlated with rotation of the body angle, suggesting that pigeons are able to redirect aerodynamic force and shift between flight modes through modulation of body angle alone.}, keywords = {Acceleration, Animals, Biomechanical Phenomena/physiology, Columbidae/*physiology, Flight, Animal/*physiology, Least-Squares Analysis, Regression Analysis, Tail/physiology, Wing/*physiology}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Berg, A. M. and Biewener, A. A.} } @article {548471, title = {Dynamics of goat distal hind limb muscle-tendon function in response to locomotor grade}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {212}, number = {Pt 13}, year = {2009}, note = {McGuigan, M PollyYoo, EdwinLee, David VBiewener, Andrew AengR01 AR47679/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralEngland2009/06/16 09:00J Exp Biol. 2009 Jul;212(Pt 13):2092-104. doi: 10.1242/jeb.028076.}, month = {Jul}, pages = {2092-104}, abstract = {The functional roles of the lateral gastrocnemius (LG), medial gastrocnemius (MG) and superficial digital flexor (SDF) muscle-tendon units (MTUs) in domestic goats (N=6) were studied as a function of locomotor grade, testing the hypothesis that changes in distal limb muscle work would reflect changes in mechanical work requirements while goats walked or trotted on the level, 15 deg. decline and 15 deg. incline. As steep terrain-adapted animals, changes in muscle work output are expected to be particularly important for goats. In vivo muscle-tendon forces, fascicle length changes and muscle activation were recorded via tendon force buckles, sonomicrometry and electromyography to evaluate the work performance and elastic energy recovery of the three distal MTUs. These recordings confirmed that fascicle strain and force within goat distal hind limb muscles are adjusted in response to changes in mechanical work demand associated with locomotor grade. In general, muscle work was modulated most consistently by changes in fascicle strain, with increased net shortening (P<0.001) observed as goats switched from decline to level to incline locomotion. Peak muscle stresses increased as goats increased speed from a walk to a trot within each grade condition (P<0.05), and also increased significantly with grade (P<0.05 to P<0.01). Due to the increase in net fascicle shortening and muscle force, net muscle work per cycle also increased significantly (P<0.05 to P<0.005) as goats switched from decline to level to incline conditions (LG work: 20 mJ to 56 mJ to 209 mJ; MG work: -7 mJ to 34 mJ to 179 mJ; SDF work: -42 mJ to 14 mJ to 71 mJ, at a 2.5 ms(-1) trot). Although muscle work was modulated in response to changes in grade, the amount of work produced by these three distal pennate muscles was small (being <3\%) in comparison with the change in mechanical energy required of the limb as a whole. Elastic energy recovery in the SDF and gastrocnemius (GA) tendons was substantial across all three grades, with the SDF tendon recovering 2.4 times more energy, on average, than the GA tendon. In parallel with the increase in muscle-tendon force, tendon energy recovery also increased as goats increased speed and changed gait, reaching the highest levels when goats trotted on an incline at 2.5 ms(-1) (GA: 173 mJ; SDF: 316 mJ). In general, tendon elastic energy exceeded net muscle work across all grade and gait conditions. These results demonstrate, for the first time in a quadruped, similar findings to those observed in ankle extensor muscles in humans, wallabies, turkeys and guinea fowl, suggesting that distal muscle-tendon architecture more generally favors a design for economic force production and tendon elastic energy recovery, with the majority of limb work during incline or decline running performed by larger proximal muscles.}, keywords = {Animals, Biomechanical Phenomena, Energy Metabolism, Female, Goats/anatomy \& histology/*physiology, Locomotion/*physiology, Muscle, Skeletal/anatomy \& histology/*physiology, Physical Exertion, Tendons/anatomy \& histology/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {McGuigan, M. P. and Yoo, E. and Lee, D. V. and Biewener, A. A.} } @article {548341, title = {Fatigue alters in vivo function within and between limb muscles during locomotion}, journal = {Proc Biol SciProc Biol SciProc Biol Sci}, volume = {276}, number = {1659}, year = {2009}, note = {Higham, Timothy EBiewener, Andrew AengR01-AR047679/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralEngland2009/01/09 09:00Proc Biol Sci. 2009 Mar 22;276(1659):1193-7. doi: 10.1098/rspb.2008.1734.}, month = {Mar 22}, pages = {1193-7}, abstract = {Muscle fatigue, a reduction in force as a consequence of exercise, is an important factor for any animal that moves, and can result from both peripheral and/or central mechanisms. Although much is known about whole-limb force generation and activation patterns in fatigued muscles under sustained isometric contractions, little is known about the in vivo dynamics of limb muscle function in relation to whole-body fatigue. Here we show that limb kinematics and contractile function in the lateral (LG) and medial (MG) gastrocnemius of helmeted guineafowl (Numida meleagris) are significantly altered following fatiguing exercise at 2ms-1 on an inclined treadmill. The two most significant findings were that the variation in muscle force generation, measured directly from the muscles{\textquoteright} tendons, increased significantly with fatigue, and fascicle shortening in the proximal MG, but not the distal MG, decreased significantly with fatigue. We suggest that the former is a potential mechanism for decreased stability associated with fatigue. The region-specific alteration of fascicle behaviour within the MG as a result of fatigue suggests a complex response to fatigue that probably depends on muscle-aponeurosis and tendon architecture not previously explored. These findings highlight the importance of studying the integrative in vivo dynamics of muscle function in response to fatigue.}, keywords = {Animals, Galliformes/*physiology, Locomotion/*physiology, Muscle Contraction/physiology, Muscle Fatigue/*physiology, Muscle, Skeletal/*physiology}, isbn = {0962-8452 (Print)0962-8452 (Linking)}, author = {Higham, T. E. and Biewener, A. A.} } @article {548271, title = {The role of intrinsic muscle mechanics in the neuromuscular control of stable running in the guinea fowl}, journal = {J PhysiolJ PhysiolJ Physiol}, volume = {587}, number = {Pt 11}, year = {2009}, note = {Daley, Monica AVoloshina, AlexandraBiewener, Andrew AengAR047679/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2009/04/11 09:00J Physiol. 2009 Jun 1;587(Pt 11):2693-707. doi: 10.1113/jphysiol.2009.171017. Epub 2009 Apr 9.}, month = {Jun 1}, pages = {2693-707}, abstract = {Here we investigate the interplay between intrinsic mechanical and neural factors in muscle contractile performance during running, which has been less studied than during walking. We report in vivo recordings of the gastrocnemius muscle of the guinea fowl (Numida meleagris), during the response and recovery from an unexpected drop in terrain. Previous studies on leg and joint mechanics following this perturbation suggested that distal leg extensor muscles play a key role in stabilisation. Here, we test this through direct recordings of gastrocnemius fascicle length (using sonomicrometry), muscle-tendon force (using buckle transducers), and activity (using indwelling EMG). Muscle recordings were analysed from the stride just before to the second stride following the perturbation. The gastrocnemius exhibits altered force and work output in the perturbed and first recovery strides. Muscle work correlates strongly with leg posture at the time of ground contact. When the leg is more extended in the drop step, net gastrocnemius work decreases (-5.2 J kg(-1) versus control), and when the leg is more flexed in the step back up, it increases (+9.8 J kg(-1) versus control). The muscle{\textquoteright}s work output is inherently stabilising because it pushes the body back toward its pre-perturbation (level running) speed and leg posture. Gastrocnemius length and force return to level running means by the second stride following the perturbation. EMG intensity differs significantly from level running only in the first recovery stride following the perturbation, not within the perturbed stride. The findings suggest that intrinsic mechanical factors contribute substantially to the initial changes in muscle force and work. The statistical results suggest that a history-dependent effect, shortening deactivation, may be an important factor in the intrinsic mechanical changes, in addition to instantaneous force-velocity and force-length effects. This finding suggests the potential need to incorporate history-dependent muscle properties into neuromechanical simulations of running, particularly if high muscle strains are involved and stability characteristics are important. Future work should test whether a Hill or modified Hill type model provides adequate prediction in such conditions. Interpreted in light of previous studies on walking, the findings support the concept of speed-dependent roles of reflex feedback.}, keywords = {*Gait, *Muscle Contraction, *Muscle Strength, *Running, Animals, Biomechanical Phenomena, Electromyography, Female, Galliformes/*physiology, Lower Extremity, Muscle, Skeletal/*innervation, Postural Balance, Recovery of Function, Reflex, Time Factors}, isbn = {1469-7793 (Electronic)0022-3751 (Linking)}, author = {Daley, M. A. and Voloshina, A. and Biewener, A. A.} } @article {548231, title = {Mono- versus biarticular muscle function in relation to speed and gait changes: in vivo analysis of the goat triceps brachii}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {212}, number = {Pt 20}, year = {2009}, note = {Carroll, Andrew MBiewener, Andrew AengAR-047679/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralEngland2009/10/06 06:00J Exp Biol. 2009 Oct;212(Pt 20):3349-60. doi: 10.1242/jeb.033639.}, month = {Oct}, pages = {3349-60}, abstract = {The roles of muscles that span a single joint (monoarticular) versus those that span two (biarticular) or more joints have been suggested to differ. Monoarticular muscles are argued to perform work at a joint, whereas biarticular muscles are argued to transfer energy while resisting moments across adjacent joints. To test these predictions, in vivo patterns of muscle activation, strain, and strain rate were compared using electromyography and sonomicrometry in two major elbow extensors, the long and lateral heads of the triceps brachii of goats (Capra hircus), across a range of speed (1-5 m s(-1)) and gait. Muscle recordings were synchronized to limb kinematics using high-speed digital video imaging (250 Hz). Measurements obtained from four goats (25-45 kg) showed that the monoarticular lateral head exhibited a stretch-shortening pattern (6.8+/-0.6\% stretch and -10.6+/-2.7\% shortening; mean+/-s.e.m. for all speeds and gaits) after being activated, which parallels the flexion-extension pattern of the elbow. By contrast, the biarticular long head shortened through most of stance (-16.4+/-3.4\%), despite elbow flexion in the first half and shoulder extension in the last half of stance. The magnitude of elbow flexion and shoulder extension increased with increasing speed (ANCOVA, P<0.05 and P<0.001), as did the magnitude and rate of active stretch of fascicles in the lateral head (P<0.001 for both). In all individuals, shortening fascicle strain rates increased with speed in the long head (P<0.001), and, in three of the four individuals, strain magnitude increased. Few independent effects of gait were found. In contrast to its expected function, the biarticular long head appears to produce positive work throughout stance, whereas the monoarticular lateral head appears to absorb work at the elbow. The biarticular anatomy of the long head may mitigate increases in muscle strain with speed in this muscle, because strain magnitude in the second phase of stance (when the shoulder extends) decreased with speed (P<0.05).}, keywords = {*Elbow Joint/anatomy \& histology/physiology, *Goats/anatomy \& histology/physiology, *Locomotion, *Muscle, Skeletal/anatomy \& histology/physiology, Animals, Biomechanical Phenomena, Electromyography, Gait/*physiology}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Carroll, A. M. and Biewener, A. A.} } @article {548536, title = {Contractile properties of the pigeon supracoracoideus during different modes of flight}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {211}, number = {Pt 2}, year = {2008}, note = {Tobalske, Bret WBiewener, Andrew AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2008/01/01 09:00J Exp Biol. 2008 Jan;211(Pt 2):170-9. doi: 10.1242/jeb.007476.}, month = {Jan}, pages = {170-9}, abstract = {The supracoracoideus (SUPRA) is the primary upstroke muscle for avian flight and is the antagonist to the downstroke muscle, the pectoralis (PECT). We studied in vivo contractile properties and mechanical power output of both muscles during take-off, level and landing flight. We measured muscle length change and activation using sonomicrometry and electromyography, and muscle force development using strain recordings on the humerus. Our results support a hypothesis that the primary role of the SUPRA is to supinate the humerus. Antagonistic forces exerted by the SUPRA and PECT overlap during portions of the wingbeat cycle, thereby offering a potential mechanism for enhancing control of the wing. Among flight modes, muscle strain was approximately the same in the SUPRA (33-40\%) and the PECT (35-42\%), whereas peak muscle stress was higher in the SUPRA (85-126 N m(-2)) than in the PECT (50-58 N m(-2)). The SUPRA mainly shortened relative to resting length and the PECT mainly lengthened. We estimated that elastic energy storage in the tendon of the SUPRA contributed between 28 and 60\% of the net work of the SUPRA and 6-10\% of the total net mechanical work of both muscles. Mechanical power output in the SUPRA was congruent with the estimated inertial power required for upstroke, but power output from the PECT was only 42-46\% of the estimated aerodynamic power requirements for flight. There was a significant effect of flight mode upon aspects of the contractile behavior of both muscles including strain, strain rate, peak stress, work and power.}, keywords = {Animals, Biomechanical Phenomena, Columbidae/*physiology, Flight, Animal/*physiology, Muscle Contraction/*physiology, Muscle, Skeletal/*physiology, Video Recording}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Tobalske, B. W. and Biewener, A. A.} } @article {548466, title = {Hind limb scaling of kangaroos and wallabies (superfamily Macropodoidea): implications for hopping performance, safety factor and elastic savings}, journal = {J AnatJ AnatJ Anat}, volume = {212}, number = {2}, year = {2008}, note = {McGowan, C PSkinner, JBiewener, A AengResearch Support, Non-U.S. Gov{\textquoteright}tEngland2007/12/19 09:00J Anat. 2008 Feb;212(2):153-63. Epub 2007 Dec 13.}, month = {Feb}, pages = {153-63}, abstract = {The aim of this study was to examine hind limb scaling of the musculoskeletal system in the Macropodoidea, the superfamily containing wallabies and kangaroos, to re-examine the effect of size on the locomotor mechanics and physiology of marsupial hopping. Morphometric musculoskeletal analyses were conducted of 15 species and skeletal specimens of 21 species spanning a size range from 0.8 to 80 kg that included representatives of 12 of the 16 extant genera of macropodoids. We found that unlike other groups, macropodoids are able to match force demands associated with increasing body size primarily through a combination of positive allometry in muscle area and muscle moment arms. Isometric scaling of primary hind limb bones suggests, however, that larger species experience relatively greater bone stresses. Muscle to tendon area ratios of the ankle extensors scale with strong positive allometry, indicating that peak tendon stresses also increase with increasing body size but to a lesser degree than previously reported. Consistent with previous morphological and experimental studies, large macropodoids are therefore better suited for elastic strain energy recovery but operate at lower safety factors, which likely poses an upper limit to body size. Scaling patterns for extant macropodoids suggest that extinct giant kangaroos (approximately 250 kg) were likely limited in locomotor capacity.}, keywords = {Acceleration, Animals, Biomechanical Phenomena, Elasticity, Energy Metabolism, Hindlimb/*anatomy \& histology/physiology, Locomotion/*physiology, Macropodidae/*anatomy \& histology/physiology, Models, Biological, Muscle, Skeletal/*anatomy \& histology/physiology, Risk Factors, Species Specificity, Statistics as Topic}, isbn = {1469-7580 (Electronic)0021-8782 (Linking)}, author = {McGowan, C. P. and Skinner, J. and Biewener, A. A.} } @article {548476, title = {Variability in forelimb bone strains during non-steady locomotor activities in goats}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {211}, number = {Pt 7}, year = {2008}, note = {Moreno, Carlos AMain, Russell PBiewener, Andrew AengEngland2008/03/18 09:00J Exp Biol. 2008 Apr;211(Pt 7):1148-62. doi: 10.1242/jeb.012419.}, month = {Apr}, pages = {1148-62}, abstract = {The purpose of this study was to investigate the effects of non-steady locomotor activities on load predictability in two goat forelimb bones and to explore the degree to which bone curvature influences load predictability. We measured in vivo bone strains in the radius and metacarpus of juvenile goats performing a variety of natural behaviors in an outdoor arena and compared these strain magnitudes and loading patterns with those measured during steady-state treadmill locomotion. We sought to test two hypotheses: our first hypothesis expects an increase in the variability of strain magnitude and pattern during outdoor non-steady behavior when compared to treadmill locomotion. Our second hypothesis was that the curved radius experiences higher peak strains but less variability during non-steady activities than the straighter metacarpus. We found that unsteady, outdoor locomotion generally caused more variable strain patterns (consistent with the first hypothesis), but not more variable strain magnitudes, than treadmill locomotion in both bones. During outdoor locomotion, higher magnitude strain events in the radius showed more constrained loading patterns than in the metacarpus (consistent with the second hypothesis). In addition to the radius experiencing significantly greater bending strains compared to the straighter metacarpus, these results support the idea of a trade-off between increased predictability of loading pattern and increased bending-induced strain. Strain magnitudes recorded during both outdoor and treadmill locomotion showed a lognormal frequency distribution, but the outdoor bone strain distributions had a greater range because they included high magnitude loading events that did not occur during steady treadmill locomotion.}, keywords = {Animals, Behavior, Animal, Bone and Bones/*physiopathology, Compressive Strength, Forelimb/*physiopathology, Goats/*physiology, Motor Activity/*physiology, Organ Size, Physical Conditioning, Animal, Sprains and Strains/*physiopathology, Tensile Strength, Weight-Bearing}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Moreno, C. A. and Main, R. P. and Biewener, A. A.} } @article {548451, title = {Differential design for hopping in two species of wallabies}, journal = {Comp Biochem Physiol A Mol Integr PhysiolComp Biochem Physiol A Mol Integr PhysiolComp Biochem Physiol A Mol Integr Physiol}, volume = {150}, number = {2}, year = {2008}, note = {McGowan, C PBaudinette, R VBiewener, A AengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.2006/07/25 09:00Comp Biochem Physiol A Mol Integr Physiol. 2008 Jun;150(2):151-8. Epub 2006 Jun 21.}, month = {Jun}, pages = {151-8}, abstract = {Hindlimb musculoskeletal anatomy and steady speed over ground hopping mechanics were compared in two species of macropod marsupials, tammar wallabies and yellow-footed rock wallabies (YFRW). These two species are relatively closely related and are of similar size and general body plan, yet they inhabit different environments with presumably different musculoskeletal demands. Tammar wallabies live in relatively flat, open habitat whereas yellow-footed rock wallabies inhabit steep cliff faces. The goal of this study was to explore musculoskeletal differences between tammar wallabies and yellow-footed rock wallabies and determine how these differences influence each species{\textquoteright} hopping mechanics. We found the cross-sectional area of the combined ankle extensor tendons of yellow-footed rock wallabies was 13\% greater than that of tammar wallabies. Both species experienced similar ankle joint moments during steady-speed hopping, however due to a lower mechanical advantage at this joint, tammar wallabies produced 26\% more muscle force. Thus, during moderate speed hopping, yellow-footed rock wallabies operated with 38\% higher tendon safety factors, while tammar wallabies were able to store 73\% more elastic strain energy (2.18 J per leg vs. 1.26 J in YFRW). This likely reflects the differing demands of the environments inhabited by these two species, where selection for non-steady locomotor performance in rocky terrain likely requires trade-offs in locomotor economy.}, keywords = {Animals, Biomechanical Phenomena, Female, Foot Joints/physiology, Hindlimb/physiology, Locomotion/*physiology, Macropodidae/*physiology, Male, Muscle, Skeletal/physiology, Tendons/physiology, Tomography, X-Ray Computed}, isbn = {1531-4332 (Electronic)1095-6433 (Linking)}, author = {McGowan, C. P. and Baudinette, R. V. and Biewener, A. A.} } @article {548396, title = {Compliance, actuation, and work characteristics of the goat foreleg and hindleg during level, uphill, and downhill running}, journal = {J Appl Physiol (1985)J Appl Physiol (1985)J Appl Physiol (1985)}, volume = {104}, number = {1}, year = {2008}, note = {Lee, David VMcGuigan, M PollyYoo, Edwin HBiewener, Andrew AengAR-047679/AR/NIAMS NIH HHS/R01 AR047679/AR/NIAMS NIH HHS/R01 AR047679-05/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Bethesda, Md. : 19852007/10/20 09:00J Appl Physiol (1985). 2008 Jan;104(1):130-41. Epub 2007 Oct 18.}, month = {Jan}, pages = {130-41}, abstract = {We model the action of muscle-tendon system(s) about a given joint as a serial actuator and spring. By this technique, the experimental joint moment is imposed while the combined angular deflection of the actuator and spring are constrained to match the experimental joint angle throughout the stance duration. The same technique is applied to the radial leg (i.e., shoulder/hip-to-foot). The spring constant that minimizes total actuator work is considered optimal, and this minimum work is expressed as a fraction of total joint/radial leg work, yielding an actuation ratio (AR; 1 = pure actuation and 0 = pure compliance). To address work modulation, we determined the specific net work (SNW), the absolute value of net divided by total work. This ratio is unity when only positive or negative work is done and zero when equal energy is absorbed and returned. Our proximodistal predictions of joint function are supported during level and 15 degrees grade running. The greatest AR and SNW are found in the proximal leg joints (elbow and knee). The ankle joint is the principal spring of the hindleg and shows no significant change in SNW with grade, reflecting the true compliance of the common calcaneal tendon. The principal foreleg spring is the metacarpophalangeal joint. The observed pattern of proximal actuation and distal compliance, as well as the substantial SNW at proximal joints, minimal SNW at intermediate joints, and variable energy absorption at distal joints, may emerge as general principles in quadruped limb mechanics and help to inform the leg designs of highly capable running robots.}, keywords = {*Running, Animals, Biomechanical Phenomena, Compliance, Female, Forelimb, Goats, Hindlimb, Joints/*physiology, Models, Biological, Muscle, Skeletal/*physiology, Physical Exertion/*physiology, Range of Motion, Articular, Tendons/*physiology, Weight-Bearing}, isbn = {8750-7587 (Print)0161-7567 (Linking)}, author = {Lee, D. V. and McGuigan, M. P. and Yoo, E. H. and Biewener, A. A.} } @article {548356, title = {Functional diversification within and between muscle synergists during locomotion}, journal = {Biol LettBiol LettBiol Lett}, volume = {4}, number = {1}, year = {2008}, note = {Higham, Timothy EBiewener, Andrew AWakeling, James MengResearch Support, N.I.H., ExtramuralEngland2007/11/08 09:00Biol Lett. 2008 Feb 23;4(1):41-4.}, month = {Feb 23}, pages = {41-4}, abstract = {Locomotion arises from the complex and coordinated function of limb muscles. Yet muscle function is dynamic over the course of a single stride and between strides for animals moving at different speeds or on variable terrain. While it is clear that motor unit recruitment can vary between and within muscles, we know little about how work is distributed within and between muscles under in vivo conditions. Here we show that the lateral gastrocnemius (LG) of helmeted guinea fowl (Numida meleagris) performs considerably more work than its synergist, the medial gastrocnemius (MG) and that the proximal region of the MG (pMG) performs more work than the distal region (dMG). Positive work done by the LG was approximately twice that of the proximal MG when the birds walked at 0.5 ms -1, and four times when running at 2.0 m s-1. This is probably due to different moments at the knee, as well as differences in motor unit recruitment. The dMG performed less work than the pMG because its apparent dynamic stiffness was greater, and because it exhibited a greater recruitment of slow-twitch fibres. The greater compliance of the pMG leads to increased stretch of its fascicles at the onset of force, further enhancing force production. Our results demonstrate the capacity for functional diversity between and within muscle synergists, which increases with changes in gait and speed.}, keywords = {Animals, Galliformes/*physiology, Muscle, Skeletal/*physiology, Running/*physiology, Walking/*physiology}, isbn = {1744-9561 (Print)1744-9561 (Linking)}, author = {Higham, T. E. and Biewener, A. A. and Wakeling, J. M.} } @article {548336, title = {Integration within and between muscles during terrestrial locomotion: effects of incline and speed}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {211}, number = {Pt 14}, year = {2008}, note = {Higham, Timothy EBiewener, Andrew AengR01-AR047679/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralEngland2008/07/01 09:00J Exp Biol. 2008 Jul;211(Pt 14):2303-16. doi: 10.1242/jeb.016139.