Publications

2011
Higham TE, Biewener AA. Functional and architectural complexity within and between muscles: regional variation and intermuscular force transmission. Philos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol Sci. 2011;366 :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.
Higham TE, Biewener AA, Delp SL. Mechanics, modulation and modelling: how muscles actuate and control movement. Philos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol Sci. 2011;366 :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.
Daley MA, Biewener AA. Leg muscles that mediate stability: mechanics and control of two distal extensor muscles during obstacle negotiation in the guinea fowl. Philos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol Sci. 2011;366 :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.
Biewener AA. Muscle function in avian flight: achieving power and control. Philos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol SciPhilos Trans R Soc Lond B Biol Sci. 2011;366 :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'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' work requirements. Muscles also produce substantial power during swimming, but this is mainly to overcome body drag rather than to support the animal'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.
Arnold AS, Richards CT, Ros IG, Biewener AA. There is always a trade-off between speed and force in a lever system: comment on McHenry (2010). Biol LettBiol LettBiol Lett. 2011;7 :878-9; discussion 880-1.
2010
Tobalske BW, Biewener AA, Warrick DR, Hedrick TL, Powers DR. Effects of flight speed upon muscle activity in hummingbirds. J Exp BiolJ Exp BiolJ Exp Biol. 2010;213 :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.
Lentink D, Biewener AA. Nature-inspired flight--beyond the leap. Bioinspir BiomimBioinspir BiomimBioinspir Biomim. 2010;5 :040201.
Berg AM, Biewener AA. Wing and body kinematics of takeoff and landing flight in the pigeon (Columba livia). J Exp BiolJ Exp BiolJ Exp Biol. 2010;213 :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.
2009
McGuigan MP, Yoo E, Lee DV, Biewener AA. Dynamics of goat distal hind limb muscle-tendon function in response to locomotor grade. J Exp BiolJ Exp BiolJ Exp Biol. 2009;212 :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.
Higham TE, Biewener AA. Fatigue alters in vivo function within and between limb muscles during locomotion. Proc Biol SciProc Biol SciProc Biol Sci. 2009;276 :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' 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.
Daley MA, Voloshina A, Biewener AA. The role of intrinsic muscle mechanics in the neuromuscular control of stable running in the guinea fowl. J PhysiolJ PhysiolJ Physiol. 2009;587 :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'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.
Carroll AM, Biewener AA. Mono- versus biarticular muscle function in relation to speed and gait changes: in vivo analysis of the goat triceps brachii. J Exp BiolJ Exp BiolJ Exp Biol. 2009;212 :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).
2008
Tobalske BW, Biewener AA. Contractile properties of the pigeon supracoracoideus during different modes of flight. J Exp BiolJ Exp BiolJ Exp Biol. 2008;211 :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.
McGowan CP, Skinner J, Biewener AA. Hind limb scaling of kangaroos and wallabies (superfamily Macropodoidea): implications for hopping performance, safety factor and elastic savings. J AnatJ AnatJ Anat. 2008;212 :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.
Moreno CA, Main RP, Biewener AA. Variability in forelimb bone strains during non-steady locomotor activities in goats. J Exp BiolJ Exp BiolJ Exp Biol. 2008;211 :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.
McGowan CP, Baudinette RV, Biewener AA. Differential design for hopping in two species of wallabies. Comp Biochem Physiol A Mol Integr PhysiolComp Biochem Physiol A Mol Integr PhysiolComp Biochem Physiol A Mol Integr Physiol. 2008;150 :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' 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.
Lee DV, McGuigan MP, Yoo EH, Biewener AA. Compliance, actuation, and work characteristics of the goat foreleg and hindleg during level, uphill, and downhill running. J Appl Physiol (1985)J Appl Physiol (1985)J Appl Physiol (1985). 2008;104 :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.
Higham TE, Biewener AA, Wakeling JM. Functional diversification within and between muscle synergists during locomotion. Biol LettBiol LettBiol Lett. 2008;4 :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.
Higham TE, Biewener AA. Integration within and between muscles during terrestrial locomotion: effects of incline and speed. J Exp BiolJ Exp BiolJ Exp Biol. 2008;211 :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.
Carroll AM, Lee DV, Biewener AA. Differential muscle function between muscle synergists: long and lateral heads of the triceps in jumping and landing goats (Capra hircus). J Appl Physiol (1985)J Appl Physiol (1985)J Appl Physiol (1985). 2008;105 :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.

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