Publications

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.

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's flight trajectory. Subsequently, the pigeon mainly reacquired the body orientation used in forward flight without affecting its flight trajectory. Surprisingly, the pigeon'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.

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.

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'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'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'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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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).

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.

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.