}, month = {Jul}, pages = {2303-16}, abstract = {Animals must continually adapt to varying locomotor demands when moving in their natural habitat. Despite the dynamic nature of locomotion, little is known about how multiple muscles, and different parts of a muscle, are functionally integrated as demand changes. In order to determine the extent to which synergist muscles are functionally heterogeneous, and whether this heterogeneity is altered with changes in demand, we examined the in vivo function of the lateral (LG) and medial (MG) gastrocnemius muscles of helmeted guinea fowl (Numida meleagris) during locomotion on different inclines (level and uphill at 14 degrees ) and at different speeds (0.5 and 2.0 m s(-1)). We also quantified function in the proximal (pMG) and distal (dMG) regions of the MG to examine the extent to which a single muscle is heterogeneous. We used electromyography, sonomicrometry and tendon force buckles to quantify activation, length change and force patterns of both muscles, respectively. We show that the LG and MG exhibited an increase in force and stress with a change in gait and an increase in locomotor speed, but not with changes in incline. While the LG and MG exhibited similar levels of stress when walking at 0.5 m s(-1), stress in the LG was 1.8 times greater than in the MG when running at 2.0 m s(-1). Fascicle shortening increased with an increase in speed on both inclines for the LG, but only on the level for the pMG. Positive work performed by the LG exceeded that of the pMG and dMG for all conditions, and this difference was magnified when locomotor speed increased. Within the MG, the pMG shortened more, and at a faster rate than the dMG, resulting in a greater amount of positive work performed by the pMG. Mean spike amplitude of the electromyogram (EMG) bursts increased for all muscle locations with an increase in speed, but changes with incline were more variable. The functional differences between the LG and MG are likely due to the different moments each exerts at the knee, as well as differences in motor unit recruitment. The differences within the MG are likely due to motor unit recruitment differences, but also differences in architecture. Fascicles within the dMG insert into an extensive aponeurosis, which results in a higher apparent dynamic stiffness relative to fascicles operating within the pMG. On the level surface, the greater compliance of the pMG leads to increased stretch of its fascicles at the onset of force, further enhancing force production. Our results demonstrate the capacity for functional diversity between and within muscle synergists, which occur with changes in gait, speed and grade.}, keywords = {Animals, Biomechanical Phenomena, Electromyography, Gait/physiology, Galliformes/*physiology, Locomotion/*physiology, Muscle Contraction/physiology, Muscle, Skeletal/anatomy \& histology/physiology, Physical Exertion, Tarsus, Animal/physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Higham, T. E. and Biewener, A. A.} } @article {548236, title = {Differential muscle function between muscle synergists: long and lateral heads of the triceps in jumping and landing goats (Capra hircus)}, journal = {J Appl Physiol (1985)J Appl Physiol (1985)J Appl Physiol (1985)}, volume = {105}, number = {4}, year = {2008}, note = {Carroll, Andrew MLee, David VBiewener, Andrew AengAR 047679/AR/NIAMS NIH HHS/Comparative StudyResearch Support, N.I.H., ExtramuralBethesda, Md. : 19852008/07/26 09:00J Appl Physiol (1985). 2008 Oct;105(4):1262-73. doi: 10.1152/japplphysiol.01316.2007. Epub 2008 Jul 24.}, month = {Oct}, pages = {1262-73}, abstract = {We investigate how the biarticular long head and monoarticular lateral head of the triceps brachii function in goats (Capra hircus) during jumping and landing. Elbow moment and work were measured from high-speed video and ground reaction force (GRF) recordings. Muscle activation and strain were measured via electromyography and sonomicrometry, and muscle stress was estimated from elbow moment and by partitioning stress based on its relative strain rate. Elbow joint and muscle function were compared among three types of limb usage: jump take-off (lead limb), the step prior to jump take-off (lag limb), and landing. We predicted that the strain and work patterns in the monoarticular lateral head would follow the kinematics and work of the elbow more closely than would those of the biarticular long head. In general this prediction was supported. For instance, the lateral head stretched (5 +/- 2\%; mean +/- SE) in the lead and lag limbs to absorb work during elbow flexion and joint work absorption, while the long head shortened (-7 +/- 1\%) to produce work. During elbow extension, both muscles shortened by similar amounts (-10 +/- 2\% long; -13 +/- 4\% lateral) in the lead limb to produce work. Both triceps heads functioned similarly in landing, stretching (13 +/- 3\% in the long head and 19 +/- 5\% in the lateral) to absorb energy. In general, the long head functioned to produce power at the shoulder and elbow, while the lateral head functioned to resist elbow flexion and absorb work, demonstrating that functional diversification can arise between mono- and biarticular muscle agonists operating at the same joint.}, keywords = {*Motor Activity, *Muscle Contraction, *Muscle Strength, Animals, Electromyography, Forelimb, Goats, Joints/*physiology, Models, Biological, Muscle, Skeletal/anatomy \& histology/*physiology, Stress, Mechanical, Video Recording}, isbn = {8750-7587 (Print)0161-7567 (Linking)}, author = {Carroll, A. M. and Lee, D. V. and Biewener, A. A.} } @article {548026, title = {Kinematics and power requirements of ascending and descending flight in the pigeon (Columba livia)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {211}, number = {Pt 7}, year = {2008}, note = {Berg, Angela MBiewener, Andrew AengEngland2008/03/18 09:00J Exp Biol. 2008 Apr;211(Pt 7):1120-30. doi: 10.1242/jeb.010413.}, month = {Apr}, pages = {1120-30}, abstract = {Ascending or descending locomotion involves a change in potential energy (PE) and a corresponding change in power requirement. We sought to test whether the mechanical power required for steady ascending or descending flight is a simple sum of the power required for level flight and the power necessary for potential energy change. Pigeons (Columba livia) were trained to fly at varying angles of ascent and descent (60 degrees , 30 degrees , 0 degrees , -30 degrees , -60 degrees ), and were recorded using high-speed video. Detailed three-dimensional kinematics were obtained from the recordings, allowing analysis of wing movement. Aerodynamic forces and power requirements were then estimated from kinematic data. As expected, ;PE flight power{\textquoteright} increased significantly with angle of flight (0.234 W deg.(-1)), though there appeared to be a limit on the amount of PE that the birds could gain or dissipate per wingbeat. We found that the total power output for flight at various angles was not different from the sum of power required for level flight and the PE rate of change for a given angle, except for the steep -60 degrees descent. The total power for steep descent was higher than this sum because of a higher induced power due to the bird{\textquoteright}s deceleration and slower flight velocity. Aerodynamic force estimates during mid-downstroke did not differ significantly in magnitude or orientation among flight angles. Pigeons flew fastest during -30 degrees flights (4.9+/-0.1 m s(-1)) and slowest at 60 degrees (2.9+/-0.1 m s(-1)). Although wingbeat frequency ranged from 6.1 to 9.6 Hz across trials, the variation was not significant across flight angles. Stroke plane angle was more horizontal, and the wing more protracted, for both +60 degrees and -60 degrees flights, compared with other flight path angles.}, keywords = {Animals, Biomechanical Phenomena, Columbidae/anatomy \& histology/*physiology, Flight, Animal/*physiology, Models, Biological, Wing/anatomy \& histology/physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Berg, A. M. and Biewener, A. A.} } @article {548551, title = {Three-dimensional kinematics of hummingbird flight}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {210}, number = {Pt 13}, year = {2007}, note = {Tobalske, Bret WWarrick, Douglas RClark, Christopher JPowers, Donald RHedrick, Tyson LHyder, Gabriel ABiewener, Andrew AengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2007/06/19 09:00J Exp Biol. 2007 Jul;210(Pt 13):2368-82.}, month = {Jul}, pages = {2368-82}, abstract = {Hummingbirds are specialized for hovering flight, and substantial research has explored this behavior. Forward flight is also important to hummingbirds, but the manner in which they perform forward flight is not well documented. Previous research suggests that hummingbirds increase flight velocity by simultaneously tilting their body angle and stroke-plane angle of the wings, without varying wingbeat frequency and upstroke: downstroke span ratio. We hypothesized that other wing kinematics besides stroke-plane angle would vary in hummingbirds. To test this, we used synchronized high-speed (500 Hz) video cameras and measured the three-dimensional wing and body kinematics of rufous hummingbirds (Selasphorus rufus, 3 g, N=5) as they flew at velocities of 0-12 m s(-1) in a wind tunnel. Consistent with earlier research, the angles of the body and the stroke plane changed with velocity, and the effect of velocity on wingbeat frequency was not significant. However, hummingbirds significantly altered other wing kinematics including chord angle, angle of attack, anatomical stroke-plane angle relative to their body, percent of wingbeat in downstroke, wingbeat amplitude, angular velocity of the wing, wingspan at mid-downstroke, and span ratio of the wingtips and wrists. This variation in bird-centered kinematics led to significant effects of flight velocity on the angle of attack of the wing and the area and angles of the global stroke planes during downstroke and upstroke. We provide new evidence that the paths of the wingtips and wrists change gradually but consistently with velocity, as in other bird species that possess pointed wings. Although hummingbirds flex their wings slightly at the wrist during upstroke, their average wingtip-span ratio of 93\% revealed that they have kinematically ;rigid{\textquoteright} wings compared with other avian species.}, keywords = {Animals, Biomechanical Phenomena, Birds/*physiology, Female, Flight, Animal/*physiology, Wing/physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Tobalske, B. W. and Warrick, D. R. and Clark, C. J. and Powers, D. R. and Hedrick, T. L. and Hyder, G. A. and Biewener, A. A.} } @article {548501, title = {Modulation of in vivo muscle power output during swimming in the African clawed frog (Xenopus laevis)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {210}, number = {Pt 18}, year = {2007}, note = {Richards, Christopher TBiewener, Andrew AengEngland2007/09/04 09:00J Exp Biol. 2007 Sep;210(Pt 18):3147-59.}, month = {Sep}, pages = {3147-59}, abstract = {The goal of this study is to explore how swimming animals produce the wide range of performance that is seen across their natural behaviors. In vivo recordings of plantaris longus muscle length change were obtained by sonomicrometry. Simultaneous with muscle length data, force measurements were obtained using a novel tendon buckle force transducer placed on the Achilles tendon of Xenopus laevis frogs during brief accelerating bursts of swimming. In vivo work loops revealed that the plantaris generates a variable amount of positive muscle work over a range of swimming cycle durations (from 0.23 to 0.76 s), resulting in a large range of cycle power output (from 2.32 to 74.17 W kg(-1) muscle). Cycle duration correlated negatively with cycle power, and cycle work correlated positively (varying as a function of peak cycle stress and, to a much lesser extent, fascicle strain amplitude). However, variation in cycle duration only contributed to 12\% of variation in power, with cycle work accounting for the remaining 88\%. Peak cycle stress and strain amplitude were also highly variable, yet peak stress was a much stronger predictor of cycle work than strain amplitude. Additionally, EMG intensity correlated positively with peak muscle stress (r(2)=0.53). Although the timing of muscle recruitment (EMG phase and EMG duty cycle) varied considerably within and among frogs, neither parameter correlated strongly with cycle power, cycle work, peak cycle stress or strain amplitude. These results suggest that relatively few parameters (cycle duration, peak cycle stress and strain amplitude) vary to permit a wide range of muscle power output, which allows anurans to swim over a large range of velocities and accelerations.}, keywords = {Animals, Biomechanical Phenomena, Electromyography, Female, Muscle, Skeletal/*physiology, Physical Exertion, Swimming/*physiology, Xenopus laevis/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Richards, C. T. and Biewener, A. A.} } @article {548481, title = {Neuromechanics: an integrative approach for understanding motor control}, journal = {Integr Comp BiolIntegr Comp BiolIntegr Comp Biol}, volume = {47}, number = {1}, year = {2007}, note = {Nishikawa, KiisaBiewener, Andrew AAerts, PeterAhn, Anna NChiel, Hillel JDaley, Monica ADaniel, Thomas LFull, Robert JHale, Melina EHedrick, Tyson LLappin, A KristopherNichols, T RichardQuinn, Roger DSatterlie, Richard ASzymik, BrettengEngland2007/07/01 00:00Integr Comp Biol. 2007 Jul;47(1):16-54. Epub 2007 May 27.}, month = {Jul}, pages = {16-54}, abstract = {Neuromechanics seeks to understand how muscles, sense organs, motor pattern generators, and brain interact to produce coordinated movement, not only in complex terrain but also when confronted with unexpected perturbations. Applications of neuromechanics include ameliorating human health problems (including prosthesis design and restoration of movement following brain or spinal cord injury), as well as the design, actuation and control of mobile robots. In animals, coordinated movement emerges from the interplay among descending output from the central nervous system, sensory input from body and environment, muscle dynamics, and the emergent dynamics of the whole animal. The inevitable coupling between neural information processing and the emergent mechanical behavior of animals is a central theme of neuromechanics. Fundamentally, motor control involves a series of transformations of information, from brain and spinal cord to muscles to body, and back to brain. The control problem revolves around the specific transfer functions that describe each transformation. The transfer functions depend on the rules of organization and operation that determine the dynamic behavior of each subsystem (i.e., central processing, force generation, emergent dynamics, and sensory processing). In this review, we (1) consider the contributions of muscles, (2) sensory processing, and (3) central networks to motor control, (4) provide examples to illustrate the interplay among brain, muscles, sense organs and the environment in the control of movement, and (5) describe advances in both robotics and neuromechanics that have emerged from application of biological principles in robotic design. Taken together, these studies demonstrate that (1) intrinsic properties of muscle contribute to dynamic stability and control of movement, particularly immediately after perturbations; (2) proprioceptive feedback reinforces these intrinsic self-stabilizing properties of muscle; (3) control systems must contend with inevitable time delays that can simplify or complicate control; and (4) like most animals under a variety of circumstances, some robots use a trial and error process to tune central feedforward control to emergent body dynamics.}, isbn = {1540-7063 (Print)1540-7063 (Linking)}, author = {Nishikawa, K. and Biewener, A. A. and Aerts, P. and Ahn, A. N. and Chiel, H. J. and Daley, M. A. and Daniel, T. L. and Full, R. J. and Hale, M. E. and Hedrick, T. L. and Lappin, A. K. and Nichols, T. R. and Quinn, R. D. and Satterlie, R. A. and Szymik, B.} } @article {548446, title = {Modulation of proximal muscle function during level versus incline hopping in tammar wallabies (Macropus eugenii)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {210}, number = {Pt 7}, year = {2007}, note = {McGowan, C PBaudinette, R VBiewener, A AengComparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2007/03/21 09:00J Exp Biol. 2007 Apr;210(Pt 7):1255-65.}, month = {Apr}, pages = {1255-65}, abstract = {We examined the functional role of two major proximal leg extensor muscles of tammar wallabies during level and inclined hopping (12 degrees, 21.3\% grade). Previous in vivo studies of hopping wallabies have revealed that, unlike certain avian bipeds, distal hindlimb muscles do not alter their force-length behavior to contribute positive work during incline hopping. This suggests that proximal muscles produce the increased mechanical work associated with moving up an incline. Based on relative size and architectural anatomy, we hypothesized that the biceps femoris (BF), primarily a hip extensor, and the vastus lateralis (VL), the main knee extensor, would exhibit changes in muscle strain and activation patterns consistent with increased work production during incline versus level hopping. Our results clearly support this hypothesis. The BF experienced similar activation patterns during level and incline hopping but net fascicle shortening increased (-0.5\% for level hopping versus -4.2\% for incline hopping) during stance when the muscle likely generated force. Unlike the BF, the VL experienced active net lengthening during stance, indicating that it absorbs energy during both level and incline hopping. However, during incline hopping, net lengthening was reduced (8.3\% for level hopping versus 3.9\% for incline hopping), suggesting that the amount of energy absorbed by the VL was reduced. Consequently, the changes in contractile behavior of these two muscles are consistent with a net production of work by the whole limb. A subsidiary aim of our study was to explore possible regional variation within the VL. Although there was slightly higher fascicle strain in the proximal VL compared with the distal VL, regional differences in strain were not significant, suggesting that the overall pattern of in vivo strain is fairly uniform throughout the muscle. Estimates of muscle work based on inverse dynamics calculations support the conclusion that both the BF and VL contribute to the additional work required for incline hopping. However, on a muscle mass-specific basis, these two muscles appear to contribute less than their share. This indicates that other hindlimb muscles, or possibly trunk and back muscles, must contribute substantial work during incline hopping.}, keywords = {Animals, Biomechanical Phenomena, Electromyography, Hindlimb/*physiology, Joints/physiology, Linear Models, Locomotion/*physiology, Macropodidae/*physiology, Muscle Contraction/*physiology, Muscle, Skeletal/*physiology, Video Recording}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {McGowan, C. P. and Baudinette, R. V. and Biewener, A. A.} } @article {548436, title = {Skeletal strain patterns and growth in the emu hindlimb during ontogeny}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {210}, number = {Pt 15}, year = {2007}, note = {Main, Russell PBiewener, Andrew AengResearch Support, Non-U.S. Gov{\textquoteright}tEngland2007/07/24 09:00J Exp Biol. 2007 Aug;210(Pt 15):2676-90.}, month = {Aug}, pages = {2676-90}, abstract = {Most studies examining changes in mechanical performance in animals across size have typically focused on inter-specific comparisons across large size ranges. Scale effects, however, can also have important consequences in vertebrates as they increase in size and mass during ontogeny. The goal of this study was to examine how growth and development in the emu (Dromaius novaehollandiae) hindlimb skeleton reflects the demands placed upon it by ontogenetic changes in locomotor mechanics and body mass. Bone strain patterns in the femur and tibiotarsus (TBT) were related to ontogenetic changes in limb kinematics, ground reaction forces, and ontogenetic scaling patterns of the cross-sectional bone geometry, curvature and mineral ash content over a 4.4-fold increase in leg length and 65-fold increase in mass. Although the distribution of principal and axial strains remained similar in both bones over the ontogenetic size range examined, principal strains on the cranial femur and caudal femur and TBT increased significantly during growth. The ontogenetic increase in principal strains in these bones was likely caused by isometry or only slight positive allometry in bone cross-sectional geometry during growth, while relative limb loading remained similar. The growth-related increase in bone strain magnitude was likely mitigated by increased bone mineralization and decreased curvature. Throughout most of ontogeny, shear strains dominated loading in both bones. This was reflected in the nearly circular cross-sectional geometry of the femur and TBT, suggesting selection for resistance to high torsional loads, as opposed to the more eccentric cross-sectional geometries often associated with the bending common to tetrapods with parasagittal limb orientations, for which in vivo bone strains have typically been measured to date.}, keywords = {Animals, Biomechanical Phenomena, Dromaiidae/anatomy \& histology/*growth \& development/*physiology, Hindlimb/anatomy \& histology/*growth \& development/*physiology, Muscle, Skeletal, Stress, Mechanical}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Main, R. P. and Biewener, A. A.} } @article {548331, title = {Low speed maneuvering flight of the rose-breasted cockatoo (Eolophus roseicapillus). II. Inertial and aerodynamic reorientation}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {210}, number = {Pt 11}, year = {2007}, note = {Hedrick, T LUsherwood, J RBiewener, A AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2007/05/23 09:00J Exp Biol. 2007 Jun;210(Pt 11):1912-24.}, month = {Jun}, pages = {1912-24}, abstract = {The reconfigurable, flapping wings of birds allow for both inertial and aerodynamic modes of reorientation. We found evidence that both these modes play important roles in the low speed turning flight of the rose-breasted cockatoo Eolophus roseicapillus. Using three-dimensional kinematics recorded from six cockatoos making a 90 degrees turn in a flight corridor, we developed predictions of inertial and aerodynamic reorientation from estimates of wing moments of inertia and flapping arcs, and a blade-element aerodynamic model. The blade-element model successfully predicted weight support (predicted was 88+/-17\% of observed, N=6) and centripetal force (predicted was 79+/-29\% of observed, N=6) for the maneuvering cockatoos and provided a reasonable estimate of mechanical power. The estimated torque from the model was a significant predictor of roll acceleration (r(2)=0.55, P<0.00001), but greatly overestimated roll magnitude when applied with no roll damping. Non-dimensional roll damping coefficients of approximately -1.5, 2-6 times greater than those typical of airplane flight dynamics (approximately -0.45), were required to bring our estimates of reorientation due to aerodynamic torque back into conjunction with the measured changes in orientation. Our estimates of inertial reorientation were statistically significant predictors of the measured reorientation within wingbeats (r(2) from 0.2 to 0.37, P<0.0005). Components of both our inertial reorientation and aerodynamic torque estimates correlated, significantly, with asymmetries in the activation profile of four flight muscles: the pectoralis, supracoracoideus, biceps brachii and extensor metacarpi radialis (r(2) from 0.27 to 0.45, P<0.005). Thus, avian flight maneuvers rely on production of asymmetries throughout the flight apparatus rather than in a specific set of control or turning muscles.}, keywords = {Animals, Biomechanical Phenomena, Cockatoos/*physiology, Flight, Animal/*physiology, Muscle, Skeletal/physiology, Wing/anatomy \& histology/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Hedrick, T. L. and Usherwood, J. R. and Biewener, A. A.} } @article {548306, title = {Low speed maneuvering flight of the rose-breasted cockatoo (Eolophus roseicapillus). I. Kinematic and neuromuscular control of turning}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {210}, number = {Pt 11}, year = {2007}, note = {Hedrick, T LBiewener, A AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2007/05/23 09:00J Exp Biol. 2007 Jun;210(Pt 11):1897-911.}, month = {Jun}, pages = {1897-911}, abstract = {Maneuvering flight has long been recognized as an important component of the natural behavior of many bird species, but has been the subject of little experimental work. Here we examine the kinematics and neuromuscular control of turning flight in the rose-breasted cockatoo Eolophus roseicapillus (N=6), testing predictions of maneuvering flight and control based on aerodynamic theory and prior kinematic and neuromuscular studies. Six cockatoos were trained to navigate between two perches placed in an L-shaped flight corridor, making a 90 degrees turn midway through each flight. Flights were recorded with three synchronized high-speed video cameras placed outside the corridor, allowing a three-dimensional reconstruction of wing and body kinematics through the turn. We simultaneously collected electromyography recordings from bilateral implants in the pectoralis, supracoracoideus, biceps brachii and extensor metacarpi radialis muscles. The cockatoos maneuvered using flapping, banked turns with an average turn radius of 0.92 m. The mean rate of change in heading during a complete wingbeat varied through the turn and was significantly correlated to roll angle at mid-downstroke. Changes in roll angle were found to include both within-wingbeat and among-wingbeat components that bear no direct relationship to one another. Within-wingbeat changes in roll were dominated by the inertial effects while among-wingbeat changes in roll were likely the result of both inertial and aerodynamic effects.}, keywords = {Animals, Biomechanical Phenomena, Cockatoos/*physiology, Electromyography, Flight, Animal/*physiology, Pectoralis Muscles/innervation/physiology, Wing/anatomy \& histology/innervation/physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Hedrick, T. L. and Biewener, A. A.} } @article {548261, title = {Running stability is enhanced by a proximo-distal gradient in joint neuromechanical control}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {210}, number = {Pt 3}, year = {2007}, note = {Daley, M AFelix, GBiewener, A AengR01 AR047679/AR/NIAMS NIH HHS/R01 AR047679-05/AR/NIAMS NIH HHS/R01-AR047679/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, Non-U.S. Gov{\textquoteright}tEngland2007/01/20 09:00J Exp Biol. 2007 Feb;210(Pt 3):383-94.}, month = {Feb}, pages = {383-94}, abstract = {We currently know little about how animals achieve dynamic stability when running over uneven and unpredictable terrain, often characteristic of their natural environment. Here we investigate how limb and joint mechanics of an avian biped, the helmeted guinea fowl Numida meleagris, respond to an unexpected drop in terrain during running. In particular, we address how joint mechanics are coordinated to achieve whole limb dynamics. Based on muscle-tendon architecture and previous studies of steady and incline locomotion, we hypothesize a proximo-distal gradient in joint neuromechanical control. In this motor control strategy, (1) proximal muscles at the hip and knee joints are controlled primarily in a feedforward manner and exhibit load-insensitive mechanical performance, and (2) distal muscles at the ankle and tarsometatarso-phalangeal (TMP) joints are highly load-sensitive, due to intrinsic mechanical effects and rapid, higher gain proprioceptive feedback. Limb kinematics and kinetics during the unexpected perturbation reveal that limb retraction, controlled largely by the hip, remains similar to level running throughout the perturbed step, despite altered limb loading. Individual joints produce or absorb energy during both level and perturbed running steps, such that the net limb work depends on the balance of energy among the joints. The hip maintains the same mechanical role regardless of limb loading, whereas the ankle and TMP switch between spring-like or damping function depending on limb posture at ground contact. Initial knee angle sets limb posture and alters the balance of work among the joints, although the knee contributes little work itself. This distribution of joint function results in posture-dependent changes in work performance of the limb, which allow guinea fowl to rapidly produce or absorb energy in response to the perturbation. The results support the hypothesis that a proximo-distal gradient exists in limb neuromuscular performance and motor control. This control strategy allows limb cycling to remain constant, whereas limb posture, loading and energy performance are interdependent. We propose that this control strategy provides simple, rapid mechanisms for managing energy and controlling velocity when running over rough terrain.