Muscle force-length dynamics during walking over obstacles indicates delayed recovery and a shift towards more 'strut-like' function in birds with proprioceptive deficit.

Recent studies of in vivo muscle function in guinea fowl revealed that distal leg muscles rapidly modulate force and work to stabilize running in uneven terrain. Previous studies focused on running only, and it remains unclear how muscular mechanisms for stability differ between walking and running. Here, we investigated in vivo function of the lateral gastrocnemius (LG) during walking over obstacles. We compared muscle function in birds with intact (iLG) versus self-reinnervated LG (rLG). Self-reinnervation results in proprioceptive feedback deficit due to loss of monosynaptic stretch reflex. We tested the hypothesis that proprioceptive deficit results in decreased modulation of EMG activity in response to obstacle contact, and a delayed obstacle recovery compared with that for iLG. We found that total myoelectric intensity (Etot) of iLG increased by 68% in obstacle strides (S 0) compared with level terrain, suggesting a substantial reflex-mediated response. In contrast, Etot of rLG increased by 31% in S 0 strides compared with level walking, but also increased by 43% in the first post-obstacle (S +1) stride. In iLG, muscle force and work differed significantly from level walking only in the S 0 stride, indicating a single-stride recovery. In rLG, force increased in S 0, S +1 and S +2 compared with level walking, indicating three-stride obstacle recovery. Interestingly, rLG showed little variation in work output and shortening velocity in obstacle terrain, indicating a shift towards near-isometric strut-like function. Reinnervated birds also adopted a more crouched posture across level and obstacle terrains compared with intact birds. These findings suggest gait-specific control mechanisms in walking and running.

Biomechanics of avian flight.

Throughout recorded human history, birds have fascinated and inspired humans to dream of flying. The Greek myth of Daedalus and his son Icarus, who flew too close to the sun and fell to his death, first written by Diodorus (60-30 B.C.E.) and later poetically revised by Ovid (8 C.E.), evokes the dangers of hubris. Many indigenous peoples invoke spiritual qualities and protection ascribed to birds that were symbols of freedom and viewed as sacred messengers of the gods. As a student of bird flight, Leonardo da Vinci (1452-1519) was the first to document dynamic soaring by birds. And, subsequently, the flight of birds inspired human engineered pursuit of powered aircraft design, with the Wright Brothers being the first to design and achieve sustained flight at Kitty Hawk, NC, USA in 1903.

White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals.

Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g. basal, resting, field, maximally-active). The scaling of metabolism is usually highly correlated with the scaling of many life history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to a) lower contents of expensive tissues (brains, liver, kidneys), and b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. A additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include: 1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries, 2) studies linking scaling to ecological or phylogenetic context, 3) studies that consider multiple, possibly interacting hypotheses, and 4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate and reproduction.

Physiology: Woodpecker skulls are not shock absorbers.

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.

Effect of muscle stimulation intensity on the heterogeneous function of regions within an architecturally complex muscle.

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 ± 0.8 mm versus 10.9 ± 0.7 mm) fibers and steeper (28.7 ± 11.0° versus 19.6 ± 6.3°) fiber angles at optimum length, and operates over a larger (17.9 ± 3.8% versus 12.6 ± 2.7%) range of its force-length curve. The proximal region also exhibits larger changes in pennation angle (5.6 ± 2.2°/mm versus 2.4 ± 1.5°/mm muscle shortening) and architectural gearing (1.82 ± 0.53 versus 1.25 ± 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.

Task-dependent recruitment across ankle extensor muscles and between mechanical demands is driven by the metabolic cost of muscle contraction.

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-the slower but stronger ankle plantarflexor-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.

Lower-limb muscle function is influenced by changing mechanical demands in cycling.

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-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.

Added mass in rat plantaris muscle causes a reduction in mechanical work.

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.

Aquatic and terrestrial takeoffs require different hindlimb kinematics and muscle function in mallard ducks.

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.

Functional morphology of the ankle extensor muscle-tendon units in the springhare Pedetes capensis shows convergent evolution with macropods for bipedal hopping locomotion.

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'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.

Tuning of feedforward control enables stable muscle force-length dynamics after loss of autogenic proprioceptive feedback.

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.

Post-activation muscle potentiation and its relevance to cyclical behaviours.

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' 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.

Skeletal Muscle Shape Change in Relation to Varying Force Requirements Across Locomotor Conditions.

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 (0.5-0.8 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-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 (r 2 = 0.86; p = 0.001); whereas, the change in muscle width (width strain) increases (r 2 = 0.88; p = 0.001) and tendon strain increases (r 2 = 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.

Broad similarities in shoulder muscle architecture and organization across two amniotes: implications for reconstructing non-mammalian synapsids.

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 "sprawling" to "erect" 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-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 pascuali.

Modulation of Flight Muscle Recruitment and Wing Rotation Enables Hummingbirds to Mitigate Aerial Roll Perturbations.

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 most maneuverable around the roll axis, yet our knowledge of roll control in biological fliers remains limited. 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 wind conditions. We challenged hummingbirds to fly within a steady, longitudinally (streamwise) oriented vortex that imposed a continuous roll perturbation, measured wing kinematics and neuromotor activation of the flight muscles with synchronized high-speed video and electromyography and used computational fluid dynamics (CFD) to estimate the aerodynamic forces generated by observed wing motions. Hummingbirds responded to the perturbation with bilateral differences in activation of the main flight muscles while maintaining symmetry in most major aspects of wing motion, including stroke amplitude, stroke plane angle, and flapping frequency. Hummingbirds did display consistent bilateral differences in subtler wing kinematic traits, including wing rotation and elevation. CFD modeling revealed that asymmetric wing rotation was critical for attenuating the effects of the perturbation. The birds also augmented 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, as well as bio-inspiration for simple yet effective control strategies that could allow robotic fliers to contend with unfamiliar and challenging real-world aerial conditions.

In vivo force-length and activation dynamics of two distal rat hindlimb muscles in relation to gait and grade.

Muscle function changes to meet the varying mechanical demands of locomotion across different gait and grade conditions. A muscle'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-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-length behavior and neuromuscular activation data reported here can be used to validate improved two-element Hill-type muscle models.

The Evolution of a Single Toe in Horses: Causes, Consequences, and the Way Forward.

Horses are a classic example of macroevolution in three major traits-large body size, tall-crowned teeth (hypsodonty), and a single toe (monodactyly)-but how and why monodactyly evolved is still poorly understood. Existing hypotheses usually connect digit reduction in horses to the spread and eventual dominance of open-habitat grasslands, which took over from forests during the Cenozoic; digit reduction has been argued to be an adaptation for speed, locomotor economy, stability, and/or increased body size. In this review, we assess the evidence for these (not necessarily mutually exclusive) hypotheses from a variety of related fields, including paleoecology, phylogenetic comparative methods, and biomechanics. Convergent evolution of digit reduction, including in litopterns and artiodactyls, is also considered. We find it unlikely that a single evolutionary driver was responsible for the evolution of monodactyly, because changes in body size, foot posture, habitat, and substrate are frequently found to influence one another (and to connect to broader potential drivers, such as changing climate). We conclude with suggestions for future research to help untangle the complex dynamics of this remarkable morphological change in extinct horses. A path forward should combine regional paleoecology studies, quantitative biomechanical work, and make use of convergence and modern analogs to estimate the relative contributions of potential evolutionary drivers for digit reduction.