}, keywords = {Animals, Biomechanical Phenomena, Galliformes/anatomy \& histology/*physiology, Joints/*physiology, Lower Extremity/physiology, Posture, Running/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Daley, M. A. and Felix, G. and Biewener, A. A.} } @article {548151, title = {Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {210}, number = {Pt 17}, year = {2007}, note = {Biewener, Andrew ADaley, Monica AengAR047679/AR/NIAMS NIH HHS/R01 AR047679/AR/NIAMS NIH HHS/R01 AR047679-05/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2007/08/21 09:00J Exp Biol. 2007 Sep;210(Pt 17):2949-60.}, month = {Sep}, pages = {2949-60}, abstract = {By integrating studies of muscle function with analysis of whole body and limb dynamics, broader appreciation of neuromuscular function can be achieved. Ultimately, such studies need to address non-steady locomotor behaviors relevant to animals in their natural environments. When animals move slowly they likely rely on voluntary coordination of movement involving higher brain centers. However, when moving fast, their movements depend more strongly on responses controlled at more local levels. Our focus here is on control of fast-running locomotion. A key observation emerging from studies of steady level locomotion is that simple spring-mass dynamics, which help to economize energy expenditure, also apply to stabilization of unsteady running. Spring-mass dynamics apply to conditions that involve lateral impulsive perturbations, sudden changes in terrain height, and sudden changes in substrate stiffness or damping. Experimental investigation of unsteady locomotion is challenging, however, due to the variability inherent in such behaviors. Another emerging principle is that initial conditions associated with postural changes following a perturbation define different context-dependent stabilization responses. Distinct stabilization modes following a perturbation likely result from proximo-distal differences in limb muscle architecture, function and control strategy. Proximal muscles may be less sensitive to sudden perturbations and appear to operate, in such circumstances, under feed-forward control. In contrast, multiarticular distal muscles operate, via their tendons, to distribute energy among limb joints in a manner that also depends on the initial conditions of limb contact with the ground. Intrinsic properties of these distal muscle-tendon elements, in combination with limb and body dynamics, appear to provide rapid initial stabilizing mechanisms that are often consistent with spring-mass dynamics. These intrinsic mechanisms likely help to simplify the neural control task, in addition to compensating for delays inherent to subsequent force- and length-dependent neural feedback. Future work will benefit from integrative biomechanical approaches that employ a combination of modeling and experimental techniques to understand how the elegant interplay of intrinsic muscle properties, body dynamics and neural control allows animals to achieve stability and agility over a variety of conditions.}, keywords = {Animals, Biomechanical Phenomena, Computer Simulation, Galliformes/anatomy \& histology/*physiology, Humans, Joints, Models, Biological, Muscle, Skeletal/*physiology, Postural Balance, Running/*physiology, Synaptic Transmission}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A. and Daley, M. A.} } @article {548461, title = {Effects of load carrying on metabolic cost and hindlimb muscle dynamics in guinea fowl (Numida meleagris)}, journal = {J Appl Physiol (1985)J Appl Physiol (1985)J Appl Physiol (1985)}, volume = {101}, number = {4}, year = {2006}, note = {McGowan, C PDuarte, H AMain, J BBiewener, A AengAR-04769/AR/NIAMS NIH HHS/R01 AR047679/AR/NIAMS NIH HHS/R01 AR047679-05/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralBethesda, Md. : 19852006/07/01 09:00J Appl Physiol (1985). 2006 Oct;101(4):1060-9. Epub 2006 Jun 29.}, month = {Oct}, pages = {1060-9}, abstract = {The goal of this study was to test whether the contractile patterns of two major hindlimb extensors of guinea fowl are altered by load-carrying exercise. We hypothesized that changes in contractile pattern, specifically a decrease in muscle shortening velocity or enhanced stretch activation, would result in a reduction in locomotor energy cost relative to the load carried. We also anticipated that changes in kinematics would reflect underlying changes in muscle strain. Oxygen consumption, muscle activation intensity, and fascicle strain rate were measured over a range of speeds while animals ran unloaded vs. when they carried a trunk load equal to 22\% of their body mass. Our results showed that loading produced no significant (P > 0.05) changes in kinematic patterns at any speed. In vivo muscle contractile strain patterns in the iliotibialis lateralis pars postacetabularis and the medial head of the gastrocnemius showed a significant increase in active stretch early in stance (P < 0.01), but muscle fascicle shortening velocity was not significantly affected by load carrying. The rate of oxygen consumption increased by 17\% (P < 0.01) during loaded conditions, equivalent to 77\% of the relative increase in mass. Additionally, relative increases in EMG intensity (quantified as mean spike amplitude) indicated less than proportional recruitment, consistent with force enhancement via stretch activation, in the proximal iliotibialis lateralis pars postacetabularis; however, a greater than proportional increase in the medial gastrocnemius was observed. As a result, when averaged for the two muscles, EMG intensity increased in direct proportion to the fractional increase in load carried.}, keywords = {Animals, Energy Metabolism/*physiology, Exercise Test, Female, Galliformes/*metabolism, Hindlimb/anatomy \& histology/physiology, Muscle Contraction/physiology, Muscle, Skeletal/anatomy \& histology/*metabolism, Physical Exertion/*physiology, Running/*physiology, Weight-Bearing/physiology}, isbn = {8750-7587 (Print)0161-7567 (Linking)}, author = {McGowan, C. P. and Duarte, H. A. and Main, J. B. and Biewener, A. A.} } @article {548431, title = {In vivo bone strain and ontogenetic growth patterns in relation to life-history strategies and performance in two vertebrate taxa: goats and emu}, journal = {Physiol Biochem ZoolPhysiol Biochem ZoolPhysiol Biochem Zool}, volume = {79}, number = {1}, year = {2006}, note = {Main, Russell PBiewener, Andrew AengResearch Support, Non-U.S. Gov{\textquoteright}t2005/12/29 09:00Physiol Biochem Zool. 2006 Jan-Feb;79(1):57-72. Epub 2005 Nov 16.}, month = {Jan-Feb}, pages = {57-72}, abstract = {This study examined ontogenetic patterns of limb loading, bone strains, and relative changes in bone geometry to explore the relationship between in vivo mechanics and size-related changes in the limb skeleton of two vertebrate taxa. Despite maintaining similar relative limb loads during ontogeny, bone strain magnitudes in the goat radius and emu tibiotarsus generally increased. However, while the strain increases in the emu tibiotarsus were mostly insignificant, strains within the radii of adult goats were two to four times greater than in young goats. The disparity between ontogenetic strain increases in these taxa resulted from differences in ontogenetic scaling patterns of the cross-sectional bone geometry. While the cross-sectional and second moments of area scaled with negative allometry in the goat radius, these measures were not significantly different from isometry in the emu tibiotarsus. Although the juveniles of both taxa exhibited lower strains and higher safety factors than the adults, the radii of the young goats were more robust relative to the adult goats than were the tibiotarsi of the young compared with adult emu. Differences in ontogenetic growth and strain patterns in the limb bones examined likely result from different threat avoidance strategies and selection pressures in the juveniles of these two taxa.}, keywords = {Animals, Biomechanical Phenomena, Body Weight, Bone and Bones/anatomy \& histology/*physiology, Bone Development/*physiology, Dromaiidae/*growth \& development/*physiology, Goats/*growth \& development/*physiology, Species Specificity}, isbn = {1522-2152 (Print)1522-2152 (Linking)}, author = {Main, R. P. and Biewener, A. A.} } @article {548266, title = {Running over rough terrain: guinea fowl maintain dynamic stability despite a large unexpected change in substrate height}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {209}, number = {Pt 1}, year = {2006}, note = {Daley, Monica AUsherwood, James RFelix, GladysBiewener, Andrew AengR01-AR047679/AR/NIAMS NIH HHS/Comparative StudyResearch Support, N.I.H., ExtramuralResearch Support, Non-U.S. Gov{\textquoteright}tEngland2005/12/16 09:00J Exp Biol. 2006 Jan;209(Pt 1):171-87.}, month = {Jan}, pages = {171-87}, abstract = {In the natural world, animals must routinely negotiate varied and unpredictable terrain. Yet, we know little about the locomotor strategies used by animals to accomplish this while maintaining dynamic stability. In this paper, we perturb the running of guinea fowl with an unexpected drop in substrate height (DeltaH). The drop is camouflaged to remove any visual cue about the upcoming change in terrain that would allow an anticipatory response. To maintain stability upon a sudden drop in substrate height and prevent a fall, the bird must compensate by dissipating energy or converting it to another form. The aim of this paper is to investigate the control strategies used by birds in this task. In particular, we assess the extent to which guinea fowl maintain body weight support and conservative spring-like body dynamics in the perturbed step. This will yield insight into how animals integrate mechanics and control to maintain dynamic stability in the face of real-world perturbations. Our results show that, despite altered body dynamics and a great deal of variability in the response, guinea fowl are quite successful in maintaining dynamic stability, as they stumbled only once (without falling) in the 19 unexpected perturbations. In contrast, when the birds could see the upcoming drop in terrain, they stumbled in 4 of 20 trials (20\%, falling twice), and came to a complete stop in an additional 6 cases (30\%). The bird{\textquoteright}s response to the unexpected perturbation fell into three general categories: (1) conversion of vertical energy (EV=EP+EKv) to horizontal kinetic energy (EKh), (2) absorption of EV through negative muscular work (-DeltaEcom), or (3) converting EP to vertical kinetic energy (EKv), effectively continuing the ballistic path of the animal{\textquoteright}s center of mass (COM) from the prior aerial phase. However, the mechanics that distinguish these categories actually occur along a continuum with varying degrees of body weight support and actuation by the limb, related to the magnitude and direction of the ground reaction force (GRF) impulse, respectively. In most cases, the muscles of the limb either produced or absorbed energy during the response, as indicated by net changes in COM energy (Ecom). The limb likely begins stance in a more retracted, extended position due to the 26 ms delay in ground contact relative to that anticipated by the bird. This could explain the diminished decelerating force during the first half of stance and the exchange between EP and EK during stance as the body vaults over the limb. The varying degree of weight support and energy absorption in the perturbed step suggests that variation in the initial limb configuration leads to different intrinsic dynamics and reflex action. Future investigation into the limb and muscle mechanics underlying these responses could yield further insight into the control mechanisms that allow such robust dynamic stability of running in the face of large, unexpected perturbations.}, keywords = {Analysis of Variance, Animals, Biomechanical Phenomena, Gait/*physiology, Galliformes/*physiology, Hindlimb/*physiology, Muscle, Skeletal/*physiology, Postural Balance/*physiology, Psychomotor Performance/*physiology, Running/*physiology, Video Recording}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Daley, M. A. and Usherwood, J. R. and Felix, G. and Biewener, A. A.} } @article {548251, title = {Running over rough terrain reveals limb control for intrinsic stability}, journal = {Proc Natl Acad Sci U S AProc Natl Acad Sci U S AProc Natl Acad Sci U S A}, volume = {103}, number = {42}, year = {2006}, note = {Daley, Monica ABiewener, Andrew AengAR047679/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, Non-U.S. Gov{\textquoteright}t2006/10/13 09:00Proc Natl Acad Sci U S A. 2006 Oct 17;103(42):15681-6. Epub 2006 Oct 10.}, month = {Oct 17}, pages = {15681-6}, abstract = {Legged animals routinely negotiate rough, unpredictable terrain with agility and stability that outmatches any human-built machine. Yet, we know surprisingly little about how animals accomplish this. Current knowledge is largely limited to studies of steady movement. These studies have revealed fundamental mechanisms used by terrestrial animals for steady locomotion. However, it is unclear whether these models provide an appropriate framework for the neuromuscular and mechanical strategies used to achieve dynamic stability over rough terrain. Perturbation experiments shed light on this issue, revealing the interplay between mechanics and neuromuscular control. We measured limb mechanics of helmeted guinea fowl (Numida meleagris) running over an unexpected drop in terrain, comparing their response to predictions of the mass-spring running model. Adjustment of limb contact angle explains 80\% of the variation in stance-phase limb loading following the perturbation. Surprisingly, although limb stiffness varies dramatically, it does not influence the response. This result agrees with a mass-spring model, although it differs from previous findings on humans running over surfaces of varying compliance. However, guinea fowl sometimes deviate from mass-spring dynamics through posture-dependent work performance of the limb, leading to substantial energy absorption following the perturbation. This posture-dependent actuation allows the animal to absorb energy and maintain desired velocity on a sudden substrate drop. Thus, posture-dependent work performance of the limb provides inherent velocity control over rough terrain. These findings highlight how simple mechanical models extend to unsteady conditions, providing fundamental insights into neuromuscular control of movement and the design of dynamically stable legged robots and prosthetic devices.}, keywords = {*Lower Extremity/anatomy \& histology/physiology, *Running, Animals, Biomechanical Phenomena, Galliformes, Humans, Muscle, Skeletal/physiology, Postural Balance/*physiology, Regression Analysis, Surface Properties}, isbn = {0027-8424 (Print)0027-8424 (Linking)}, author = {Daley, M. A. and Biewener, A. A.} } @article {548106, title = {Patterns of mechanical energy change in tetrapod gait: pendula, springs and work}, journal = {J Exp Zool A Comp Exp BiolJ Exp Zool A Comp Exp BiolJ Exp Zool A Comp Exp Biol}, volume = {305}, number = {11}, year = {2006}, note = {Biewener, Andrew AengAR047679/AR/NIAMS NIH HHS/Comparative StudyResearch Support, N.I.H., ExtramuralResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Review2006/10/10 09:00J Exp Zool A Comp Exp Biol. 2006 Nov 1;305(11):899-911.}, month = {Nov 1}, pages = {899-911}, abstract = {Kinematic and center of mass (CoM) mechanical variables used to define terrestrial gaits are compared for various tetrapod species. Kinematic variables (limb phase, duty factor) provide important timing information regarding the neural control and limb coordination of various gaits. Whereas, mechanical variables (potential and kinetic energy relative phase, \%Recovery, \%Congruity) provide insight into the underlying mechanisms that minimize muscle work and the metabolic cost of locomotion, and also influence neural control strategies. Two basic mechanisms identified by Cavagna et al. (1977. Am J Physiol 233:R243-R261) are used broadly by various bipedal and quadrupedal species. During walking, animals exchange CoM potential energy (PE) with kinetic energy (KE) via an inverted pendulum mechanism to reduce muscle work. During the stance period of running (including trotting, hopping and galloping) gaits, animals convert PE and KE into elastic strain energy in spring elements of the limbs and trunk and regain this energy later during limb support. The bouncing motion of the body on the support limb(s) is well represented by a simple mass-spring system. Limb spring compliance allows the storage and return of elastic energy to reduce muscle work. These two distinct patterns of CoM mechanical energy exchange are fairly well correlated with kinematic distinctions of limb movement patterns associated with gait change. However, in some cases such correlations can be misleading. When running (or trotting) at low speeds many animals lack an aerial period and have limb duty factors that exceed 0.5. Rather than interpreting this as a change of gait, the underlying mechanics of the body{\textquoteright}s CoM motion indicate no fundamental change in limb movement pattern or CoM dynamics has occurred. Nevertheless, the idealized, distinctive patterns of CoM energy fluctuation predicted by an inverted pendulum for walking and a bouncing mass spring for running are often not clear cut, especially for less cursorial species. When the kinematic and mechanical patterns of a broader diversity of quadrupeds and bipeds are compared, more complex patterns emerge, indicating that some animals may combine walking and running mechanics at intermediate speeds or at very large size. These models also ignore energy costs that are likely associated with the opposing action of limbs that have overlapping support times during walking. A recent model of terrestrial gait (Ruina et al., 2005. J Theor Biol, in press) that treats limb contact with the ground in terms of collisional energy loss indicates that considerable CoM energy can be conserved simply by matching the path of CoM motion perpendicular to limb ground force. This model, coupled with the earlier ones of pendular exchange during walking and mass-spring elastic energy savings during running, provides compelling argument for the view that the legged locomotion of quadrupeds and other terrestrial animals has generally evolved to minimize muscle work during steady level movement.}, keywords = {Animals, Biomechanical Phenomena, Gait/*physiology, Models, Anatomic, Running/physiology, Vertebrates/*physiology, Walking/physiology}, isbn = {1548-8969 (Print)1548-8969 (Linking)}, author = {Biewener, A. A.} } @article {548116, title = {Tired of fatigue? Factors affecting the force-length relationship of muscle}, journal = {J Appl Physiol (1985)J Appl Physiol (1985)J Appl Physiol (1985)}, volume = {101}, number = {1}, year = {2006}, note = {Biewener, Andrew AAhn, A NengCommentEditorialBethesda, Md. : 19852006/06/20 09:00J Appl Physiol (1985). 2006 Jul;101(1):5-6.}, month = {Jul}, pages = {5-6}, keywords = {Actin Cytoskeleton/physiology, Animals, Biomechanical Phenomena, Elasticity, Humans, Muscle Contraction/*physiology, Muscle Fatigue/*physiology, Muscle Fibers, Skeletal/cytology/physiology, Muscle, Skeletal/*anatomy \& histology/innervation/*physiology, Physical Endurance/physiology, Psychomotor Performance/physiology, Rats}, isbn = {8750-7587 (Print)0161-7567 (Linking)}, author = {Biewener, A. A. and Ahn, A. N.} } @article {548561, title = {Dynamic pressure maps for wings and tails of pigeons in slow, flapping flight, and their energetic implications}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {208}, number = {Pt 2}, year = {2005}, note = {Usherwood, James RHedrick, Tyson LMcGowan, Craig PBiewener, Andrew AengComparative StudyEngland2005/01/07 09:00J Exp Biol. 2005 Jan;208(Pt 2):355-69.}, month = {Jan}, pages = {355-69}, abstract = {Differential pressure measurements offer a new approach for studying the aerodynamics of bird flight. Measurements from differential pressure sensors are combined to form a dynamic pressure map for eight sites along and across the wings, and for two sites across the tail, of pigeons flying between two perches. The confounding influence of acceleration on the pressure signals is shown to be small for both wings and tail. The mean differential pressure for the tail during steady, level flight was 25.6 Pa, which, given an angle of attack for the tail of 47.6 degrees , suggests the tail contributes 7.91\% of the force required for weight support, and requires a muscle-mass specific power of 19.3 W kg(-1) for flight to overcome its drag at 4.46 m s(-1). Differential pressures during downstroke increase along the wing length, to 300-400 Pa during take-off and landing for distal sites. Taking the signals obtained from five sensors sited along the wing at feather bases as representative of the mean pressure for five spanwise elements at each point in time, and assuming aerodynamic forces act within the x-z plane (i.e. no forces in the direction of travel) and perpendicular to the wing during downstroke, we calculate that 74.5\% of the force required to support weight was provided by the wings, and that the aerodynamic muscle-mass specific power required to flap the wings was 272.7 W kg(-1).}, keywords = {*Acceleration, *Flight, Animal, Animals, Biomechanical Phenomena, Columbidae/*physiology, Muscle, Skeletal/physiology, Pressure, Tail/*physiology, Video Recording, Wing/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Usherwood, J. R. and Hedrick, T. L. and McGowan, C. P. and Biewener, A. A.} } @article {548571, title = {In vivo muscle function vs speed. II. Muscle function trotting up an incline}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {208}, number = {Pt 6}, year = {2005}, note = {Wickler, Steven JHoyt, Donald FBiewener, Andrew ACogger, Edward ADe La Paz, Kristin LengS06 GM53933/GM/NIGMS NIH HHS/Comparative StudyResearch Support, U.S. Gov{\textquoteright}t, P.H.S.England2005/03/16 09:00J Exp Biol. 2005 Mar;208(Pt 6):1191-200.}, month = {Mar}, pages = {1191-200}, abstract = {Different locomotor tasks, such as moving up or down grades or changing speed, require that muscles adjust the amount of work they perform to raise or lower, accelerate or decelerate the animal{\textquoteright}s center of mass. During level trotting in the horse, the triceps had shortening strains of around 10.6\% while the vastus shortened 8.1\% during the stance phase. Because of the 250\% increase in metabolic rate in horses trotting up a 10\% incline which is, presumably, a result of the increased requirement for mechanical work, we hypothesized that muscle strain during trotting would be increased in both the triceps and the vastus over that observed when trotting on the level. Because times of contact are similar in level and incline trotting, we also hypothesized that strain rates of these muscles would be increased, accompanied by an increase in EMG activity. We examined the lateral head of the triceps and the vastus lateralis while trotting up a 10\% incline (5.7 degrees) over a range of speeds. The triceps shortened by 18\% compared with 10.6\% shortening on the level, and the vastus shortened by 18.5\% compared with 8.1\% on the level. The increased shortening velocities that were observed in both muscles probably reduced the force that any given set of activated muscle fibers could produce. If this pattern held for other limb muscles that do work to elevate the horse{\textquoteright}s center of mass on an incline, then a greater volume of muscle would have to be recruited to generate an equivalent force for body support. This was reflected in significant increases in the EMG intensity (IEMG) of both muscles.}, keywords = {Analysis of Variance, Animals, Biomechanical Phenomena, Electromyography, Energy Metabolism/physiology, Forelimb/physiology, Hindlimb/physiology, Horses/*physiology, Joints/physiology, Locomotion/*physiology, Muscle Contraction/*physiology, Muscle, Skeletal/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Wickler, S. J. and Hoyt, D. F. and Biewener, A. A. and Cogger, E. A. and De La Paz, K. L.} } @article {548521, title = {Regional patterns of pectoralis fascicle strain in the pigeon Columba livia during level flight}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {208}, number = {Pt 4}, year = {2005}, note = {Soman, AryaHedrick, Tyson LBiewener, Andrew AengComparative StudyResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2005/02/08 09:00J Exp Biol. 2005 Feb;208(Pt 4):771-86.}, month = {Feb}, pages = {771-86}, abstract = {Regional fascicle strains were recorded in vivo from the pectoralis of carneau pigeons using sonomicrometry during level slow flight, together with regional electromyography (EMG) and deltopectoral crest (DPC) strain measurements of whole muscle force. Fascicle strain measurements were obtained at four sites within the pectoralis: the anterior (Ant), middle (Mid) and posterior (Post) sternobrachium (SB), and the smaller thoracobrachium (TB). Strains were also recorded along the intramuscular aponeurosis of the pectoralis to assess its {\textquoteright}in-series{\textquoteright} compliance with respect to strains of Post SB and TB fascicles. In-series segment strains were also obtained along Ant SB and Mid SB fascicles, which insert directly on the DPC without attaching to the intramuscular aponeurosis. In-series segment strains differed from 2\% to 17.2\%, averaging differences of 6.1\% at the Ant SB site and 1.4\% at the Mid SB site. Temporal patterns of in-series fascicle segment strain were similar at both sites. Regional fascicle strains also exhibited similar temporal patterns of lengthening and shortening and were most uniform in magnitude at the Ant SB, Mid SB and TB sites (total strain: 33.7\%, 35.9\% and 33.2\% respectively), but were smaller at the Post SB site (24.4\%). Strains measured along the aponeurosis tracked the patterns of contractile fascicle strain but were significantly lower in magnitude (19.1\%). Fascicle lengthening strains (+25.4\%) greatly exceeded net shortening strains (-6.5\%) at all sites. Much of the variation in regional fascicle strain patterns resulted from variation of in vivo recording sites among individual animals, despite attempts to define consistent regions for obtaining in vivo recordings. No significant variation in EMG activation onset was found, but deactivation of the Ant SB occurred before the other muscle sites. Even so, the range of variation was small, with all muscle regions being activated midway through lengthening (upstroke) and turned off midway through shortening (downstroke). While subtle differences in the timing and rate of fascicle strain may relate to differing functional roles of the pectoralis, regional patterns of fascicle strain and activation suggest a generally uniform role for the muscle as a whole throughout the wingbeat cycle. Shorter fascicles located in more posterior regions of the muscle underwent generally similar strains as longer fascicles located in more anterior SB regions. The resulting differences in fiber length were accommodated by strain in the intramuscular aponeurosis and rotation of the pectoralis insertion with respect to the origin. As a result, longer Ant and Mid SB fascicles were estimated to contribute substantially more work per unit mass than shorter Post SB and TB fascicles. When the mass fractions of these regions are accounted for, our regional fascicle strain measurements show that the anterior regions of the pectoralis likely contribute 76\%, and the posterior regions 24\%, of the muscle{\textquoteright}s total work output. When adjusted for mass fraction and regional fascicle strain, pectoralis work averaged 24.7+/-5.1 J kg(-1) (206.6+/-43.5 W kg(-1)) during level slow (approximately 4-5 m s(-1)) flight.}, keywords = {Analysis of Variance, Animals, Biomechanical Phenomena, Body Weights and Measures, Columbidae/*physiology, Electromyography, Flight, Animal/*physiology, Muscle Contraction/*physiology, Pectoralis Muscles/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Soman, A. and Hedrick, T. L. and Biewener, A. A.} } @article {548456, title = {The mechanics of jumping versus steady hopping in yellow-footed rock wallabies}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {208}, number = {Pt 14}, year = {2005}, note = {McGowan, C PBaudinette, R VUsherwood, J RBiewener, A AengComparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tEngland2005/07/08 09:00J Exp Biol. 2005 Jul;208(Pt 14):2741-51.}, month = {Jul}, pages = {2741-51}, abstract = {The goal of our study was to explore the mechanical power requirements associated with jumping in yellow-footed rock wallabies and to determine how these requirements are achieved relative to steady-speed hopping mechanics. Whole body power output and limb mechanics were measured in yellow-footed rock wallabies during steady-speed hopping and moving jumps up to a landing ledge 1.0 m high (approximately 3 times the animals{\textquoteright} hip height). High-speed video recordings and ground reaction force measurements from a runway-mounted force platform were used to calculate whole body power output and to construct a limb stiffness model to determine whole limb mechanics. The combined mass of the hind limb extensor muscles was used to estimate muscle mass-specific power output. Previous work suggested that a musculoskeletal design that favors elastic energy recovery, like that found in tammar wallabies and kangaroos, may impose constraints on mechanical power generation. Yet rock wallabies regularly make large jumps while maneuvering through their environment. As jumping often requires high power, we hypothesized that yellow-footed rock wallabies would be able to generate substantial amounts of mechanical power. This was confirmed, as we found net extensor muscle power outputs averaged 155 W kg(-1) during steady hopping and 495 W kg(-1) during jumping. The highest net power measured reached nearly 640 W kg(-1). As these values exceed the maximum power-producing capability of vertebrate skeletal muscle, we suggest that back, trunk and tail musculature likely play a substantial role in contributing power during jumping. Inclusion of this musculature yields a maximum power output estimate of 452 W kg(-1) muscle. Similar to human high-jumpers, rock wallabies use a moderate approach speed and relatively shallow leg angle of attack (45-55 degrees) during jumps. Additionally, initial leg stiffness increases nearly twofold from steady hopping to jumping, facilitating the transfer of horizontal kinetic energy into vertical kinetic energy. Time of contact is maintained during jumping by a substantial extension of the leg, which keeps the foot in contact with the ground.}, keywords = {*Models, Biological, Analysis of Variance, Animals, Biomechanical Phenomena, Hindlimb/*physiology, Locomotion/*physiology, Macropodidae/*physiology, Muscle, Skeletal/*physiology, Video Recording}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {McGowan, C. P. and Baudinette, R. V. and Usherwood, J. R. and Biewener, A. A.} } @article {548441, title = {Joint work and power associated with acceleration and deceleration in tammar wallabies (Macropus eugenii)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {208}, number = {Pt 1}, year = {2005}, note = {McGowan, C PBaudinette, R VBiewener, A AengComparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2004/12/17 09:00J Exp Biol. 2005 Jan;208(Pt 1):41-53.}, month = {Jan}, pages = {41-53}, abstract = {Measurements of joint work and power were determined using inverse dynamics analysis based on ground reaction force and high-speed video recordings of tammar wallabies as they decelerated and accelerated while hopping over a force platform on level ground. Measurements were obtained over a range of accelerations ranging from -6 m s(-2) to 8 m s(-2). The goal of our study was to determine which joints are used to modulate mechanical power when tammar wallabies change speed. From these measurements, we also sought to determine which hind limb muscle groups are the most important for producing changes in mechanical work. Because our previous in vivo analyses of wallaby distal muscle function indicated that these muscle-tendon units favor elastic energy savings and perform little work during steady level and incline hopping, we hypothesized that proximal muscle groups operating at the hip and knee joint are most important for the modulation of mechanical work and power. Of the four hind limb joints examined, the ankle joint had the greatest influence on the total limb work, accounting for 89\% of the variation observed with changing speed. The hip and metatarsophalageal (MP) joints also contributed to modulating whole limb work, but to a lesser degree than the ankle, accounting for 28\% (energy production) and -24\% (energy absorption) of the change in whole limb work versus acceleration, respectively. In contrast, the work produced at the knee joint was independent of acceleration. Based on the results of our previous in vivo studies and given that the magnitude of power produced at the ankle exceeds that which these muscles alone could produce, we conclude that the majority of power produced at the ankle joint is likely transferred from the hip and knee joints via proximal bi-articular muscles, operating in tandem with bi-articular ankle extensors, to power changes in hopping speed of tammar wallabies. Additionally, over the observed range of performance, peak joint moments at the ankle (and resulting tendon strains) did not increase significantly with acceleration, indicating that having thin tendons favoring elastic energy storage does not necessarily limit a tammar wallaby{\textquoteright}s ability to accelerate or decelerate.}, keywords = {*Acceleration, Animals, Biomechanical Phenomena, Joints/*physiology, Locomotion/*physiology, Macropodidae/*physiology, Muscle, Skeletal/physiology, Tendons/physiology, Video Recording}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {McGowan, C. P. and Baudinette, R. V. and Biewener, A. A.} } @article {548366, title = {In vivo muscle function vs speed. I. Muscle strain in relation to length change of the muscle-tendon unit}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {208}, number = {Pt 6}, year = {2005}, note = {Hoyt, Donald FWickler, Steven JBiewener, Andrew ACogger, Edward ADe La Paz, Kristin LengS06 GM053933/GM/NIGMS NIH HHS/Comparative StudyResearch Support, U.S. Gov{\textquoteright}t, P.H.S.England2005/03/16 09:00J Exp Biol. 2005 Mar;208(Pt 6):1175-90.}, month = {Mar}, pages = {1175-90}, abstract = {The activity of muscles can be concentric (shortening), eccentric (lengthening) or isometric (constant length). When studying muscle function it is important to know what the muscle fascicles are actually doing because the performance of muscle is strongly influenced by the type of activity: force decreases as a function of shortening velocity during concentric contractions; force produced during eccentric contractions can be stronger than maximum isometric force, and force production is enhanced if a concentric contraction follows an eccentric phase. It is well known that length changes of muscle fascicles may be different from length changes of the overall muscle-tendon unit because of the compliance of the series elasticity. Consequently, fascicles of joint extensor muscles may not undergo eccentric activity even when the joint flexes, but the extent to which this occurs may vary with the compliance of the series elasticity and may differ between species: the vastus lateralis, a knee extensor, shortens when active during trotting in dogs and lengthens in rats. Previous studies of kinematics of trotting in horses have shown that during stance, the elbow extends nearly continuously with a brief period of flexion near mid-stance and the knee exhibits two phases of flexion followed by extension. The lateral triceps (an elbow extensor) has no external tendon but the vastus lateralis has a relatively long external tendon and the fascicles insert on an aponeurosis. Thus, one might expect the relation between fascicle strain and overall length change of the muscle-tendon units to be quite different in these two muscles. In the present study in horses, fascicle length changes of the lateral triceps and vastus lateralis were measured with sonomicrometry and length changes of the muscle-tendon units were estimated from muscle architecture and joint kinematics for four horses trotting on a treadmill at nine speeds. Because the focus of this study was the relation between length changes of the muscle-tendon unit (estimated from kinematics) and length changes in the muscle fascicles, we divided the stance-phase sonomicrometry records into phases that corresponded to the alternating flexion and extension of the joint as indicated by the kinematic records. During its one eccentric phase, the triceps shortened by 0.7+/-0.4\% despite a predicted lengthening of 1\%. Similarly, the vastus shortened by 3.7+/-1.9\% when kinematics predicted 3.2\% lengthening. During their concentric phases the triceps shortened by 10.6\% and the vastus shortened by 8.1\%. Strain in the triceps did not change with speed but it did in the vastus. Strain rate increased with speed in both muscles as did the integrated EMG, indicating an increase in the volume of muscle recruited. Thus, despite differences in their architecture and the kinematic patterns of the associated joints, these two joint extensors exhibited similar activity.}, keywords = {Analysis of Variance, Animals, Biomechanical Phenomena, Electromyography, Forelimb/physiology, Hindlimb/physiology, Horses/*physiology, Joints/physiology, Locomotion/*physiology, Muscle Contraction/*physiology, Muscle, Skeletal/*physiology, Tendons/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Hoyt, D. F. and Wickler, S. J. and Biewener, A. A. and Cogger, E. A. and De La Paz, K. L.} } @article {548301, title = {Patterns of strain and activation in the thigh muscles of goats across gaits during level locomotion}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {208}, number = {Pt 24}, year = {2005}, note = {Gillis, Gary BFlynn, John PMcGuigan, PollyBiewener, Andrew AengR01 AR47679/AR/NIAMS NIH HHS/Comparative StudyResearch Support, N.I.H., ExtramuralResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2005/12/06 09:00J Exp Biol. 2005 Dec;208(Pt 24):4599-611.}, month = {Dec}, pages = {4599-611}, abstract = {Unlike homologous muscles in many vertebrates, which appear to function similarly during a particular mode of locomotion (e.g. red muscle in swimming fish, pectoralis muscle in flying birds, limb extensors in jumping and swimming frogs), a major knee extensor in mammalian quadrupeds, the vastus lateralis, appears to operate differently in different species studied to date. In rats, the vastus undergoes more stretching early in stance than shortening in later stance. In dogs, the reverse is true; more substantial shortening follows small amounts of initial stretching. And in horses, while the vastus strain trajectory is complex, it is characterized mainly by shortening during stance. In this study, we use sonomicrometry and electromyography to study the vastus lateralis and biceps femoris of goats, with three goals in mind: (1) to see how these muscles work in comparison to homologous muscles studied previously in other taxa; (2) to address how speed and gait impact muscle actions and (3) to test whether fascicles in different parts of the same muscle undergo similar length changes. Results indicate that the biceps femoris undergoes substantial shortening through much of stance, with higher strains in walking and trotting [32-33\% resting length (L0)] than galloping (22\% L0). These length changes occur with increasing biceps EMG intensities as animals increase speed from walking to galloping. The vastus undergoes a stretch-shorten cycle during stance. Stretching strains are higher during galloping (15\% L0) than walking and trotting (9\% L0). Shortening strains follow a reverse pattern and are greatest in walking (24\% L0), intermediate in trotting (20\% L0) and lowest during galloping (17\% L0). As a result, the ratio of stretching to shortening increases from below 0.5 in walking and trotting to near 1.0 during galloping. This increasing ratio suggests that the vastus does relatively more positive work than energy absorption at the slower speeds compared with galloping, although an understanding of the timing and magnitude of force production is required to confirm this. Length-change regimes in proximal, middle and distal sites of the vastus are generally comparable, suggesting strain homogeneity through the muscle. When strain rates are compared across taxa, vastus shortening velocities exhibit the scaling pattern predicted by theoretical and empirical work: fascicles shorten relatively faster in smaller animals than larger animals (strain rates near 2 L s-1 have been reported for trotting dogs and were found here for goats, versus 0.6-0.8 L s-1 reported in horses). Interestingly, biceps shortening strain rates are very similar in both goats and rats during walking (1-1.5 L s-1) and trotting (1.5-2.5 L s-1, depending on speed of trot), suggesting that the ratio of in vivo shortening velocities (V) to maximum shortening velocities (Vmax) is smaller in small animals (because of their higher V(max)).}, keywords = {Analysis of Variance, Animals, Biomechanical Phenomena, Electromyography, Gait/*physiology, Goats/*physiology, Locomotion/*physiology, Muscle Contraction/physiology, Muscle, Skeletal/*physiology, Thigh/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Gillis, G. B. and Flynn, J. P. and McGuigan, P. and Biewener, A. A.} } @article {548101, title = {Biomechanical consequences of scaling}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {208}, number = {Pt 9}, year = {2005}, note = {Biewener, Andrew AengAR-047679/AR/NIAMS NIH HHS/Research Support, N.I.H., ExtramuralResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.ReviewEngland2005/04/28 09:00J Exp Biol. 2005 May;208(Pt 9):1665-76.}, month = {May}, pages = {1665-76}, abstract = {To function over a lifetime of use, materials and structures must be designed to have sufficient factors of safety to avoid failure. Vertebrates are generally built from materials having similar properties. Safety factors are most commonly calculated based on the ratio of a structure{\textquoteright}s failure stress to its peak operating stress. However, yield stress is a more likely limit, and work of fracture relative to energy absorption is likely the most relevant measure of a structure{\textquoteright}s safety factor, particularly under impact loading conditions characteristic of locomotion. Yet, it is also the most difficult to obtain. For repeated loading, fatigue damage and eventual failure may be critical to the design of biological structures and will result in lower safety factors. Although area:volume scaling predicts that stresses will increase with size, interspecific comparisons of mammals and birds show that skeletal allometry is modest, with most groups scaling (l proportional, variant d0.89) closer to geometric similarity (isometry: l proportional, variant d1.0) than to elastic similarity (l proportional, variant d0.67) or stress similarity (l proportional, variant d0.5). To maintain similar peak bone and muscle stresses, terrestrial mammals change posture when running, with larger mammals becoming more erect. More erect limbs increases their limb muscle mechanical advantage (EMA) or ratio of ground impulse to muscle impulse (r/R= integral G/integral Fm). The increase in limb EMA with body weight (proportional, variant W0.25) allows larger mammals to match changes in bone and muscle area (proportional, variant W0.72-0.80) to changes in muscle force generating requirements (proportional, variantW0.75), keeping bone and muscle stresses fairly constant across a size range 0.04-300 kg. Above this size, extremely large mammals exhibit more pronounced skeletal allometry and reduced locomotor ability. Patterns of ontogenetic scaling during skeletal growth need not follow broader interspecific scaling patterns. Instead, negative allometric growth (becoming more slender) is often observed and may relate to maturation of the skeleton{\textquoteright}s properties or the need for younger animals to move at faster speeds compared with adults. In contrast to bone and muscle stress patterns, selection for uniform safety factors in tendons does not appear to occur. In addition to providing elastic energy savings, tendons transmit force for control of motion of more distal limb segments. Their role in elastic savings requires that some tendons operate at high stresses (and strains), which compromises their safety factor. Other {\textquoteright}low stress{\textquoteright} tendons have larger safety factors, indicating that their primary design is for stiffness to reduce the amount of stretch that their muscles must overcome when contracting to control movement.}, keywords = {*Biophysics, Animals, Biomechanical Phenomena, Biophysical Phenomena, Body Size, Bone and Bones/*physiology, Locomotion/*physiology, Muscle, Skeletal/*physiology, Species Specificity, Tendons/*physiology, Vertebrates/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A.} } @article {548426, title = {Ontogenetic patterns of limb loading, in vivo bone strains and growth in the goat radius}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {207}, number = {Pt 15}, year = {2004}, note = {Main, Russell PBiewener, Andrew AengComparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tEngland2004/06/18 05:00J Exp Biol. 2004 Jul;207(Pt 15):2577-88.}, month = {Jul}, pages = {2577-88}, abstract = {As tetrapods increase in size and weight through ontogeny, the limb skeleton must grow to accommodate the increases in body weight and the resulting locomotor forces placed upon the limbs. No study to date, however, has examined how morphological changes in the limb skeleton during growth reflect ontogenetic patterns of limb loading and the resulting stresses and strains produced in the limbs. The goal of this study was to relate forelimb loads to in vivo bone strains in the radius of the domestic goat (Capra hircus) across a range of gaits and speeds through ontogeny while observing how the growth patterns of the bone relate to the mechanics of the limb. In vivo bone strains in the radius were recorded from two groups of juvenile goats (4 kg, 6 weeks and 9 kg, 15 weeks) and compared with previously reported strain data for the radius of adult goats. Ontogenetic strain patterns were examined in relation to peak forelimb ground reaction forces, ontogenetic scaling patterns of cross-sectional geometry and bone curvature, and percentage mineral ash content. Peak principal longitudinal tensile strains on the cranial surface and compressive strains on the caudal surface of the radius increased during ontogeny but maintained a uniform distribution, resulting in the radius being loaded primarily in bending through ontogeny. The increase in strain occurred despite uniform loading (relative to body weight) of the forelimb through ontogeny. Instead, the increase in bone strain resulted from strong negative growth allometry of the cross-sectional area (proportional to M(0.53)) and medio-lateral and cranio-caudal second moments of area (I(ML) proportional to M(1.03), I(CC) proportional to M(0.84)) of the radius and only a small increase (+2.8\%) in mineral ash content. Even though bone strains increased with growth and age, strains in the younger goats were small enough to suggest that they maintain safety factors at least comparable with adults when moving at similar absolute speeds. Increased variability of loading in juvenile animals may also favor the more robust dimensions of the radius, and possibly other limb bones, early in growth.}, keywords = {Analysis of Variance, Animals, Biomechanical Phenomena, Body Weights and Measures, Forelimb/anatomy \& histology/growth \& development/*physiology, Gait/*physiology, Goats/*growth \& development, Radius/*physiology, Stress, Mechanical}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Main, R. P. and Biewener, A. A.} } @article {548326, title = {Wing inertia and whole-body acceleration: an analysis of instantaneous aerodynamic force production in cockatiels (Nymphicus hollandicus) flying across a range of speeds}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {207}, number = {Pt 10}, year = {2004}, note = {Hedrick, Tyson LUsherwood, James RBiewener, Andrew AengComparative StudyResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2004/04/10 05:00J Exp Biol. 2004 Apr;207(Pt 10):1689-702.}, month = {Apr}, pages = {1689-702}, abstract = {We used a combination of high-speed 3-D kinematics and three-axis accelerometer recordings obtained from cockatiels flying in a low-turbulence wind tunnel to characterize the instantaneous accelerations and, by extension, the net aerodynamic forces produced throughout the wingbeat cycle across a broad range of flight speeds (1-13 m s(-1)). Our goals were to investigate the variation in instantaneous aerodynamic force production during the wingbeat cycle of birds flying across a range of steady speeds, testing two predictions regarding aerodynamic force generation in upstroke and the commonly held assumption that all of the kinetic energy imparted to the wings of a bird in flapping flight is recovered as useful aerodynamic work. We found that cockatiels produce only a limited amount of lift during upstroke (14\% of downstroke lift) at slower flight speeds (1-3 m s(-1)). Upstroke lift at intermediate flight speeds (7-11 m s(-1)) was moderate, averaging 39\% of downstroke lift. Instantaneous aerodynamic forces were greatest near mid-downstroke. At the end of each half-stroke, during wing turnaround, aerodynamic forces were minimal, but inertial forces created by wing motion were large. However, we found that the inertial power requirements of downstroke (minimum of 0.29+/-0.10 W at 7 m s(-1) and maximum of 0.56+/-0.13 W at 1 m s(-1)) were consistent with the assumption that nearly all wing kinetic energy in downstroke was applied to the production of aerodynamic forces and therefore should not be added separately to the overall power cost of flight. The inertial power requirements of upstroke (minimum of 0.16+/-0.04 W at 7 m s(-1) and maximum of 0.35+/-0.11 W at 1 m s(-1)) cannot be recovered in a similar manner, but their magnitude was such that the power requirements for the upstroke musculature (minimum of 54+/-13 W kg(-1) at 7 m s(-1) and maximum of 122+/-35 W at 1 m s(-1)) fall within the established range for cockatiel flight muscle (<185 W kg(-1)).}, keywords = {*Acceleration, *Flight, Animal, Animals, Biomechanical Phenomena, Birds/*physiology, Body Weights and Measures, Video Recording, Wing/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Hedrick, T. L. and Usherwood, J. R. and Biewener, A. A.} } @article {548181, title = {Dynamics of leg muscle function in tammar wallabies (M. eugenii) during level versus incline hopping}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {207}, number = {Pt 2}, year = {2004}, note = {Biewener, A AMcGowan, CCard, G MBaudinette, R VengComparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2003/12/12 05:00J Exp Biol. 2004 Jan;207(Pt 2):211-23.}, month = {Jan}, pages = {211-23}, abstract = {The goal of our study was to examine whether the in vivo force-length behavior, work and elastic energy savings of distal muscle-tendon units in the legs of tammar wallabies (Macropus eugenii) change during level versus incline hopping. To address this question, we obtained measurements of muscle activation (via electromyography), fascicle strain (via sonomicrometry) and muscle-tendon force (via tendon buckles) from the lateral gastrocnemius (LG) and plantaris (PL) muscles of tammar wallabies trained to hop on a level and an inclined (10 degrees, 17.4\% grade) treadmill at two speeds (3.3 m s(-1) and 4.2 m s(-1)). Similar patterns of muscle activation, force and fascicle strain were observed under both level and incline conditions. This also corresponded to similar patterns of limb timing and movement (duty factor, limb contact time and hopping frequency). During both level and incline hopping, the LG and PL exhibited patterns of fascicle stretch and shortening that yielded low levels of net fascicle strain [LG: level, -1.0+/-4.6\% (mean +/- S.E.M.) vs incline, 0.6+/-4.5\%; PL: level, 0.1+/-1.0\% vs incline, 0.4+/-1.6\%] and muscle work (LG: level, -8.4+/-8.4 J kg(-1) muscle vs incline, -6.8+/-7.5 J kg(-1) muscle; PL: level, -2.0+/-0.6 J kg(-1) muscle vs incline, -1.4+/-0.7 J kg(-1) muscle). Consequently, neither muscle significantly altered its contractile dynamics to do more work during incline hopping. Whereas electromyographic (EMG) phase, duration and intensity did not differ for the LG, the PL exhibited shorter but more intense periods of activation, together with reduced EMG phase (P<0.01), during incline versus level hopping. Our results indicate that design for spring-like tendon energy savings and economical muscle force generation is key for these two distal muscle-tendon units of the tammar wallaby, and the need to accommodate changes in work associated with level versus incline locomotion is achieved by more proximal muscles of the limb.}, keywords = {Animals, Biomechanical Phenomena, Electromyography, Hindlimb/*physiology, Locomotion/*physiology, Macropodidae/*physiology, Muscle Contraction/*physiology, Muscle, Skeletal/*physiology, Tendons/*physiology, Time Factors, Transducers}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A. and McGowan, C. and Card, G. M. and Baudinette, R. V.} } @article {548161, title = {Muscle mechanical advantage of human walking and running: implications for energy cost}, journal = {J Appl Physiol (1985)J Appl Physiol (1985)J Appl Physiol (1985)}, volume = {97}, number = {6}, year = {2004}, note = {Biewener, Andrew AFarley, Claire TRoberts, Thomas JTemaner, MarcoengAR-046499/AR/NIAMS NIH HHS/AR-047679/AR/NIAMS NIH HHS/Research Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.Bethesda, Md. : 19852004/07/20 05:00J Appl Physiol (1985). 2004 Dec;97(6):2266-74. Epub 2004 Jul 16.}, month = {Dec}, pages = {2266-74}, abstract = {Muscular forces generated during locomotion depend on an animal{\textquoteright}s speed, gait, and size and underlie the energy demand to power locomotion. Changes in limb posture affect muscle forces by altering the mechanical advantage of the ground reaction force (R) and therefore the effective mechanical advantage (EMA = r/R, where r is the muscle mechanical advantage) for muscle force production. We used inverse dynamics based on force plate and kinematic recordings of humans as they walked and ran at steady speeds to examine how changes in muscle EMA affect muscle force-generating requirements at these gaits. We found a 68\% decrease in knee extensor EMA when humans changed gait from a walk to a run compared with an 18\% increase in hip extensor EMA and a 23\% increase in ankle extensor EMA. Whereas the knee joint was extended (154-176 degrees) during much of the support phase of walking, its flexed position (134-164 degrees) during running resulted in a 5.2-fold increase in quadriceps impulse (time-integrated force during stance) needed to support body weight on the ground. This increase was associated with a 4.9-fold increase in the ground reaction force moment about the knee. In contrast, extensor impulse decreased 37\% (P < 0.05) at the hip and did not change at the ankle when subjects switched from a walk to a run. We conclude that the decrease in limb mechanical advantage (mean limb extensor EMA) and increase in knee extensor impulse during running likely contribute to the higher metabolic cost of transport in running than in walking. The low mechanical advantage in running humans may also explain previous observations of a greater metabolic cost of transport for running humans compared with trotting and galloping quadrupeds of similar size.}, keywords = {Adult, Ankle Joint/physiology, Biomechanical Phenomena, Energy Metabolism/*physiology, Gait/*physiology, Hip Joint/physiology, Humans, Knee Joint/physiology, Leg/physiology, Male, Muscle, Skeletal/anatomy \& histology/*metabolism, Running/*physiology, Walking/*physiology}, isbn = {8750-7587 (Print)0161-7567 (Linking)}, author = {Biewener, A. A. and Farley, C. T. and Roberts, T. J. and Temaner, M.} } @article {548006, title = {Walking and running in the red-legged running frog, Kassina maculata}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {207}, number = {Pt 3}, year = {2004}, note = {Ahn, A NFurrow, EBiewener, A AengF32 AR 47741/AR/NIAMS NIH HHS/Comparative StudyResearch Support, U.S. Gov{\textquoteright}t, P.H.S.England2003/12/24 05:00J Exp Biol. 2004 Jan;207(Pt 3):399-410.}, month = {Jan}, pages = {399-410}, abstract = {Although most frog species are specialized for jumping or swimming, Kassina maculata (red-legged running frog) primarily uses a third type of locomotion during which the hindlimbs alternate. In the present study, we examined Kassina{\textquoteright}s distinct locomotory mode to determine whether these frogs walk or run and how their gait may change with speed. We used multiple methods to distinguish between terrestrial gaits: the existence or absence of an aerial phase, duty factor, relative footfall patterns and the mechanics of the animal{\textquoteright}s center of mass (COM). To measure kinematic and kinetic variables, we recorded digital video as the animals moved over a miniature force platform (N=12 individuals). With respect to footfall patterns, the frogs used a single gait and walked at all speeds examined. Duty factor always exceeded 0.59. Based on COM mechanics, however, the frogs used both walking and running gaits. At slower speeds, the fluctuations in the horizontal kinetic energy (E(k)) and gravitational potential energy (E(p)) of the COM were largely out of phase, indicating a vaulting or walking gait. In most of the trials, Kassina used a combined gait at intermediate speeds, unlike cursorial animals with distinct gait transitions. This combined gait, much like a mammalian gallop, exhibited the mechanics of both vaulting and bouncing gaits. At faster speeds, the E(k) and E(p) of Kassina{\textquoteright}s COM were more in phase, indicating the use of a bouncing or running gait. Depending on the definition used to distinguish between walking and running, Kassina either only used a walking gait at all speeds or used a walking gait at slower speeds but then switched to a running gait as speed increased.}, keywords = {Animals, Anura/*physiology, Biomechanical Phenomena, Gait/*physiology, Running/*physiology, Video Recording, Walking/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Ahn, A. N. and Furrow, E. and Biewener, A. A.} } @article {548556, title = {The aerodynamics of avian take-off from direct pressure measurements in Canada geese (Branta canadensis)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {206}, number = {Pt 22}, year = {2003}, note = {Usherwood, James RHedrick, Tyson LBiewener, Andrew AengComparative StudyResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2003/10/14 05:00J Exp Biol. 2003 Nov;206(Pt 22):4051-6.}, month = {Nov}, pages = {4051-6}, abstract = {Direct pressure measurements using electronic differential pressure transducers along bird wings provide insight into the aerodynamics of these dynamically varying aerofoils. Acceleration-compensated pressures were measured at five sites distributed proximally to distally from the tertials to the primaries along the wings of Canada geese. During take-off flight, ventral-to-dorsal pressure is maintained at the proximal wing section throughout the wingstroke cycle, whereas pressure sense is reversed at the primaries during upstroke. The distal sites experience double pressure peaks during the downstroke. These observations suggest that tertials provide weight-support throughout the wingbeat, that the wingtip provides thrust during upstroke and that the kinetic energy of the rapidly flapping wings may be dissipated via retarding aerodynamic forces (resulting in aerodynamic work) at the end of downstroke.}, keywords = {*Pressure, Acceleration, Animals, Biomechanical Phenomena, Flight, Animal/*physiology, Geese/*physiology, Transducers, Pressure, Wing/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Usherwood, J. R. and Hedrick, T. L. and Biewener, A. A.} } @article {548546, title = {Comparative power curves in bird flight}, journal = {NatureNatureNature}, volume = {421}, number = {6921}, year = {2003}, note = {Tobalske, B WHedrick, T LDial, K PBiewener, A AengComparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2003/01/24 04:00Nature. 2003 Jan 23;421(6921):363-6.}, month = {Jan 23}, pages = {363-6}, abstract = {The relationship between mechanical power output and forward velocity in bird flight is controversial, bearing on the comparative physiology and ecology of locomotion. Applied to flying birds, aerodynamic theory predicts that mechanical power should vary as a function of forward velocity in a U-shaped curve. The only empirical test of this theory, using the black-billed magpie (Pica pica), suggests that the mechanical power curve is relatively flat over intermediate velocities. Here, by integrating in vivo measurements of pectoralis force and length change with quasi-steady aerodynamic models developed using data on wing and body movement, we present mechanical power curves for cockatiels (Nymphicus hollandicus) and ringed turtle-doves (Streptopelia risoria). In contrast to the curve reported for magpies, the power curve for cockatiels is acutely concave, whereas that for doves is intermediate in shape and shows higher mass-specific power output at most speeds. We also find that wing-beat frequency and mechanical power output do not necessarily share minima in flying birds. Thus, aspects of morphology, wing kinematics and overall style of flight can greatly affect the magnitude and shape of a species{\textquoteright} power curve.}, keywords = {*Models, Biological, Animals, Biomechanical Phenomena, Birds/*physiology, Bone and Bones/physiology, Columbidae/physiology, Flight, Animal/*physiology, Muscle, Skeletal/physiology, Psittaciformes/physiology, Wing/*physiology}, isbn = {0028-0836 (Print)0028-0836 (Linking)}, author = {Tobalske, B. W. and Hedrick, T. L. and Dial, K. P. and Biewener, A. A.} } @article {548316, title = {How cockatiels (Nymphicus hollandicus) modulate pectoralis power output across flight speeds}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {206}, number = {Pt 8}, year = {2003}, note = {Hedrick, Tyson LTobalske, Bret WBiewener, Andrew AengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2003/03/08 04:00J Exp Biol. 2003 Apr;206(Pt 8):1363-78.}, month = {Apr}, pages = {1363-78}, abstract = {The avian pectoralis muscle must produce a varying mechanical power output to achieve flight across a range of speeds (1-13 m s(-1)). We used the natural variation in the power requirements with flight speed to investigate the mechanisms employed by cockatiels (Nymphicus hollandicus) to modulate muscle power output. We found that pectoralis contractile function in cockatiels was generally conserved across speed and over a wide range of aerodynamic power requirements. Despite the 2-fold range of variation in muscle power output, many aspects of muscle performance varied little: duration of muscle shortening was invariant, and overall wingbeat frequency and muscle strain varied to a lesser degree (1.2-fold and 1.4-fold, respectively) than muscle power or work. Power output was primarily modulated by muscle force (accounting for 65\% of the variation) rather than by muscle strain, cycle frequency or changes in the timing of force production relative to muscle strain. Strain rate and electromyogram (EMG) results suggest that the additional force was provided via increasing pectoralis recruitment. Due to their effect on the transformation of muscle work into useful aerodynamic work, changes in wing position and orientation during the downstroke probably also affect the magnitude of muscle force developed for a given level of motor recruitment. Analysis of the variation in muscle force and airflow over the wing suggests that the coefficients of lift and drag of the wing vary 4-fold over the speed range examined in this study.}, keywords = {Analysis of Variance, Animals, Biomechanical Phenomena, Birds/*physiology, Electromyography, Flight, Animal/*physiology, Least-Squares Analysis, Models, Biological, Muscle Contraction/*physiology, Pectoralis Muscles/*physiology, Wing/physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Hedrick, T. L. and Tobalske, B. W. and Biewener, A. A.} } @article {548246, title = {Muscle force-length dynamics during level versus incline locomotion: a comparison of in vivo performance of two guinea fowl ankle extensors}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {206}, number = {Pt 17}, year = {2003}, note = {Daley, Monica ABiewener, Andrew AengR01-AR047679/AR/NIAMS NIH HHS/Comparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, P.H.S.England2003/07/25 05:00J Exp Biol. 2003 Sep;206(Pt 17):2941-58.}, month = {Sep}, pages = {2941-58}, abstract = {For a terrestrial animal to move in the complex natural environment, the limb muscles must modulate force and work performance to meet changing mechanical requirements; however, it is not clear whether this is accomplished via a collective shift in function by all limb muscles, or a division of labor among limb muscles. Do muscles differ in their ability to modulate force-length contractile function to meet the mechanical demands of different locomotor tasks? We explore this question by examining the in vivo force-length performance of the guinea fowl Numida meleagris lateral gastrocnemius (LG) and digital flexor-IV (DF-IV), during level and incline locomotion. During level locomotion, the LG and DF-IV exhibit differing muscle fascicle strain patterns: the LG shortens by 10-15\% while developing force, whereas the DF-IV undergoes a stretch-shorten cycle with large strain amplitudes and small net strains of 1-8\%. Furthermore, the DF-IV operates at higher muscle stresses (92-130 kPa, compared to 23-39 kPa for LG) and possesses a longer tendon, which allows the DF-IV tendon to recover greater elastic energy than the LG tendon. During incline locomotion, these muscles contribute only one-third of the energy expected for their mass, with the DF-IV exhibiting high stride-to-stride variability in work output. While the stretch-shorten cycle of the DF-IV muscle may allow more economic force production, it also leads to large changes in work output with small changes in the relative timing of force and strain. Thus, while the primary determinants of LG work are net strain and mean force, the primary determinant of DF-IV work is the phase relationship between force and strain. Our results suggest that, in addition to influencing a muscle{\textquoteright}s mechanical performance during steady level locomotion, morphology also affects its capacity and mechanism for altering work output for different locomotor tasks.}, keywords = {Analysis of Variance, Animals, Biomechanical Phenomena, Birds/*physiology, Electromyography, Locomotion/*physiology, Lower Extremity/*physiology, Muscle Contraction/*physiology, Muscle, Skeletal/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Daley, M. A. and Biewener, A. A.} } @article {548011, title = {In vivo and in vitro heterogeneity of segment length changes in the semimembranosus muscle of the toad}, journal = {J PhysiolJ PhysiolJ Physiol}, volume = {549}, number = {Pt 3}, year = {2003}, note = {Ahn, A NMonti, R JBiewener, A AengF32 AR08646/AR/NIAMS NIH HHS/F32 AR47741/AR/NIAMS NIH HHS/Research Support, U.S. Gov{\textquoteright}t, P.H.S.England2003/04/30 05:00J Physiol. 2003 Jun 15;549(Pt 3):877-88. Epub 2003 Apr 25.}, month = {Jun 15}, pages = {877-88}, abstract = {Many studies examine sarcomere dynamics in single fibres or length-tension dynamics in whole muscles in vivo or in vitro, but few studies link the various levels of organisation. To relate data addressing in vitro muscle segment behaviour with in vivo whole muscle behaviour during locomotion, we measured in vivo strain patterns of muscle segments using three sonomicrometry crystals implanted along a fascicle of the semimembranosus muscle in the American toad (Bufo americanus; n = 6) during hopping. The centre crystal emitted an ultrasonic signal, while the outer crystals received the signal allowing the instantaneous measurement of lengths from two adjacent muscle segments. On the first day, we recorded from the central and distal segments. On the second day of recordings, the most distal crystal was moved to a proximal position to record from a proximal segment and the same central segment. When the toads hopped a distance of two body lengths, the proximal and central segments strained -15.1 +/- 6.1 and -14.0 +/- 4.9 \% (i.e. shortening), respectively. Strain of the distal segment, however, was significantly lower and more variable in pattern, often lengthening before shortening during a hop. From rest length, the distal segment initially lengthened by 2.6 +/- 2.0 \% before shortening by 6.5 +/- 3.2 \% at the same hop distance. Under in vitro conditions, the central segment always shortened more than the distal segment, except when passively cycled, during which the segments strained similarly. When the whole muscle was cycled sinusoidally and stimulated phasically in vitro, the two adjacent segments strained in opposite directions over much (up to 34 \%) of the cycle. These differences in strain amplitude and direction imply that two adjacent segments can not only produce and/or absorb varying amounts of mechanical energy, but can also operate on different regions of their force-length and force-velocity relationships when activated by the same neural signal. Understanding regional differences in contractile dynamics within muscles is therefore important to linking our understanding of sarcomere behaviour with whole muscle behaviour during locomotion.}, keywords = {Animals, Bufonidae, Electromyography, Models, Neurological, Movement/physiology, Muscle Contraction/physiology, Muscle Fibers, Skeletal/physiology, Muscle, Skeletal/*anatomy \& histology/*physiology/ultrastructure, Sarcomeres/physiology, Ultrasonics}, isbn = {0022-3751 (Print)0022-3751 (Linking)}, author = {Ahn, A. N. and Monti, R. J. and Biewener, A. A.} } @article {548371, title = {Energetics and mechanics of human running on surfaces of different stiffnesses}, journal = {J Appl Physiol (1985)J Appl Physiol (1985)J Appl Physiol (1985)}, volume = {92}, number = {2}, year = {2002}, note = {Kerdok, Amy EBiewener, Andrew AMcMahon, Thomas AWeyand, Peter GHerr, Hugh MengResearch Support, Non-U.S. Gov{\textquoteright}tBethesda, Md. : 19852002/01/18 10:00J Appl Physiol (1985). 2002 Feb;92(2):469-78.}, month = {Feb}, pages = {469-78}, abstract = {Mammals use the elastic components in their legs (principally tendons, ligaments, and muscles) to run economically, while maintaining consistent support mechanics across various surfaces. To examine how leg stiffness and metabolic cost are affected by changes in substrate stiffness, we built experimental platforms with adjustable stiffness to fit on a force-plate-fitted treadmill. Eight male subjects [mean body mass: 74.4 +/- 7.1 (SD) kg; leg length: 0.96 +/- 0.05 m] ran at 3.7 m/s over five different surface stiffnesses (75.4, 97.5, 216.8, 454.2, and 945.7 kN/m). Metabolic, ground-reaction force, and kinematic data were collected. The 12.5-fold decrease in surface stiffness resulted in a 12\% decrease in the runner{\textquoteright}s metabolic rate and a 29\% increase in their leg stiffness. The runner{\textquoteright}s support mechanics remained essentially unchanged. These results indicate that surface stiffness affects running economy without affecting running support mechanics. We postulate that an increased energy rebound from the compliant surfaces studied contributes to the enhanced running economy.}, keywords = {*Energy Metabolism, Biomechanical Phenomena, Elasticity, Humans, Leg/*physiology, Male, Models, Biological, Running/*physiology}, isbn = {8750-7587 (Print)0161-7567 (Linking)}, author = {Kerdok, A. E. and Biewener, A. A. and McMahon, T. A. and Weyand, P. G. and Herr, H. M.} } @article {548311, title = {Estimates of circulation and gait change based on a three-dimensional kinematic analysis of flight in cockatiels (Nymphicus hollandicus) and ringed turtle-doves (Streptopelia risoria)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {205}, number = {Pt 10}, year = {2002}, note = {Hedrick, Tyson LTobalske, Bret WBiewener, Andrew AengComparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2002/04/27 10:00J Exp Biol. 2002 May;205(Pt 10):1389-409.}, month = {May}, pages = {1389-409}, abstract = {Birds and bats are known to employ two different gaits in flapping flight, a vortex-ring gait in slow flight and a continuous-vortex gait in fast flight. We studied the use of these gaits over a wide range of speeds (1-17 ms(-1)) and transitions between gaits in cockatiels (Nymphicus hollandicus) and ringed turtle-doves (Streptopelia risoria) trained to fly in a recently built, variable-speed wind tunnel. Gait use was investigated via a combination of three-dimensional kinematics and quasi-steady aerodynamic modeling of bound circulation on the distal and proximal portions of the wing. Estimates of lift from our circulation model were sufficient to support body weight at all but the slowest speeds (1 and 3 ms(-1)). From comparisons of aerodynamic impulse derived from our circulation analysis with the impulse estimated from whole-body acceleration, it appeared that our quasi-steady aerodynamic analysis was most accurate at intermediate speeds (5-11 ms(-1)). Despite differences in wing shape and wing loading, both species shifted from a vortex-ring to a continuous-vortex gait at 7 ms(-1). We found that the shift from a vortex-ring to a continuous-vortex gait (i) was associated with a phase delay in the peak angle of attack of the proximal wing section from downstroke into upstroke and (ii) depended on sufficient forward velocity to provide airflow over the wing during the upstroke similar to that during the downstroke. Our kinematic estimates indicated significant variation in the magnitude of circulation over the course the wingbeat cycle when either species used a continuous-vortex gait. This variation was great enough to suggest that both species shifted to a ladder-wake gait as they approached the maximum flight speed (cockatiels 15 ms(-1), doves 17 ms(-1)) that they would sustain in the wind tunnel. This shift in flight gait appeared to reflect the need to minimize drag and produce forward thrust in order to fly at high speed. The ladder-wake gait was also employed in forward and vertical acceleration at medium and fast flight speeds.}, keywords = {Animals, Birds/*physiology, Columbidae/physiology, Flight, Animal/*physiology, Gait/*physiology, Models, Biological, Postural Balance/physiology, Psittaciformes/*physiology, Species Specificity, Wind, Wing/physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Hedrick, T. L. and Tobalske, B. W. and Biewener, A. A.} } @article {548296, title = {Effects of surface grade on proximal hindlimb muscle strain and activation during rat locomotion}, journal = {J Appl Physiol (1985)J Appl Physiol (1985)J Appl Physiol (1985)}, volume = {93}, number = {5}, year = {2002}, note = {Gillis, Gary BBiewener, Andrew Aeng1F32AR-08559-01/AR/NIAMS NIH HHS/Research Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.Bethesda, Md. : 19852002/10/17 04:00J Appl Physiol (1985). 2002 Nov;93(5):1731-43.}, month = {Nov}, pages = {1731-43}, abstract = {Sonomicrometry and electromyography were used to determine how surface grade influences strain and activation patterns in the biceps femoris and vastus lateralis of the rat. Muscle activity is generally present during much of stance and is most intense on an incline, intermediate on the level, and lowest on a decline, where the biceps remains inactive except at high speeds. Biceps fascicles shorten during stance, with strains ranging from 0.07-0.30 depending on individual, gait, and grade. Shortening strains vary significantly among grades (P = 0.05) and average 0.21, 0.16, and 0.14 for incline, level, and decline walking, respectively; similar trends are present during trotting and galloping. Vastus fascicles are stretched while active over the first half of stance on all grades, and then typically shorten over the second half of stance. Late-stance shortening is highest during galloping, averaging 0.14, 0.10, and 0.02 in the leading limb on incline, level, and decline surfaces, respectively. Our results suggest that modulation of strain and activation in these proximal limb muscles is important for accommodating different surface grades.}, keywords = {*Hindlimb, Animals, Electromyography, Female, Motor Activity/*physiology, Muscle, Skeletal/*physiology/ultrasonography, Rats, Rats, Sprague-Dawley, Stress, Mechanical, Time Factors}, isbn = {8750-7587 (Print)0161-7567 (Linking)}, author = {Gillis, G. B. and Biewener, A. A.} } @article {548091, title = {Future directions for the analysis of musculoskeletal design and locomotor performance}, journal = {J MorpholJ MorpholJ Morphol}, volume = {252}, number = {1}, year = {2002}, note = {Biewener, Andrew AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.2002/03/29 10:00J Morphol. 2002 Apr;252(1):38-51.}, month = {Apr}, pages = {38-51}, abstract = {New techniques and conceptual frameworks offer new challenges and exciting opportunities for research on the biomechanics and physiology of vertebrate musculoskeletal design and locomotor performance. Past research based on electromyography and two-dimensional kinematics has greatly advanced the field of vertebrate functional morphology. Studies using these approaches have revealed much about vertebrate structure and function and have emphasized the importance of incorporating historical and developmental constraint and ecological context. Continued use of these experimental tools, but with greater emphasis on three-dimensional analysis of body movement, in combination with 3D kinetics and flow visualization of fluid movement past moving organisms, can now take advantage of the considerable advances in computing power and digital video technology. Indeed, surprisingly few detailed 3D analyses of movement for many locomotor modes and differing organisms are presently available. A challenge of 3D analyses will be to reduce the complexity of the data obtained in order to identify general principles of movement and biomechanics. New techniques and approaches for measuring muscle forces and length changes, together with activation patterns and movement, under dynamic conditions of more varied motor behavior are now also available. These provide the opportunity to study the mechanics and physiology of muscle function at greater depth and under more realistic conditions than has been previously possible. The importance of studying intact, behaving organisms under a broader range of locomotor conditions (other than steady state) and in the context of their natural environment remains a critical need for vertebrate biologists. This provides the much-needed opportunity for placing advances at more cellular and molecular levels into the context of whole organism function. Hence, studies at the organismal level remain paramount.}, keywords = {Animals, Biomechanical Phenomena, Forecasting, Image Processing, Computer-Assisted, Imaging, Three-Dimensional, Motor Activity/*physiology, Muscles/anatomy \& histology/*physiology, Musculoskeletal System/*anatomy \& histology, Vertebrates/anatomy \& histology/*physiology}, isbn = {0362-2525 (Print)0022-2887 (Linking)}, author = {Biewener, A. A.} } @article {548096, title = {Walking with tyrannosaurs}, journal = {NatureNatureNature}, volume = {415}, number = {6875}, year = {2002}, note = {Biewener, Andrew AengCommentNewsEngland2002/03/05 10:00Nature. 2002 Feb 28;415(6875):971-3.}, month = {Feb 28}, pages = {971-3}, keywords = {*Dinosaurs/physiology, *Walking/physiology, Alligators and Crocodiles, Animals, Biomechanical Phenomena, Body Constitution, Body Weight, Chickens, Extremities, Muscle, Skeletal/physiology}, isbn = {0028-0836 (Print)0028-0836 (Linking)}, author = {Biewener, A. A.} } @article {548581, title = {Pectoralis muscle performance during ascending and slow level flight in mallards (Anas platyrhynchos)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {204}, number = {Pt 3}, year = {2001}, note = {Williamson, M RDial, K PBiewener, A AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2001/02/15 11:00J Exp Biol. 2001 Feb;204(Pt 3):495-507.}, month = {Feb}, pages = {495-507}, abstract = {In vivo measurements of pectoralis muscle length change and force production were obtained using sonomicrometry and delto-pectoral bone strain recordings during ascending and slow level flight in mallards (Anas platyrhynchos). These measurements provide a description of the force/length properties of the pectoralis under dynamic conditions during two discrete flight behaviors and allow an examination of the effects of differences in body size and morphology on pectoralis performance by comparing the results with those of a recent similar study of slow level flight in pigeons (Columbia livia). In the present study, the mallard pectoralis showed a distinct pattern of active lengthening during the upstroke. This probably enhances the rate of force generation and the magnitude of the force generated and, thus, the amount of work and power produced during the downstroke. The power output of the pectoralis averaged 17.0 W kg(-)(1 )body mass (131 W kg(-)(1 )muscle mass) during slow level flight (3 m s(-)(1)) and 23.3 W kg(-)(1 )body mass (174 W kg(-)(1 )muscle mass) during ascending flight. This increase in power was achieved principally via an increase in muscle strain (29 \% versus 36 \%), rather than an increase in peak force (107 N versus 113 N) or cycle frequency (8.4 Hz versus 8.9 Hz). Body-mass-specific power output of mallards during slow level flight (17.0 W kg(-)(1)), measured in terms of pectoralis mechanical power, was similar to that measured recently in pigeons (16.1 W kg(-)(1)). Mallards compensate for their greater body mass and proportionately smaller wing area and pectoralis muscle volume by operating with a high myofibrillar stress to elevate mechanical power output.}, keywords = {Animals, Columbidae, Flight, Animal/*physiology, Muscle Contraction/physiology, Pectoralis Muscles/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Williamson, M. R. and Dial, K. P. and Biewener, A. A.} } @article {548291, title = {Hindlimb muscle function in relation to speed and gait: in vivo patterns of strain and activation in a hip and knee extensor of the rat (Rattus norvegicus)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {204}, number = {Pt 15}, year = {2001}, note = {Gillis, G BBiewener, A Aeng1F32 AR08559-01/AR/NIAMS NIH HHS/Research Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.England2001/09/05 10:00J Exp Biol. 2001 Aug;204(Pt 15):2717-31.}, month = {Aug}, pages = {2717-31}, abstract = {Understanding how animals actually use their muscles during locomotion is an important goal in the fields of locomotor physiology and biomechanics. Active muscles in vivo can shorten, lengthen or remain isometric, and their mechanical performance depends on the relative magnitude and timing of these patterns of fascicle strain and activation. It has recently been suggested that terrestrial animals may conserve metabolic energy during locomotion by minimizing limb extensor muscle strain during stance, when the muscle is active, facilitating more economical force generation and elastic energy recovery from limb muscle-tendon units. However, whereas the ankle extensors of running turkeys and hopping wallabies have been shown to generate force with little length change (<6\% strain), similar muscles in cats appear to change length more substantially while active. Because previous work has tended to focus on the mechanical behavior of ankle extensors during animal movements, the actions of more proximal limb muscles are less well understood. To explore further the hypothesis of force economy and isometric behavior of limb muscles during terrestrial locomotion, we measured patterns of electromyographic (EMG) activity and fascicle strain (using sonomicrometry) in two of the largest muscles of the rat hindlimb, the biceps femoris (a hip extensor) and vastus lateralis (a knee extensor) during walking, trotting and galloping. Our results show that the biceps and vastus exhibit largely overlapping bursts of electrical activity during the stance phase of each step cycle in all gaits. During walking and trotting, this activity typically commences shortly before the hindlimb touches the ground, but during galloping the onset of activity depends on whether the limb is trailing (first limb down) or leading (second limb down), particularly in the vastus. In the trailing limb, the timing of the onset of vastus activity is slightly earlier than that observed during walking and trotting, but in the leading limb, this activity begins much later, well after the foot makes ground contact (mean 7\% of the step cycle). In both muscles, EMG activity typically ceases approximately two-thirds of the way through the stance phase. While electrically active during stance, biceps fascicles shorten, although the extent of shortening differs significantly among gaits (P<0.01). Total average fascicle shortening strain in the biceps is greater during walking (23+/-3\%) and trotting (27+/-5\%) than during galloping (12+/-5\% and 19+/-6\% in the trailing and leading limbs, respectively). In contrast, vastus fascicles typically lengthen (by 8-16\%, depending on gait) over the first half of stance, when the muscle is electrically active, before shortening slightly or remaining nearly isometric over much of the second half of stance. Interestingly, in the leading limb during galloping, vastus fascicles lengthen prior to muscle activation and exhibit substantial shortening (10+/-2\%) during the period when EMG activity is recorded. Thus, patterns of muscle activation and/or muscle strain differ among gaits, between muscles and even within the same muscle of contralateral hindlimbs (as during galloping). In contrast to the minimal strain predicted by the force economy hypothesis, our results suggest that proximal limb muscles in rats operate over substantial length ranges during stance over various speeds and gaits and exhibit complex and changing activation and strain regimes, exemplifying the variable mechanical roles that muscles can play, even during level, steady-speed locomotion.}, keywords = {*Gait, *Hindlimb, Animals, Biomechanical Phenomena, Hip Joint, Locomotion/*physiology, Muscle, Skeletal/*physiology, Rats/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Gillis, G. B. and Biewener, A. A.} } @article {548221, title = {Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {204}, number = {Pt 6}, year = {2001}, note = {Blob, R WBiewener, A AengNS10813-01/NS/NINDS NIH HHS/NS10813-02/NS/NINDS NIH HHS/Research Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.England2001/02/27 10:00J Exp Biol. 2001 Mar;204(Pt 6):1099-122.}, month = {Mar}, pages = {1099-122}, abstract = {In vivo measurements of strain in the femur and tibia of Iguana iguana (Linnaeus) and Alligator mississippiensis (Daudin) have indicated three ways in which limb bone loading in these species differs from patterns observed in most birds and mammals: (i) the limb bones of I. iguana and A. mississippiensis experience substantial torsion, (ii) the limb bones of I. iguana and A. mississippiensis have higher safety factors than those of birds or mammals, and (iii) load magnitudes in the limb bones of A. mississippiensis do not decrease uniformly with the use of a more upright posture. To verify these patterns, and to evaluate the ground and muscle forces that produce them, we collected three-dimensional kinematic and ground reaction force data from subadult I. iguana and A. mississippiensis using a force platform and high-speed video. The results of these force/kinematic studies generally confirm the loading regimes inferred from in vivo strain measurements. The ground reaction force applies a torsional moment to the femur and tibia in both species; for the femur, this moment augments the moment applied by the caudofemoralis muscle, suggesting large torsional stresses. In most cases, safety factors in bending calculated from force/video data are lower than those determined from strain data, but are as high or higher than the safety factors of bird and mammal limb bones in bending. Finally, correlations between limb posture and calculated stress magnitudes in the femur of I. iguana confirm patterns observed during direct bone strain recordings from A. mississippiensis: in more upright steps, tensile stresses on the anterior cortex decrease, but peak compressive stresses on the dorsal cortex increase. Equilibrium analyses indicate that bone stress increases as posture becomes more upright in saurians because the ankle and knee extensor muscles exert greater forces during upright locomotion. If this pattern of increased bone stress with the use of a more upright posture is typical of taxa using non-parasagittal kinematics, then similar increases in load magnitudes were probably experienced by lineages that underwent evolutionary shifts to a non-sprawling posture. High limb bone safety factors and small body size in these lineages could have helped to accommodate such increases in limb bone stress.}, keywords = {*Extremities, *Locomotion, Alligators and Crocodiles/*physiology, Animals, Biomechanical Phenomena, Bone and Bones/*physiology, Femur/physiology, Hindlimb, Iguanas/*physiology, Muscle, Skeletal/physiology, Stress, Mechanical, Tibia/physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Blob, R. W. and Biewener, A. A.} } @article {548141, title = {Dynamics of mallard (Anas platyrynchos) gastrocnemius function during swimming versus terrestrial locomotion}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {204}, number = {Pt 10}, year = {2001}, note = {Biewener, A ACorning, W RengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.England2001/04/24 10:00J Exp Biol. 2001 May;204(Pt 10):1745-56.}, month = {May}, pages = {1745-56}, abstract = {This study investigates how the contractile function of a muscle may be modulated to accommodate changes in locomotor mode and differences in the physical environment. In vivo recordings of lateral gastrocnemius (LG) activation, force development (measured using tendon buckle transducers) and length change (measured using sonomicrometry) were obtained from mallard ducks (Anas platyrhynchos) as they swam at steady speeds in a water tank and walked or ran on land. LG force recordings were compared with combined lateral and medial gastrocnemius (MG) muscle-tendon force recordings obtained from the contralateral limb, allowing force development by the MG to be estimated relative to that of the LG. Although similar stresses were calculated to act in the LG and MG muscles during terrestrial locomotion (126 and 115 kPa, respectively), stresses were considerably greater in the LG compared with the MG during swimming (62 versus 34 kPa, respectively). During both steady swimming and terrestrial locomotion, the LG developed force while shortening over a considerable range of its length (swimming 23.6 \% versus terrestrial 37.4 \%). Activation of the muscle occurred near the end of passive lengthening during the recovery stroke, just prior to muscle shortening. As a result, the muscle generated broad positive work loops during both locomotor modes. LG work during swimming (4.8 J x kg(-1)) averaged 37 \% of the work performed during terrestrial locomotion (13.1 J x kg(-1)), consistent with the twofold greater force and 58 \% greater strain of the muscle during walking and running. Because limb cycle frequency was similar for the two locomotor modes (swimming 2.65 versus terrestrial 2.61 Hz), differences in power output (swimming 12.6 W x kg(-1 )versus terrestrial 32.4 W x kg(-1)) largely reflected difference in work per cycle. Tendon elastic energy savings was a small fraction (<5 \%) of the work performed by the muscle, consistent with a fiber-tendon design of these two muscles that favors muscle work to produce limb movement with little tendon strain. These results are consistent with a higher cost of terrestrial locomotion in ducks compared with other, more cursorial birds that may operate their muscles more economically and achieve greater tendon elastic savings.}, keywords = {Animals, Biomechanical Phenomena, Ducks/anatomy \& histology/*physiology, Female, Implants, Experimental, Locomotion/*physiology, Male, Muscle Contraction, Muscle, Skeletal/anatomy \& histology/*physiology, Swimming/*physiology, Tendons/physiology, Video Recording}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A. and Corning, W. R.} } @article {548526, title = {Exercise and reduced muscle mass in starlings}, journal = {NatureNatureNature}, volume = {406}, number = {6796}, year = {2000}, note = {Swaddle, J PBiewener, A AengENGLAND2000/08/19 11:00Nature. 2000 Aug 10;406(6796):585-6.}, month = {Aug 10}, pages = {585-6}, keywords = {*Physical Exertion, Animals, Muscle, Skeletal/*physiology, Songbirds/*physiology}, isbn = {0028-0836 (Print)0028-0836 (Linking)}, author = {Swaddle, J. P. and Biewener, A. A.} } @article {548286, title = {Hindlimb extensor muscle function during jumping and swimming in the toad (Bufo marinus)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {203}, number = {Pt 23}, year = {2000}, note = {Gillis, G BBiewener, A Aeng1 F32 AR08559-01/AR/NIAMS NIH HHS/Research Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.ENGLAND2000/11/04 11:00J Exp Biol. 2000 Dec;203(Pt 23):3547-63.}, month = {Dec}, pages = {3547-63}, abstract = {Many anurans use their hindlimbs to generate propulsive forces during both jumping and swimming. To investigate the musculoskeletal dynamics and motor output underlying locomotion in such physically different environments, we examined patterns of muscle strain and activity using sonomicrometry and electromyography, respectively, during jumping and swimming in the toad Bufo marinus. We measured strain and electromyographic (EMG) activity in four hindlimb muscles: the semimembranosus, a hip extensor; the plantaris, an ankle extensor; and the gluteus and cruralis, two knee extensors. During jumping, these four muscles are activated approximately simultaneously; however, joint extension appears to be temporally staggered, with the hip beginning to extend prior to or initially faster than the more distal knee and ankle joints. Mirroring this pattern, the gluteus and plantaris shorten quite slowly and over a small distance during the first half of limb extension during take-off, before beginning to shorten rapidly. The hip and knee extensors finish shortening near the point of take-off (when the feet leave the ground), while the ankle-extending plantaris, which exhibits the longest-duration EMG burst, on average, always completes its shortening after take-off (mean 26 ms). During swimming, activation of the four muscles is also nearly synchronous at the start of a propulsive stroke. The onset of fascicle shortening is temporally staggered, with the knee extensors beginning to shorten first, prior to the hip and ankle extensors. In addition, the knee extensors also often exhibit some degree of slow passive shortening prior to the onset of EMG activity. The offset of muscle shortening during swimming is also staggered, and to a much greater extent than during jumping. During swimming, the cruralis and gluteus finish shortening first, the semimembranosus finishes 30-60 ms later, and the plantaris, which again exhibits the longest EMG burst, finishes shortening last (mean 150 ms after the cruralis). Interestingly, much of this extended shortening in the plantaris occurs at a relatively slow velocity and may reflect passive ankle extension caused by fluid forces, associated with previously generated unsteady (accelerative) limb movements, acting on the foot. Average EMG burst intensity tends to be greater during jumping than during swimming in all muscles but the gluteus. However, EMG burst duration only changes between jumping and swimming in the cruralis (duration during jumping is nearly twice as long as during swimming). The cruralis is also the only muscle to exhibit substantially greater fractional shortening during jumping (mean 0.28) than during swimming (mean 0.20 active strain, 0.22 total strain). On the basis of these results, it appears that toad hindlimb function is altered between jumping and swimming. Moreover, these functional differences are influenced by passive effects associated with physical differences between the external environments, but are also actively mediated by shifts in the motor output and mechanical behavior of several muscles.}, keywords = {*Hindlimb, Animals, Bufo marinus/*physiology, Electromyography, Locomotion/*physiology, Muscle Contraction, Muscle, Skeletal/*physiology, Swimming/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Gillis, G. B. and Biewener, A. A.} } @article {548186, title = {Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective}, journal = {Exerc Sport Sci RevExerc Sport Sci RevExerc Sport Sci Rev}, volume = {28}, number = {3}, year = {2000}, note = {Biewener, A ARoberts, T JengComparative StudyReview2000/08/05 11:00Exerc Sport Sci Rev. 2000 Jul;28(3):99-107.}, month = {Jul}, pages = {99-107}, abstract = {Muscle-tendon architecture underlies muscle function. Whereas muscles generally contribute most to mechanical work, tendons provide the majority of elastic energy savings. Isometric or eccentric contractions enhance force and further reduce energy cost. However, elastic savings is probably constrained by the need to reduce compliance for accurate control of position.}, keywords = {Animals, Biomechanical Phenomena, Energy Metabolism, Humans, Locomotion/*physiology, Muscle, Skeletal/anatomy \& histology/*physiology, Tendons/anatomy \& histology/*physiology, Weight-Bearing}, isbn = {0091-6331 (Print)0091-6331 (Linking)}, author = {Biewener, A. A. and Roberts, T. J.} } @article {548226, title = {Experimental alteration of limb posture in the chicken (Gallus gallus) and its bearing on the use of birds as analogs for dinosaur locomotion}, journal = {J MorpholJ MorpholJ Morphol}, volume = {240}, number = {3}, year = {1999}, note = {Carrano, M TBiewener, A AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.1999/06/15 10:00J Morphol. 1999 Jun;240(3):237-49.}, month = {Jun}, pages = {237-49}, abstract = {Extant birds represent the only diverse living bipeds, and can be informative for investigations into the life-history parameters of their extinct dinosaurian relatives. However, morphological changes that occurred during early avian evolution, including the unique adoption of a nearly horizontal femoral orientation associated with a shift in center of mass (CM), suggest that caution is warranted in the use of birds as analogs for nonavian dinosaur locomotion. In this study, we fitted a group of white leghorn chickens (Gallus gallus) with a weight suspended posterior to the hip in order to examine the effects on loading and morphology. This caused a CM shift that necessitated a change in femoral posture (by 35 degrees towards the horizontal, P < 0.001), and resulted in reorientation of the ground reaction force (GRF) vector relative to the femur (from 41 degrees to 82 degrees, P < 0.001). Despite similar strain magnitudes, an overall increase in torsion relative to bending (from 1.70 to 1.95 times bending, P < 0.001) was observed, which was weakly associated with a tendency for increased femoral cross-sectional dimensions (P = 0.1). We suggest that a relative increase in torsion is consistent with a change in femoral posture towards the horizontal, since this change increases the degree to which the bone axis and the GRF vector produce mediolateral long-axis rotation of the bone. These results support the hypothesis that a postural change during early avian evolution could underlie the allometric differences seen between bird and nonavian dinosaur femora by requiring more robust femoral dimensions in birds due to an increase in torsion.}, keywords = {*Paleontology, Animals, Biological Evolution, Biomechanical Phenomena, Chickens/*physiology, Extremities/*physiology, Femur/physiology, Gait/*physiology, Locomotion/physiology, Posture/*physiology, Torsion Abnormality, Weight-Bearing/physiology}, isbn = {0362-2525 (Print)0022-2887 (Linking)}, author = {Carrano, M. T. and Biewener, A. A.} } @article {548216, title = {In vivo locomotor strain in the hindlimb bones of alligator mississippiensis and iguana iguana: implications for the evolution of limb bone safety factor and non-sprawling limb posture}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {202 (Pt 9)}, year = {1999}, note = {BlobBiewenerEng1999/04/02 03:02J Exp Biol. 1999 May;202 (Pt 9):1023-46.}, month = {May}, pages = {1023-46}, abstract = {Limb postures of terrestrial tetrapods span a continuum from sprawling to fully upright; however, most experimental investigations of locomotor mechanics have focused on mammals and ground-dwelling birds that employ parasagittal limb kinematics, leaving much of the diversity of tetrapod locomotor mechanics unexplored. This study reports measurements of in vivo locomotor strain from the limb bones of lizard (Iguana iguana) and crocodilian (Alligator mississippiensis) species, animals from previously unsampled phylogenetic lineages with non-parasagittal limb posture and kinematics. Principal strain orientations and shear strain magnitudes indicate that the limb bones of these species experience considerable torsion during locomotion. This contrasts with patterns commonly observed in mammals, but matches predictions from kinematic observations of axial rotation in lizard and crocodilian limbs. Comparisons of locomotor load magnitudes with the mechanical properties of limb bones in Alligator and Iguana indicate that limb bone safety factors in bending for these species range from 5.5 to 10.8, as much as twice as high as safety factors previously calculated for mammals and birds. Limb bone safety factors in shear (3.9-5.4) for Alligator and Iguana are also moderately higher than safety factors to yield in bending for birds and mammals. Finally, correlations between limb posture and strain magnitudes in Alligator show that at some recording locations limb bone strains can increase during upright locomotion, in contrast to expectations based on size-correlated changes in posture among mammals that limb bone strains should decrease with the use of an upright posture. These data suggest that, in some lineages, strain magnitudes may not have been maintained at constant levels through the evolution of a non-sprawling posture unless the postural change was accompanied by a shift to parasagittal kinematics or by an evolutionary decrease in body size.}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Blob, R. W. and Biewener, A. A.} } @article {548171, title = {Dynamics of muscle function during locomotion: accommodating variable conditions}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {202}, number = {Pt 23}, year = {1999}, note = {Biewener, A AGillis, G Beng1 F32 AR08559-01/AR/NIAMS NIH HHS/Research Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.ENGLAND1999/11/24 09:00J Exp Biol. 1999 Dec;202(Pt 23):3387-96.}, month = {Dec}, pages = {3387-96}, abstract = {Much of what we know about animal locomotion is derived from studies examining animals moving within a single, homogeneous environment, at a steady speed and along a flat grade. As a result, the issue of how musculoskeletal function might shift to accommodate variability within the external environment has remained relatively unexplored. One possibility is that locomotor muscles are differentially recruited depending upon the environment in which the animal is moving. A second possibility is that the same muscles are recruited, but that they are activated in a different manner so that their contractile function differs according to environment. Finally, it is also possible that, in some cases, animals may not need to alter their musculoskeletal function to move under different external conditions. In this case, however, the mechanical behavior appropriate for one environmental condition may constrain locomotor performance in another. To begin to explore the means by which animals accommodate variable conditions in their environment, we present three case studies examining how musculoskeletal systems function to allow locomotion under variable conditions: (1) eels undulating through water and across land, (2) turkeys running on level and inclined surfaces, and (3) ducks using their limbs to walk and to paddle. In all three of these examples, the mechanical behavior of some muscle(s) involved in locomotion are altered, although to different degrees and in different ways. In the running turkeys, the mechanical function of a major ankle extensor muscle shifts from contracting isometrically on a flat surface (producing little work and power), to shortening actively during contraction on an uphill gradient (increasing the amount of work and power generated). In the ducks, the major ankle extensor undergoes the same general pattern of activation and shortening in water and on land, except that the absolute levels of muscle stress and strain and work output are greater during terrestrial locomotion. In eels, a transition to land elicits changes in electromyographic duty cycles and the relative timing of muscle activation, suggesting some alteration in the functional mechanics of the underlying musculature. Only by studying muscle function in animals moving under more variable conditions can we begin to characterize the functional breadth of the vertebrate musculoskeletal system and understand more fully its evolutionary design.}, keywords = {Animals, Biomechanical Phenomena, Environment, Gait/physiology, Locomotion/*physiology, Muscle, Skeletal/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A. and Gillis, G. B.} } @article {548376, title = {Evaluation of a bone{\textquoteright}s in vivo 24-hour loading history for physical exercise compared with background loading}, journal = {J Orthop ResJ Orthop ResJ Orthop Res}, volume = {16}, number = {1}, year = {1998}, note = {Konieczynski, D DTruty, M JBiewener, A AengAR39828-01A1/AR/NIAMS NIH HHS/Comparative StudyResearch Support, U.S. Gov{\textquoteright}t, P.H.S.1998/05/09J Orthop Res. 1998 Jan;16(1):29-37.}, month = {Jan}, pages = {29-37}, abstract = {The present study sought to answer two research questions. First, how distinctive, as a potential osteogenic stimulus, are short-duration bouts of treadmill exercise relative to sedentary background activity? Second, how well does daily effective strain stimulus relate the loading history for one such exercise program, in comparison with other experimental loading programs, to bone formation? In vivo cortical strains were measured in the tibiotarsus of White Leghorn chickens at a late stage of skeletal growth (14-34 weeks old) under the conditions of a previous investigation of bone formation in response to an exercise program (15 min/day, treadmill gait at 60\% maximum speed while carrying 20\% body mass) that included sedentary background activity. These strain data were compiled into 24-hour loading histories of peak cyclic strain, demonstrating that strains were statistically different for exercise and background activities (p < 0.0001), with both the magnitude and number of cyclic strain events being greater during exercise (generally greater than 500 microstrain, 2,500 cycles/day) than during background activity (generally less than 500 microstrain, mean: 775 cycles/day). Strains during exercise accounted for more than 97\% of the daily effective strain stimulus for bone adaptation, despite the fact that exercise comprised only 1\% of the daily period (15 min/day). The levels of the daily effective strain stimulus were similar to those calculated for strains engendered by artificial loading of functionally isolated avian ulnae, which either maintained bone mass or resulted in a 15\% increase of cortical cross-sectional area in both sets of studies. These results indicate that short-duration bouts of treadmill exercise and sedentary background activity can represent distinct osteogenic stimuli for adaptive bone modeling. They also provide experimental support for the use of a daily effective strain stimulus to quantify skeletal loading histories for differing programs of physical exercise, although the relative importance of other mechanical and nonmechanical factors requires further investigation.}, keywords = {*Physical Conditioning, Animal, Animals, Bone and Bones/*physiology, Bone Development, Chickens, Female, Male, Time Factors}, isbn = {0736-0266 (Print)0736-0266 (Linking)}, author = {Konieczynski, D. D. and Truty, M. J. and Biewener, A. A.} } @article {548241, title = {In vivo strains in pigeon flight feather shafts: implications for structural design}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {201 (Pt 22)}, year = {1998}, note = {CorningBiewenerEng1998/10/27 03:02J Exp Biol. 1998 Nov;201 (Pt 22):3057-65.}, month = {Nov}, pages = {3057-65}, abstract = {To evaluate the safety factor for flight feather shafts, in vivo strains were recorded during free flight from the dorsal surface of a variety of flight feathers of captive pigeons (Columba livia) using metal foil strain gauges. Strains recorded while the birds flew at a slow speed (approximately 5-6 m s-1) were used to calculate functional stresses on the basis of published values for the elastic modulus of feather keratin. These stresses were then compared with measurements of the failure stress obtained from four-point bending tests of whole sections of the rachis at a similar location. Recorded strains followed an oscillatory pattern, changing from tensile strain during the upstroke to compressive strain during the downstroke. Peak compressive strains were 2.2+/-0. 9 times (mean +/- s.d.) greater than peak tensile strains. Tensile strain peaks were generally not as large in more proximal flight feathers. Maximal compressive strains averaged -0.0033+/-0.0012 and occurred late in the downstroke. Bending tests demonstrated that feather shafts are most likely to fail through local buckling of their compact keratin cortex. A comparison of the mean (8.3 MPa) and maximum (15.7 MPa) peak stresses calculated from the in vivo strain recordings with the mean failure stress measured in four-point bending (137 MPa) yields a safety factor of between 9 and 17. Under more strenuous flight conditions, feather stresses are estimated to be 1.4-fold higher, reducing their safety factor to the range 6-12. These values seem high, considering that the safety factor of the humerus of pigeons has been estimated to be between 1.9 and 3.5. Several hypotheses explaining this difference in safety factor are considered, but the most reasonable explanation appears to be that flexural stiffness is more critical than strength to feather shaft performance.}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Corning, W. R. and Biewener, A. A.} } @article {548176, title = {In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {201}, number = {Pt 11}, year = {1998}, note = {Biewener, A AKonieczynski, D DBaudinette, R VengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.ENGLAND1998/05/13J Exp Biol. 1998 Jun;201(Pt 11):1681-94.}, month = {Jun}, pages = {1681-94}, abstract = {Moderate to large macropodids can increase their speed while hopping with little or no increase in energy expenditure. This has been interpreted by some workers as resulting from elastic energy savings in their hindlimb tendons. For this to occur, the muscle fibers must transmit force to their tendons with little or no length change. To test whether this is the case, we made in vivo measurements of muscle fiber length change and tendon force in the lateral gastrocnemius (LG) and plantaris (PL) muscles of tammar wallabies Macropus eugenii as they hopped at different speeds on a treadmill. Muscle fiber length changes were less than +/-0.5 mm in the plantaris and +/-2.2 mm in the lateral gastrocnemius, representing less than 2 \% of total fiber length in the plantaris and less than 6 \% in the lateral gastrocnemius, with respect to resting length. The length changes of the plantaris fibers suggest that this occurred by means of elastic extension of attached cross-bridges. Much of the length change in the lateral gastrocnemius fibers occurred at low force early in the stance phase, with generally isometric behavior at higher forces. Fiber length changes did not vary significantly with increased hopping speed in either muscle (P>0.05), despite a 1. 6-fold increase in muscle-tendon force between speeds of 2.5 and 6.0 m s-1. Length changes of the PL fibers were only 7+/-4 \% and of the LG fibers 34+/-12 \% (mean +/- S.D., N=170) of the stretch calculated for their tendons, resulting in little net work by either muscle (plantaris 0.01+/-0.03 J; gastrocnemius -0.04+/-0.30 J; mean +/- s.d. ). In contrast, elastic strain energy stored in the tendons increased with increasing speed and averaged 20-fold greater than the shortening work performed by the two muscles. These results show that an increasing amount of strain energy stored within the hindlimb tendons is usefully recovered at faster steady hopping speeds, without being dissipated by increased stretch of the muscles{\textquoteright} fibers. This finding supports the view that tendon elastic saving of energy is an important mechanism by which this species is able to hop at faster speeds with little or no increase in metabolic energy expenditure.}, keywords = {*Locomotion, Animals, Biomechanical Phenomena, Elasticity, Electromyography, Energy Metabolism, Female, Macropodidae/*physiology, Male, Muscle Contraction, Muscle Fibers, Skeletal/physiology, Muscle, Skeletal/anatomy \& histology/*physiology, Tendons/physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A. and Konieczynski, D. D. and Baudinette, R. V.} } @article {548146, title = {In vivo pectoralis muscle force-length behavior during level flight in pigeons (Columba livia)}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {201 (Pt 24)}, year = {1998}, note = {BiewenerCorningTobalskeEng1998/11/18 03:02J Exp Biol. 1998 Dec;201 (Pt 24):3293-307.}, month = {Dec}, pages = {3293-307}, abstract = {For the first time, we report in vivo measurements of pectoralis muscle length change obtained using sonomicrometry combined with measurements of its force development via deltopectoral crest strain recordings of a bird in free flight. These measurements allow us to characterize the contractile behavior and mechanical power output of the pectoralis under dynamic conditions of slow level flight in pigeons Columba livia. Our recordings confirm that the pigeon pectoralis generates in vivo work loops that begin with the rapid development of force as the muscle is being stretched or remains nearly isometric near the end of the upstroke. The pectoralis then shortens by a total of 32 \% of its resting length during the downstroke, generating an average of 10.33.6 J kg-1 muscle (mean s.d.) of work per cycle for the anterior and posterior sites recorded among the five animals. In contrast to previous kinematic estimates of muscle length change relative to force development, the sonomicrometry measurements of fascicle length change show that force declines during muscle shortening. Simultaneous measurements of fascicle length change at anterior and posterior sites within the same muscle show significant (P<0.001, three of four animals) differences in fractional length (strain) change that averaged 1912 \%, despite exhibiting similar work loop shape. Length changes at both anterior and posterior sites were nearly synchronous and had an asymmetrical pattern, with shortening occupying 63 \% of the cycle. This nearly 2:1 phase ratio of shortening to lengthening probably favors the ability of the muscle to do work. Mean muscle shortening velocity was 5.381.33 and 4.881.27 lengths s-1 at the anterior and posterior sites respectively. Length excursions of the muscle were more variable at the end of the downstroke (maximum shortening), particularly when the birds landed, compared with highly uniform length excursions at the end of the upstroke (maximum lengthening). When averaged for the muscle as a whole, our in vivo work measurements yield a mass-specific net mechanical power output of 70. 2 W kg-1 for the muscle when the birds flew at 5-6 m s-1, with a wingbeat frequency of 8.7 Hz. This is 38 \% greater than the value that we obtained previously for wild-type pigeons, but still 24-50 \% less than that predicted by theory.}, isbn = {1477-9145 (Electronic)0022-0949 (Linking)}, author = {Biewener, A. A. and Corning, W. R. and Tobalske, B. W.} } @article {548086, title = {Muscle-tendon stresses and elastic energy storage during locomotion in the horse}, journal = {Comp Biochem Physiol B Biochem Mol BiolComp Biochem Physiol B Biochem Mol BiolComp Biochem Physiol B Biochem Mol Biol}, volume = {120}, number = {1}, year = {1998}, note = {Biewener, A AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.ReviewENGLAND1998/10/27Comp Biochem Physiol B Biochem Mol Biol. 1998 May;120(1):73-87.}, month = {May}, pages = {73-87}, abstract = {The stresses acting in muscle-tendon units and ligaments of the forelimb and hindlimb of horses were determined over a range of speed and gait based on recordings of ground reaction forces and limb kinematics. Maximum stresses of 40-50 MPa were calculated to act in several of the principal forelimb (superficial digital flexor (SDF), deep digital flexor (DDF), ulnaris lateralis (UL) and flexor carpi ulnaris/radialis (FCU/R)) and hindlimb tendons (plantaris, DDF) at the fastest galloping speeds recorded (up to 7.4 m s-1). Smaller stresses were found for the gastrocnemius (GAST) tendon (30 MPa) and suspensory ligaments (S-Ligs) (18-25 MPa). Average peak muscle stresses reached 200-240 kPa during galloping. Tendon and muscle stresses increased more steeply with changes of gait and during galloping, than during trotting. Calculations of elastic strain energy storage based on tendon stress showed similar patterns of increase with change of speed and gait, with the greatest contribution to elastic savings by the DDF tendons of the forelimb and hindlimb. In general, the hindlimb contributed two-thirds and the forelimb one-third to overall energy storage. Comparison of tendon elastic energy savings with mechanical work showed a maximum 40\% recovery of mechanical work by elastic savings when the horses changed gait from a walk to a slow trot. Percentage of recovery then decreased with increased trotting speed, but increased again with a change of gait to a gallop, reaching 36\% recovery at the fastest measured galloping speed (7.4 m s-1). The long length of horse tendons in relation to extremely short pennate muscle fibers suggests a highly specialized design for economical muscle force generation and enhanced elastic energy savings. However, elastic energy savings in terms of percentage of recovery of mechanical work and metabolic energy is less than that observed in wallabies and kangaroos during hopping, but similar to that in humans during running, and greater than that for dogs during trotting and galloping.}, keywords = {Animals, Energy Metabolism/*physiology, Extremities/physiology, Horses/*physiology, Locomotion/*physiology, Muscles/*physiology, Stress, Physiological/physiopathology, Tendons/*physiology}, isbn = {1096-4959 (Print)1096-4959 (Linking)}, author = {Biewener, A. A.} } @article {548166, title = {Adaptive changes in trabecular architecture in relation to functional strain patterns and disuse}, journal = {BoneBoneBone}, volume = {19}, number = {1}, year = {1996}, note = {Biewener, A AFazzalari, N LKonieczynski, D DBaudinette, R VengAR39828/AR/NIAMS NIH HHS/Research Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, P.H.S.1996/07/01Bone. 1996 Jul;19(1):1-8.}, month = {Jul}, pages = {1-8}, abstract = {Principal strains and their orientation, determined from in vivo and in situ strains recorded from the lateral cortical surface of the calcaneus of potoroos (a small marsupial) during treadmill exercise and tension applied via the Achilles tendon, were compared with the underlying trabecular architecture and its alignment to test Wolff{\textquoteright}s "trajectorial theory" of trabecular alignment. In vivo and in situ principal compressive strains (-800 to -2000 mu e) were found to be aligned (mean 161 +/- 7 degrees) close to the preferred alignment (160 degrees) of underlying trabeculae within the calcaneal metaphysis [a second trabecular arcade was closely aligned (70 degrees) with the direction (71 degrees) of principal tensile strain]. This finding represents quantitative verification of Wolff{\textquoteright}s trajectorial theory of trabecular alignment. These trabecular alignments, as measured by trabecular anisotropy (TbAn, the ratio of horizontal: vertical intercepts), remained unchanged (p > 0.05) after 8 weeks of disuse. However, trabecular bone volume fraction (BV/TV, -35\%), trabecular thickness (TbTh, -25\%), and trabecular number (TbN, -16\%) were reduced for the tenotomized calcaneii relative to their contralateral controls (p < 0.001 to < 0.003). The reduction in trabecular number was associated with a corresponding increase in trabecular spacing (TbSp, +30\%). Together, these results suggest that once trabecular alignment is established during growth (along the directions of principal strain during locomotion), it is not altered when functional strains are removed.}, keywords = {*Adaptation, Physiological, *Stress, Mechanical, Animals, Bone Resorption/physiopathology, Calcaneus/pathology/*physiology/radiography, Female, Immobilization/*adverse effects, Male, Marsupialia, Physical Conditioning, Animal/*adverse effects}, isbn = {8756-3282 (Print)1873-2763 (Linking)}, author = {Biewener, A. A. and Fazzalari, N. L. and Konieczynski, D. D. and Baudinette, R. V.} } @article {548126, title = {Structural response of growing bone to exercise and disuse}, journal = {J Appl Physiol (1985)J Appl Physiol (1985)J Appl Physiol (1985)}, volume = {76}, number = {2}, year = {1994}, note = {Biewener, A ABertram, J EengAR-39828/AR/NIAMS NIH HHS/Research Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, P.H.S.Bethesda, Md. : 19851994/02/01J Appl Physiol (1985). 1994 Feb;76(2):946-55.}, month = {Feb}, pages = {946-55}, abstract = {The limbs of growing chicks (2-12 wk of age) were subjected to differing conditions of mechanical use to examine the effect of extrinsic loading on bone modeling early in postnatal growth. One group of chicks was subjected to intensive exercise by running on a treadmill 5 days/wk at 60\% maximum speed while carrying on their trunk a load equal to 20\% of body weight (EXER). In a second group, weight-bearing function was eliminated by sciatic denervation of one hindlimb at 2 wk of age (DNV). A third group grew under sedentary conditions (SED). Comparisons among groups were made on the basis of bone mass and length, cortical cross-sectional area and second moment of area, cortical thickness, longitudinal curvature, and \% ash. After normalizing for growth-related differences in body mass among the three groups, we found that exercise led to an overall 16 +/- 13\% increase in cortical cross-sectional area and a 26 +/- 21\% increase in second moment of area measured at proximal, midshaft, and distal levels of the bone compared with values of SED animals. These increases in cortical geometry corresponded to a 10\% increase in total bone mass and were generally established by 8 wk of age (6 wk of training) and maintained to 12 wk of age. When deprived of functional use, the growing bones of DNV animals were reduced in mass (-19\%), cortical area (-8 +/- 7\%), and second moment of area (-11 +/- 9\%) compared with SED animals. DNV tibiotarsi were also significantly shorter (7\% at 8 wk and 14\% at 12 wk); however, the contralateral load-bearing tibiotarsus of the DNV animals was similarly reduced compared with SED and EXER animals, suggesting a general reduction of growth in the DNV group. Even more pronounced than the reductions in bone mass and area, however, were the loss of normal longitudinal curvature and an increase in the variability of cross-sectional shape and cortical thickness of the DNV tibiotarsi compared with SED and EXER animals.}, keywords = {*Bone Development, *Physical Exertion, Aging/physiology, Animals, Animals, Newborn, Bone and Bones/radiography, Bone Density, Chickens, Male, Motor Activity/physiology, Weight-Bearing}, isbn = {8750-7587 (Print)0161-7567 (Linking)}, author = {Biewener, A. A. and Bertram, J. E.} } @article {548121, title = {Skeletal strain patterns in relation to exercise training during growth}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {185}, year = {1993}, note = {Biewener, A ABertram, J EengAR 39828/AR/NIAMS NIH HHS/Research Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, P.H.S.ENGLAND1993/12/01J Exp Biol. 1993 Dec;185:51-69.}, month = {Dec}, pages = {51-69}, abstract = {Bones are believed to alter their shape in response to changes in tissue strains produced by physical activity and the goal of this study is to examine whether modeling responses of a growing bone to changes in physical exercise are adjusted to maintain a uniform distribution of functional strains. We test this idea by comparing in vivo strains recorded in the tibiotarsus of white leghorn chicks during {\textquoteright}intensive{\textquoteright} treadmill exercise (60\% of maximum speed, carrying a weight equal to 20\% body weight on the trunk: 60\%/L) with strains that had been recorded previously during {\textquoteright}moderate{\textquoteright} treadmill exercise (35\% of maximum speed, unloaded: 35\%/UNL) at similar bone sites. Our hypothesis is that modeling adjustments of bones subjected to the intensive load-carrying exercise should re-establish strains recorded in the bones subjected to moderate exercise. At each exercise level, the animals were exercised for 5 days per week (2500 loading cycles per day) from 2 to 12 weeks of age. As in the moderate exercise group studied earlier, strains measured at six functionally equivalent sites on the tibiotarsus of the 60\%/L group were consistently maintained during growth from 4 to 12 weeks of age. In addition, the pattern of strain recorded at these sites was uniformly maintained over the full range of speeds recorded (from 0.48 to 2.70 m s-1 at 12 weeks of age). Peak strains measured at 4 weeks of age in the load-carrying exercise group were initially elevated by 57\% overall compared with peak strains recorded in the moderate exercise group. At 8 weeks of age, strain levels in the 60\%/L group differed by only 4\% overall compared with those recorded in the 35\%/UNL group. The nature of strain (tensile versus compressive) and the orientation of principal strain at corresponding sites were also similar in the two groups. At 12 weeks of age, however, bone strain levels in the 60\%/L group were again elevated (47\% overall) compared with those recorded in the 35\%/UNL group, although the general pattern and orientation of strains remained similar. This finding suggests a transient modeling response of the bone to the onset of exercise training, which was lost during subsequent growth, possibly because the normal pattern of functional strain was not altered significantly by the faster load-carrying exercise.}, keywords = {*Bone Development, Aging, Animals, Bone and Bones/*physiology, Chickens, Male, Physical Exertion/*physiology, Stress, Mechanical}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A. and Bertram, J. E.} } @article {548081, title = {Safety factors in bone strength}, journal = {Calcif Tissue IntCalcif Tissue IntCalcif Tissue Int}, volume = {53 Suppl 1}, year = {1993}, note = {Biewener, A AengAR39828/AR/NIAMS NIH HHS/Comparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.Review1993/01/01Calcif Tissue Int. 1993;53 Suppl 1:S68-74.}, pages = {S68-74}, abstract = {Functional in vivo strain data are examined in relation to bone material properties in an attempt to evaluate the relative importance of osteoporotic bone loss versus fatigue damage accumulation as factors underlying clinical bone fragility. Specifically, does the skeleton have a sufficiently large safety factor (ratio of bone failure strain to maximum functional strain) to require that fatigue damage accumulation is the main factor contributing to increased risk of fracture in the elderly? Existing methods limit in vivo strain measurements to the surfaces of cortical bone. Peak principal compressive strains measured at cortical sites during strenuous activity in various mammalian and avian species range from -1700 to -5200 mu epsilon, averaging -2500 mu epsilon (-0.0025 strain). Much of this threefold variation reflects differences in the intensity of physical activity, as well as differences among species and bones that have been studied. Peak strains can also vary as much as tenfold at different cortical sites within the same bone. No data exist for cortical bone strain during strenuous activity in humans, but it is likely that human bones experience a similar range of peak strain levels. Compact bone fails in longitudinal compression at strains as high as -14,000 to -21,000 mu epsilon, but begins to yield at strains between -6000 and -8000 mu epsilon. Given that yielding involves rapid accumulation of microdamage within the bone, it seems prudent to base skeletal safety factors on the yield strain, rather than the ultimate failure strain of bone tissue. Safety factors to yield failure therefore range from 1.4 to 4.1.(ABSTRACT TRUNCATED AT 250 WORDS)}, keywords = {Aging/physiology, Animals, Biomechanical Phenomena, Bone Density/*physiology, Bone Remodeling, exercise, Fractures, Bone/etiology/*physiopathology, Humans, Osteoporosis/*physiopathology, Risk Factors, Stress, Mechanical}, isbn = {0171-967X (Print)0171-967X (Linking)}, author = {Biewener, A. A.} } @article {548281, title = {The functional morphology of xenarthrous vertebrae in the armadillo Dasypus novemcinctus (Mammalia, Xenarthra)}, journal = {J MorpholJ MorpholJ Morphol}, volume = {214}, number = {1}, year = {1992}, note = {Gaudin, T JBiewener, A AengComparative StudyResearch Support, Non-U.S. Gov{\textquoteright}t1992/10/01J Morphol. 1992 Oct;214(1):63-81.}, month = {Oct}, pages = {63-81}, abstract = {In order to assess the mechanical properties of xenarthrous vertebrae, and to evaluate the role of xenarthrae as fossorial adaptations, in vitro bending tests were performed on posterior thoracic and lumbar vertebral segments excised from specimens of the armadillo Dasypus novemcinctus and the opossum Didelphis virginiana, the latter being used to represent the primitive mammalian condition. The columns of the two species were subjected to dorsal, ventral, and lateral bending, as well as torsion, in order to determine their stiffness in each of these directions. During these tests, bone strains in the centra of selected vertebrae were determined using rosette strain gages. Overall stiffness of the armadillo backbone at physiologically relevant displacement levels was significantly higher than that of the opossum for both dorsal and lateral bending. The two species also exhibited significant differences in angular displacement of individual vertebrae and in vertebral strain magnitudes and orientations in these two directions. No significant differences were observed when the columns of the two species were subjected to torsion or to ventral bending. Our results suggest that some, but not all, of the mechanical differences between the two species are due to the presence of xenarthrae. For example, removal of the xenarthrae from selected vertebrae (L2-L4) changes strain orientation and shear, but not strain magnitudes. Comparisons with functional data from other digging mammals indicate that the modified mechanical properties of the Dasypus column are consistent with an interpretation of xenarthrae as digging adaptations and lend support to the idea that the order Xenarthra represents an early offshoot of placental mammals specialized for fossoriality.}, keywords = {Animals, Armadillos/*anatomy \& histology/physiology, Biomechanical Phenomena, Data Interpretation, Statistical, Opossums/anatomy \& histology/physiology, Species Specificity, Spine/*anatomy \& histology/physiology}, isbn = {0362-2525 (Print)0022-2887 (Linking)}, author = {Gaudin, TJ and Biewener, A. A.} } @article {548076, title = {Musculoskeletal design in relation to body size}, journal = {J BiomechJ BiomechJ Biomech}, volume = {24 Suppl 1}, year = {1991}, note = {Biewener, A AengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Review1991/01/01J Biomech. 1991;24 Suppl 1:19-29.}, pages = {19-29}, abstract = {Irrespective of body size and phylogenetic diversity, the skeletal systems of terrestrial mammals are built of tissue components having similar mechanical properties and material organization. Because of scale effects on skeletal form, therefore, larger mammals increase the effective mechanical advantage of their limbs to decrease mass-specific forces associated with the support of gravitational loads imposed during locomotion to maintain a similar safety factor. Larger animals accomplish this by adopting a more upright posture while running, which aligns their limb joints more closely with the resultant ground reaction force, thereby decreasing the mass-specific force that their muscles must generate to support externally applied joint moments. As a result, peak (compressive) bone stresses determined from in vivo bone strain recordings and force platform and kinematic analyses of the limb generally range from -40 to -80 MPa (mean: -55 +/- 23 MPa), corresponding to a safety factor to compressive bone failure of about three to four. The decrease in mass-specific muscle force indicates that the maximum stresses developed in limb muscles of different sized species are also similar at equivalent levels of performance. Stresses developed in the midshafts of most long bones are primarily the result of bending, often engendered by axial forces transmitted about the bone{\textquoteright}s longitudinal curvature. The consistency of bending-induced skeletal strain over a range of physical activity and the associated expense of increased strain magnitude that this form of loading incurs suggest that functional strain patterns developed through bending may be a desirable architectural objective of most long bones. Alteration of a bone{\textquoteright}s normal functional strain distribution, therefore, is likely a key factor underlying adaptive remodeling in response to changes in mechanical loading.}, keywords = {Animals, Biomechanical Phenomena, Body Constitution/*physiology, Bone and Bones/*anatomy \& histology/physiology, Locomotion/physiology, Muscles/*anatomy \& histology/physiology}, isbn = {0021-9290 (Print)0021-9290 (Linking)}, author = {Biewener, A. A.} } @article {548071, title = {Biomechanics of mammalian terrestrial locomotion}, journal = {ScienceScienceScience}, volume = {250}, number = {4984}, year = {1990}, note = {Biewener, A AengAM18140/AM/NIADDK NIH HHS/Research Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.New York, N.Y.1990/11/23Science. 1990 Nov 23;250(4984):1097-103.}, month = {Nov 23}, pages = {1097-103}, abstract = {Mammalian skeletons experience peak locomotor stresses (force per area) that are 25 to 50\% of their failure strength, indicating a safety factor of between two and four. The mechanism by which animals achieve a constant safety factor varies depending on the size of the animal. Over much of their size (0.1 to 300 kilograms), larger mammals maintain uniform skeletal stress primarily by having a more upright posture, which decreases mass-specific muscle force by increasing muscle mechanical advantage. At greater sizes, increased skeletal allometry and decreased locomotor performance likely maintain stresses constant. At smaller sizes, skeletal stiffness may be more critical than strength. The decrease in mass-specific muscle force in mammals weighing 0.1 to 300 kilogram indicates that peak muscle stresses are also constant and correlates with a decrease in mass-specific energy cost of locomotion. The consistent pattern of locomotor stresses developed in long bones at different speeds and gaits within a species may have important implications for how bones adaptively remodel to changes in stress.}, keywords = {Animals, Biomechanical Phenomena, Body Constitution, Bone and Bones/anatomy \& histology/*physiology, Bone Development, Bone Resorption, Energy Metabolism, Gait/physiology, Locomotion/*physiology, Mammals/*physiology, Muscle Contraction, Muscles/anatomy \& histology/*physiology, Posture, Stress, Mechanical}, isbn = {0036-8075 (Print)0036-8075 (Linking)}, author = {Biewener, A. A.} } @article {548041, title = {Differential scaling of the long bones in the terrestrial carnivora and other mammals}, journal = {J MorpholJ MorpholJ Morphol}, volume = {204}, number = {2}, year = {1990}, note = {Bertram, J EBiewener, A AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.1990/05/01J Morphol. 1990 May;204(2):157-69.}, month = {May}, pages = {157-69}, abstract = {We measured the lengths and diameters of four long bones from 118 terrestrial carnivoran species using museum specimens. Though intrafamilial regressions scaled linearly, nearly all intraordinal regressions scaled non-linearly. The observed non-linear scaling of bone dimensions within this order results from a systematic decrease in intrafamilial allometric slope with increasing body size. A change in limb posture (more upright in larger species) to maintain similar peak bone stresses may allow the nearly isometric scaling of skeletal dimensions observed in smaller sized mammals (below about 100 kg). However, strong positive allometry is consistently observed in a number of large terrestrial mammals (the largest Carnivora, the large Bovidae, and the Ceratomorpha). This suggests that the capacity to compensate for size increases through alteration of limb posture is limited in extremely large-sized mammals, such that radical changes in bone shape are required to maintain similar levels of peak bone stress.}, keywords = {Animals, Arm, Biometry, Bone and Bones/*anatomy \& histology, Carnivora/*anatomy \& histology, Female, Leg, Male, Mammals/*anatomy \& histology, Regression Analysis, Ruminants/anatomy \& histology}, isbn = {0362-2525 (Print)0022-2887 (Linking)}, author = {Bertram, J. E. and Biewener, A. A.} } @article {548531, title = {Telemetered in vivo strain analysis of locomotor mechanics of brachiating gibbons}, journal = {NatureNatureNature}, volume = {342}, number = {6247}, year = {1989}, note = {Swartz, S MBertram, J EBiewener, A AengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.ENGLAND1989/11/16Nature. 1989 Nov 16;342(6247):270-2.}, month = {Nov 16}, pages = {270-2}, abstract = {The slender elongated form that is characteristic of the forelimb long bones of gibbons (Hylobates) has long been attributed to their functional adaptation to habitual armswinging locomotion, although potential selective advantages of this morphology for brachiation have yet to be demonstrated. If the forces exerted on the limb skeleton during brachiation indeed differ greatly from those of other locomotor modes, then the changes in skeletal loading accompanying a shift in locomotor behaviour could favour alterations in skeletal morphology in brachiating lineages. In vivo skeletal strain patterns recorded by using radiotelemetry during brachiation indicate that the forelimb bones of the gibbon are loaded in substantial tension and show reduced bending and compression in comparison with those of other mammals. We suggest that this unique loading regime could have contributed to the evolution of the distinctive morphology of hylobatid limbs.}, keywords = {Animals, Arm/*physiology, Biological Evolution, Hominidae/*physiology, Humerus/physiology, Hylobates/*physiology, locomotion, Radius/physiology, Stress, Mechanical, telemetry, Ulna/physiology}, isbn = {0028-0836 (Print)0028-0836 (Linking)}, author = {Swartz, S. M. and Bertram, J. E. and Biewener, A. A.} } @article {548066, title = {Scaling body support in mammals: limb posture and muscle mechanics}, journal = {ScienceScienceScience}, volume = {245}, number = {4913}, year = {1989}, note = {Biewener, A AengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.New York, N.Y.1989/07/07Science. 1989 Jul 7;245(4913):45-8.}, month = {Jul 7}, pages = {45-8}, abstract = {The scaling of bone and muscle geometry in mammals suggests that peak stresses (ratio of force to cross-sectional area) acting in these two support elements increase with increasing body size. Observations of stresses acting in the limb bones of different sized mammals during strenuous activity, however, indicate that peak bone stress is independent of size (maintaining a safety factor of between 2 and 4). It appears that similar peak bone stresses and muscle stresses in large and small mammals are achieved primarily by a size-dependent change in locomotor limb posture: small animals run with crouched postures, whereas larger species run more upright. By adopting an upright posture, large animals align their limbs more closely with the ground reaction force, substantially reducing the forces that their muscles must exert (proportional to body mass) and hence, the forces that their bones must resist, to counteract joint moments. This change in limb posture to maintain locomotor stresses within safe limits, however, likely limits the maneuverability and accelerative capability of large animals.}, keywords = {Animals, Biomechanical Phenomena, Extremities/anatomy \& histology/physiology, Joints/physiology, Mammals/*physiology, Muscles/anatomy \& histology/*physiology, Posture, Species Specificity}, isbn = {0036-8075 (Print)0036-8075 (Linking)}, author = {Biewener, A. A.} } @article {548491, title = {Preferred speeds in terrestrial vertebrates: are they equivalent?}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {137}, year = {1988}, note = {Perry, A KBlickhan, RBiewener, A AHeglund, N CTaylor, C Reng5 R01 AM 18140/AM/NIADDK NIH HHS/Comparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, P.H.S.ENGLAND1988/07/01J Exp Biol. 1988 Jul;137:207-19.}, month = {Jul}, pages = {207-19}, abstract = {Terrestrial animals have {\textquoteright}preferred speeds{\textquoteright} within each gait, that are used much more frequently than others for moving along the ground. Energy costs reach minimal values at these speeds within each gait. In this study we asked whether these speeds are mechanically equivalent among different animals (i.e. speeds where the same levels of peak muscle stress occur). If so, this would help in establishing a link between the energetics and the mechanics of the active muscles at these speeds, providing a first step in understanding why energy costs are minimal. We also asked whether peak muscle stress reaches a similar fraction of the maximal isometric stress at these speeds. If so, this would suggest that muscles are structured so that a similar reserve capacity remains, with a similar safety factor for avoidance of injury in response to prolonged repetitive loading. We compared two species that use quite different locomotory methods at their preferred speeds: white rats that gallop and kangaroo rats that hop. We measured peak stress in the ankle extensor muscles of these two species, as they moved at their preferred speeds, using a force platform/cine analysis technique. We also measured the maximum isometric force that this muscle group could develop in situ in the same individuals. We found the ankle extensors of white rats and kangaroo rats developed virtually identical levels of peak stress at their preferred speeds (70 +/- 6 kPa and 69 +/- 6 kPa, respectively, mean +/- S.E.), despite a fourfold difference in peak ground reaction force per unit body mass exerted on each limb. The values of peak isometric stress in situ were also virtually identical (206 +/- 17 kPa and 200 +/- 9 kPa, respectively). Our finding that the peak muscle stress is about one-third of maximum isometric stress at the preferred speeds is consistent with the idea that these are mechanically equivalent speeds, where the same fraction of available muscle fibres is recruited. Finding nearly identical values in two species that move in such different ways (galloping vs hopping), and have such large differences in ground reaction force exerted by each limb, suggests this may be true more generally for terrestrial vertebrates.}, keywords = {*Locomotion, Animals, Dipodomys/*physiology, Gait, Isometric Contraction, Muscles/*physiology, Rats/*physiology, Rodentia/*physiology, Species Specificity, Stress, Mechanical}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Perry, A. K. and Blickhan, R. and Biewener, A. A. and Heglund, N. C. and Taylor, C. R.} } @article {548131, title = {Kangaroo rat locomotion: design for elastic energy storage or acceleration?}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {140}, year = {1988}, note = {Biewener, A ABlickhan, RengResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.ENGLAND1988/11/01J Exp Biol. 1988 Nov;140:243-55.}, month = {Nov}, pages = {243-55}, abstract = {Mechanical stresses (force/cross-sectional area) acting in muscles, tendons and bones of the hindlimbs of kangaroo rats (Dipodomys spectabilis) were calculated during steady-speed hops and vertical jumps. Stresses were determined from both high-speed cine films (light and X-ray) and force plate recordings, as well as from in vivo tendon force recordings. Stresses in each hindlimb support element during hopping (1.6-3.1 m s-1) were generally only 33\% of those acting during jumping (greater than or equal to 40 cm height): ankle extensor muscles, 80 +/- 12 (S.D.) versus 297 +/- 42 kPa; ankle extensor tendons, 7.9 +/- 1.5 versus 32.7 +/- 4.8 MPa; tibia, -29 +/- 5 versus -110 +/- 25 MPa (all values are for hopping versus jumping). The magnitude of stress in each structure during these locomotor activities was similarly matched to the strength of each element, so that a consistent safety factor to failure is achieved for the hindlimb as a whole (1.5-2.0). The large stresses during jumping were correlated with a three-fold increase in ground reaction forces exerted on the ground compared with the fastest steady hopping speeds. We conclude that, for its size, the kangaroo rat has disproportionately large hindlimb muscles, tendons and bones to withstand the large forces associated with rapid acceleration to avoid predation, which limits their ability to store and recover elastic strain energy. Middle ear morphology and behavioural observations of kangaroo rats jumping vertically to avoid predation by owls and rattlesnakes support this view.}, keywords = {*Energy Metabolism, *Locomotion, Acceleration, Analog-Digital Conversion, Animals, Behavior, Animal, Bone and Bones/metabolism/physiology, Deceleration, Dipodomys/*physiology, Hindlimb/anatomy \& histology/metabolism, Motion Pictures as Topic, Muscles/metabolism/physiology, Rodentia/*physiology, Safety, Stress, Mechanical, Tendons/metabolism/physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A. and Blickhan, R.} } @article {548136, title = {Muscle forces during locomotion in kangaroo rats: force platform and tendon buckle measurements compared}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {137}, year = {1988}, note = {Biewener, A ABlickhan, RPerry, A KHeglund, N CTaylor, C Reng5 R01 AM 18140/AM/NIADDK NIH HHS/Research Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.ENGLAND1988/07/01J Exp Biol. 1988 Jul;137:191-205.}, month = {Jul}, pages = {191-205}, abstract = {The muscle forces and stresses occurring during normal locomotor activity in kangaroo rats are compared with the peak isometric force developed by the same muscles in situ. Two methods were used simultaneously to determine the stresses (force/cross-sectional area) acting in the ankle extensors during steady-speed hopping and during jumps when animals were startled: a direct measurement using a force buckle surgically implanted around a tendon; and an indirect measurement using a force platform/cine analysis technique. We obtained essentially the same values with the two techniques. We found that at slow speeds (0.7 m s-1) the ankle extensor muscles of kangaroo rats exerted 20\% of the maximum isometric force developed when the muscles were stimulated via the tibial nerve. This increased to 53\% at higher speeds (1.9 m s-1). At the animals{\textquoteright}s preferred hopping speed (1.5 m s-1), peak force was approximately 40\% of maximum isometric force. In jumps when animals were startled, peak forces as high as 175\% of the maximal elicited isometric force were recorded. These high forces always occurred when the muscles were being stretched. It appears that kangaroo rats utilize nearly the entire range of muscle force possible during normal locomotor events (i.e. up to 175\% of maximum isometric force when muscles are stretched).}, keywords = {*Isometric Contraction, *Locomotion, *Muscle Contraction, Animals, Dipodomys/*physiology, Muscles/*physiology, Rodentia/*physiology, Stress, Mechanical, Tendons/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A. and Blickhan, R. and Perry, A. K. and Heglund, N. C. and Taylor, C. R.} } @article {548036, title = {Bone curvature: sacrificing strength for load predictability?}, journal = {J Theor BiolJ Theor BiolJ Theor Biol}, volume = {131}, number = {1}, year = {1988}, note = {Bertram, J EBiewener, A AengResearch Support, Non-U.S. Gov{\textquoteright}tENGLAND1988/03/07J Theor Biol. 1988 Mar 7;131(1):75-92.}, month = {Mar 7}, pages = {75-92}, abstract = {Nearly all long bones of terrestrial mammals that have been studied are loaded in bending. Yet bending requires greater bone mass than axial compression for effective support of equivalent static loads. Most long bones, in fact, are curved along their length; their curvature augmenting rather than diminishing stresses developed due to bending. The most "efficient" design of a bone (maximal strength per unit mass) should be a form which is straight and resists axial compression. Bone curvature and the bending developed in the long bones of most species studied, therefore, poses a paradox in design. However, under natural conditions an animal{\textquoteright}s skeleton must support a range of dynamic loads that vary in both direction and magnitude. Thus, improved predictability of dynamic loading should represent an important feature in the design of the bone, in addition to its absolute strength. We present an explanation of long bone curvature, based on the conditions of stability for bending vs. axial compression in a column, that describes this apparent design paradox as a mechanism for improving the predictability of loading direction (and, consequently, the pattern of stresses within the bone). Our hypothesis argues that in order to understand the design "effectiveness" of long bone shape the role of the bone as a structural unit must be redefined to one in which bone strength is optimized concurrently with loading predictability. In agreement with our hypothesis, bone curvature appears to meet this requirement.}, keywords = {Animals, Biomechanical Phenomena, Bone and Bones/*anatomy \& histology/physiology, Dogs, Mammals, Models, Anatomic, Running, Stress, Mechanical}, isbn = {0022-5193 (Print)0022-5193 (Linking)}, author = {Bertram, J. E. and Biewener, A. A.} } @article {548196, title = {Bone modeling during growth: dynamic strain equilibrium in the chick tibiotarsus}, journal = {Calcif Tissue IntCalcif Tissue IntCalcif Tissue Int}, volume = {39}, number = {6}, year = {1986}, note = {Biewener, A ASwartz, S MBertram, J EengResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, P.H.S.GERMANY, WEST1986/12/01Calcif Tissue Int. 1986 Dec;39(6):390-5.}, month = {Dec}, pages = {390-5}, abstract = {Bone loading was quantified, using in vivo strain recordings, in the tibiotarsus of growing chicks at 4, 8, 12, and 17 weeks of age. The animals were exercised on a treadmill at 35\% of their maximum running speed for 15 minutes/day. In vivo bone strains were recorded at six sites on the tibiotarsus. Percentages of the bone{\textquoteright}s length and a percentage of top running speed were used to define functionally equivalent sites on the bone, and a consistent exercise level over the period of growth was studied. The pattern of bone strain defined in terms of strain magnitude, sign, and orientation remained unchanged from 4-17 weeks of age, a period when bone mass and length increased 10-fold and threefold, respectively. Our findings support the hypothesis that bones model (and remodel) during growth to achieve and maintain a similar distribution of dynamic strains at functionally equivalent sites. Because strain magnitude and sign (tensile versus compressive) differed among recording sites, these data also suggest that cellular responses to strain-mediated stimuli differ from site to site within a bone.}, keywords = {*Bone Development, Animals, Biomechanical Phenomena, Chickens/growth \& development, Physical Exertion, Stress, Mechanical, Tarsus, Animal/growth \& development, Tibia/growth \& development}, isbn = {0171-967X (Print)0171-967X (Linking)}, author = {Biewener, A. A. and Swartz, S. M. and Bertram, J. E.} } @article {548201, title = {Bone strain: a determinant of gait and speed?}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {123}, year = {1986}, note = {Biewener, A ATaylor, C Reng3-3008-9512/PHS HHS/AM18140/AM/NIADDK NIH HHS/Comparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, P.H.S.ENGLAND1986/07/01J Exp Biol. 1986 Jul;123:383-400.}, month = {Jul}, pages = {383-400}, abstract = {Principal strains were recorded in vivo from the radial and tibial midshafts of three goats as they increased speed and changed gait. These data were compared with strain data measured for the radius and tibia of the dog (Rubin \& Lanyon, 1982) and the horse (Biewener, Thomason \& Lanyon, 1983b) in order to test the hypothesis that similar peak bone strains (stresses) occur at functionally equivalent points in the gaits of different species. Multiple recordings of in vivo strain along the caudal diaphyses of the radius and tibia of one goat were made to test the validity of this technique for measuring peak locomotor stress. Measured strains were extremely consistent over the animal{\textquoteright}s full range of speed (coefficient of variation for the radius 0.05-0.08, and for the tibia 0.06-0.11). The data from the three gauges, which were spaced 15 mm apart, demonstrated that maximal strains act at the midshaft, substantiating the use of this technique to measure peak locomotor bone strains. Strain levels recorded at the trot-gallop transition and top galloping speeds of the goat were similar to the values reported for the dog and horse, despite large differences in absolute speed (goat, 4.3 ms-1; dog, 6.9 ms-1; horse, 7.5 ms-1 at maximum gallop). The second moments of area of the tibia and radius (+ ulna) of the dog are 29\% and 113\% greater than for goats of equal size, explaining how similar strains are achieved in the dog at higher speeds than the goat. Furthermore, peak bone strains recorded at the fastest trotting speed were similar to those recorded at the fastest galloping speed for each species. Peak strains recorded for the goat at a maximum gallop correspond to stresses of +37.9 MPa (cranial) and -47.7 MPa (caudal) in the radius and +36.3 MPa (cranial) and -50.3 MPa (caudal) in the tibia, representing a safety factor to yield failure of three.}, keywords = {*Gait, *Locomotion, Animals, Biomechanical Phenomena, Goats/*physiology, Radius/*physiology, Stress, Mechanical, Tibia/*physiology}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A. and Taylor, C. R.} } @article {548191, title = {Regulation of respiratory airflow during panting and feeding in the dog}, journal = {Respir PhysiolRespir PhysiolRespir Physiol}, volume = {61}, number = {2}, year = {1985}, note = {Biewener, A ASoghikian, G WCrompton, A WengT32-GMO7117/GM/NIGMS NIH HHS/Research Support, U.S. Gov{\textquoteright}t, P.H.S.NETHERLANDS1985/08/01Respir Physiol. 1985 Aug;61(2):185-95.}, month = {Aug}, pages = {185-95}, abstract = {Cineradiographic study of the movement patterns of oropharyngeal and laryngeal structures during breathing and panting in dogs, correlated with recordings of expiratory and inspiratory airflow patterns (via thermocouples) at the nose and mouth show that the soft palate is the principal structural component regulating the path of respiratory in these animals. Cyclical movements of the soft palate during panting are accompanied by complementary movements of the posterior dorsum of the tongue (and epiglottis) to open and to close alternately the oropharynx and nasopharynx. The epiglottis appears to play a passive role during changes in airflow direction; its movements at this time being closely coupled to movements of the posterior tongue and hyoid. The dogs did not breathe during lapping or mastication, indicating the loss of functional separation of respiratory and feeding activities - a role traditionally held for the evolution of a secondary palate in mammals. Food stored in the posterior region of the oral cavity was observed to obstruct airflow via the nasopharynx during food transport and breakdown. Respiration commenced only after the food bolus had been swallowed. We suggest that specializations of the soft palate and epiglottis in dogs for thermal panting appear to restrict the formation of an adequate oropharyngeal seal during feeding.}, keywords = {*Pulmonary Ventilation, Animals, Cineradiography, Dogs, Epiglottis/physiology, Feeding Behavior/*physiology, Larynx/physiology, Nasopharynx/physiology, Oropharynx/physiology, Palate, Soft/physiology, Pharynx/physiology}, isbn = {0034-5687 (Print)0034-5687 (Linking)}, author = {Biewener, A. A. and Soghikian, G. W. and Crompton, A. W.} } @article {548061, title = {Bone and its functions: the mechanical adaptations of bones}, journal = {ScienceScienceScience}, volume = {227}, number = {4687}, year = {1985}, note = {Biewener, A AengNew York, N.Y.1985/02/08 00:00Science. 1985 Feb 8;227(4687):629-30.}, month = {Feb 8}, pages = {629-30}, isbn = {0036-8075 (Print)0036-8075 (Linking)}, author = {Biewener, A. A.} } @article {548206, title = {Bone stress in the horse forelimb during locomotion at different gaits: a comparison of two experimental methods}, journal = {J BiomechJ BiomechJ Biomech}, volume = {16}, number = {8}, year = {1983}, note = {Biewener, A AThomason, JGoodship, ALanyon, L EengAM18140/AM/NIADDK NIH HHS/T32GM07117-04/GM/NIGMS NIH HHS/Comparative StudyResearch Support, Non-U.S. Gov{\textquoteright}tResearch Support, U.S. Gov{\textquoteright}t, P.H.S.1983/01/01J Biomech. 1983;16(8):565-76.}, pages = {565-76}, abstract = {Longitudinal stresses acting in the cranial and caudal cortices of the radius and the dorsal and palmar cortices of the metacarpus in the horse were determined using two independent methods simultaneously. One approach involved the use of rosette strain gauges to record in vivo bone strain; the other involved filming the position of the horse{\textquoteright}s forelimb as it passed over a force plate. Agreement between the two analyses was better for the radius than for the metacarpus. Both methods showed the radius to be loaded primarily in sagittal bending, acting to place the caudal cortex in compression and the cranial cortex in tension. At each gait the magnitude of peak stress in each cortex based on the film/force analysis was 1.5-2 times higher than that determined from the bone strain recordings. In the metacarpus, the magnitude of stress in each cortex calculated from the film/force method was 2-3 times greater at each gait than that shown by the bone strain recordings. However, whereas the film/force analysis indicated that the metacarpus was loaded in sagittal bending (acting to place the palmar cortex in compression and the dorsal cortex in tension), the bone strain recordings showed the metacarpus to be loaded primarily in axial compression at each gait. Because the film/force method depends on an accurate measure of limb segment orientation relative to the direction of ground reaction force, comparatively small errors in calculations of bending moments may lead to a significant difference in the level and distribution of stress determined to act in the bone{\textquoteright}s cortices. The discrepancy in metacarpal loading obtained by the two methods may be explained in part by the simplicity of the biomechanical model which, for instance, neglected the force exerted by the sesamoids on the distal end of the metacarpus. The records of stress determined from the in vivo bone strain recordings showed that each bone was subjected to a consistent loading regime despite changes of gait. Such a consistent strain distribution should allow these bones to maximize economy in the use of tissue required to support the dynamic loads applied. Peak stresses measured from the bone strain recordings in the radius during locomotion at constant speed (-40.8 +/- 4.1 MN m-2) were significantly larger than those in the metacarpus (-25.1 +/- 2.8 MN m-2), regardless of speed and gait. During acceleration and deceleration, however, peak stress rose dramatically in the metacarpus (-40.6 +/- 3.4 MN m-2) but remained constant in the radius (-37.8 +/- 5.8 MN m-2).(ABSTRACT TRUNCATED AT 400 WORDS)}, keywords = {*Gait, *Locomotion, *Stress, Mechanical, Animals, Forelimb/anatomy \& histology, Horses/*physiology, Metacarpus/anatomy \& histology/*physiology, Methods, Radius/anatomy \& histology/*physiology}, isbn = {0021-9290 (Print)0021-9290 (Linking)}, author = {Biewener, A. A. and Thomason, J. and Goodship, A. and Lanyon, L. E.} } @article {548056, title = {Locomotory stresses in the limb bones of two small mammals: the ground squirrel and chipmunk}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {103}, year = {1983}, note = {Biewener, A AengT32GM07117/GM/NIGMS NIH HHS/Research Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.ENGLAND1983/03/01J Exp Biol. 1983 Mar;103:131-54.}, month = {Mar}, pages = {131-54}, abstract = {Peak stresses acting in limb bones should increase with increasing size if the forces acting on the bones increase in direct proportion to the animal{\textquoteright}s body weight. This is a direct consequence of the scaling of limb bone geometry over a wide range in size in mammals. In addition, recent work has shown that the material strength of bone is similar in large and small animals. If the assumptions in this analysis are correct, large animals would have a lower safety factor to failure than small animals. The purpose of this study was to measure peak stresses acting in the limb bones of small animals during locomotion and compare the results with similar measurements available for larger animals. Locomotory stresses acting in the fore and hindlimb bones of two rodents, the ground squirrel (Spermophilus tridecemlineatus) and chipmunk (Tamais striatus), were calculated using ground force recordings and measurements of limb position taken from high speed x-ray cine films. Peak (compressive) stresses calculated to act in the bones of these animals (-31 to -86 MN/m2) are similar in magnitude to those determined for much larger mammals. The more proximal bones of the fore and hindlimb, the humerus and femur, were found to develop stresses (-31 to -42 MN/m2) significantly lower than those acting in the more distal bones of each limb: the radius, ulna and tibia (-58 to -86 MN/m2). All of the long bones from both species, except their femora, were found to be loaded principally in bending. The caudal cortices of each bone developed a peak compressive stress, whereas the cranial cortices were loaded in tension. Various features of the musculo-skeletal organization and manner of locomotion of these rodents are considered to explain how animals of different size maintain a uniform safety factor to failure.}, keywords = {*Locomotion, Animals, Biophysical Phenomena, Biophysics, Body Weight, Bone and Bones/*physiology, Extremities/physiology, Sciuridae/*physiology, Stress, Mechanical}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A.} } @article {548051, title = {Allometry of quadrupedal locomotion: the scaling of duty factor, bone curvature and limb orientation to body size}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {105}, year = {1983}, note = {Biewener, A AengT32GM07117/GM/NIGMS NIH HHS/Comparative StudyResearch Support, U.S. Gov{\textquoteright}t, Non-P.H.S.Research Support, U.S. Gov{\textquoteright}t, P.H.S.ENGLAND1983/07/01J Exp Biol. 1983 Jul;105:147-71.}, month = {Jul}, pages = {147-71}, abstract = {Measurements of the chord length (alpha M0.31) and diameter (alpha M0.35) of the femora, tibiae, humeri and radii from 32 species of mammals, ranging in approximate body mass from 0.020-3500 kg, support previous data which show that mammalian long bones scale close to geometric similarity. Scaling of peak stresses based on these measurements of limb bone geometry predicts that peak stress increases alpha M0.28, assuming that the forces acting on a bone are directly proportional to an animal{\textquoteright}s weight. Peak locomotory stresses measured in small and large quadrupeds contradict this scaling prediction, however, showing that the magnitude of peak bone stress is similar over a range of size. Consequently, a uniform safety factor is maintained. Bone curvature (alpha M-0.09) and limb bone angle relative to the direction of ground force (alpha M-0.07) exhibit a slight, but significant, decrease with increasing body mass. Duty factor measured at the animal{\textquoteright}s trot--gallop transition speed does not change significantly with body size. The moment arm ratio of ground force to muscular force exerted about a joint was found to decrease dramatically for horses as compared to ground squirrels and chipmunks. This six-fold decrease (alpha M-0.23) provides preliminary data which appear to explain, along with the decrease in bone curvature and angle, the similar magnitudes of peak bone stress developed during locomotion in different sized animals. The crouched posture adopted by small quadrupeds while running may allow greater changes in momentum (when accelerating or decelerating) or a decrease in the forces exerted on their limbs.}, keywords = {*Locomotion, Animals, Biomechanical Phenomena, Bone and Bones/*anatomy \& histology, Mammals/*anatomy \& histology, Muscles/anatomy \& histology, Posture, Species Specificity}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A.} } @article {548046, title = {Bone strength in small mammals and bipedal birds: do safety factors change with body size?}, journal = {J Exp BiolJ Exp BiolJ Exp Biol}, volume = {98}, year = {1982}, note = {Biewener, A AengAM18140/AM/NIADDK NIH HHS/T32GM07117/GM/NIGMS NIH HHS/Comparative StudyResearch Support, U.S. Gov{\textquoteright}t, P.H.S.ENGLAND1982/06/01J Exp Biol. 1982 Jun;98:289-301.}, month = {Jun}, pages = {289-301}, abstract = {Measurements of the cross-sectional geometry and length of bones from animals of different sizes suggest that peak locomotory stresses might be as much as nine times greater in the limb bones of a 300 kg horse than those of a 0.10 kg chipmunk. To determine if the bones of larger animals are stronger than those of small animals, the bending strength of whole bone specimens from the limbs of small mammals and bipedal birds was measured and compared with published data for large mammalian cortical bone (horses and bovids). No significant difference (P greater than 0.2) was found in the failure stress of bone over a range in size from 0.05-700 kg (233 +/- 53 MN/m2 for small animals compared to 200 +/- 28 MN/m2 for large animals). This finding suggests that either the limb bones of small animals are much stronger than they need to be, or that other aspects of locomotion (e.g. duty factor and limb orientation relative to the direction of the ground force) act to decrease peak locomotory stresses in larger animals.}, keywords = {Animals, Body Weight, Bone and Bones/*physiology, locomotion, Stress, Mechanical}, isbn = {0022-0949 (Print)0022-0949 (Linking)}, author = {Biewener, A. A.} }