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Most birds can navigate seamlessly between aerial and terrestrial environments. Whereas the forelimbs evolved into wings primarily for flight, the hindlimbs serve diverse functions such as walking, hopping and leaping, and jumping take-off for transitions into flight 1 . These capabilities have inspired engineers to aim for similar multimodality in aerial robots, expanding their range of applications across diverse environments. However, challenges remain in reproducing multimodal locomotion, across gaits with distinct kinematics and propulsive characteristics, such as walking and jumping, while preserving lightweight mass for flight. This trade-off between mechanical complexity and versatility 2 limits most existing aerial robots to only one additional locomotor mode 3-5 . Here we overcome the complexity-versatility trade-off with RAVEN (Robotic Avian-inspired Vehicle for multiple ENvironments), which uses its bird-inspired multifunctional legs to jump rapidly into flight, walk on the ground, and hop over obstacles and gaps similar to the multimodal locomotion of birds. We show that jumping for take-off contributes substantially to the initial flight take-off speed 6-9 and, remarkably, that it is more energy efficient than taking off without the jump. Our analysis suggests an important trade-off in mass distribution between legs and body among birds adapted for different locomotor strategies, with greater investment in leg mass among terrestrial birds with multimodal gait demands. Multifunctional robot legs expand the opportunities to deploy traditional fixed-wing aircraft in complex terrains through autonomous take-offs and multimodal gaits., Competing Interests: Competing interests: The authors declare no competing interests., (© 2024. The Author(s), under exclusive licence to Springer Nature Limited.)

Traditional work loop studies, that use sinusoidal length trajectories with constant frequencies, lack the complexities of in vivo muscle mechanics observed in modern studies. This study refines methodology of the 'avatar' method (a modified work loop) to infer in vivo muscle mechanics using ex vivo experiments with mouse extensor digitorum longus (EDL) muscles. The 'avatar' method involves using EDL muscles to replicate in vivo time-varying force, as demonstrated by previous studies focusing on guinea fowl lateral gastrocnemius (LG). The present study extends this method by using in vivo length trajectories and electromyographic activity from rat medial gastrocnemius (MG) during various gaits on a treadmill. Methodological enhancements from previous work, including adjusted stimulation protocols and systematic variation of starting length, improved predictions of in vivo time-varying force production (R2=0.80-0.96). The study confirms there is a significant influence of length, stimulation and their interaction on work loop variables (peak force, length at peak force, highest and average shortening velocity, and maximum and minimum active velocity), highlighting the importance of these interactions when muscles produce in vivo forces. We also investigated the limitations of traditional work loops in capturing muscle dynamics in legged locomotion (R2=0.01-0.71). While in vivo length trajectories enhanced force prediction, accurately predicting work per cycle remained challenging. Overall, the study emphasizes the utility of the 'avatar' method in elucidating dynamic muscle mechanics and highlights areas for further investigation to refine its application in understanding in vivo muscle function., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2024. Published by The Company of Biologists Ltd.)

The isometric force-length (F-L) and isotonic force-velocity (F-V) relationships characterize the contractile properties of skeletal muscle under controlled conditions, yet it remains unclear how these properties relate to in vivo muscle function. Here, we map the in situ F-L and F-V characteristics of guinea fowl (Numida meleagris) lateral gastrocnemius (LG) to the in vivo operating range during walking and running. We test the hypothesis that muscle fascicles operate on the F-L plateau, near the optimal length for force (L0) and near velocities that maximize power output (Vopt) during walking and running. We found that in vivo LG velocities are consistent with optimizing power during work production, and economy of force at higher loads. However, LG does not operate near L0 at higher loads. LG length was near L0 at the time of electromyography (EMG) onset but shortened rapidly such that force development during stance occurred on the ascending limb of the F-L curve, around 0.8L0. Shortening across L0 in late swing might optimize potential for rapid force development near the swing-stance transition, providing resistance to unexpected perturbations that require rapid force development. We also found evidence of in vivo passive force rise in late swing, without EMG activity, at lengths where in situ passive force is zero, suggesting that dynamic viscoelastic effects contribute to in vivo force development. Comparison of in vivo operating ranges with F-L and F-V properties suggests the need for new approaches to characterize muscle properties in controlled conditions that more closely resemble in vivo dynamics., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2024. Published by The Company of Biologists Ltd.)

Objective assessment of activity via accelerometry can provide valuable insights into dog health and welfare. Common activity metrics involve using acceleration cut-points to group data into intensity categories and reporting the time spent in each category. Lack of consistency and transparency in cut-point derivation makes it difficult to compare findings between studies. We present an alternative metric for use in dogs: the acceleration threshold (as a fraction of standard gravity, 1 g = 9.81 m/s 2 ) above which the animal's X most active minutes are accumulated (MX ACC ) over a 24-hour period. We report M2 ACC, M30 ACC and M60 ACC data from a colony of healthy beagles ( n = 6) aged 3-13 months. To ensure that reference values are applicable across a wider dog population, we incorporated labelled data from beagles and volunteer pet dogs ( n = 16) of a variety of ages and breeds. The dogs' normal activity patterns were recorded at 200 Hz for 24 hours using collar-based Axivity-AX3 accelerometers. We calculated acceleration vector magnitude and MX ACC metrics. Using labelled data from both beagles and pet dogs, we characterize the range of acceleration outputs exhibited enabling meaningful interpretation of MX ACC . These metrics will help standardize measurement of canine activity and serve as outcome measures for veterinary and translational research., Competing Interests: We have no competing interests., (© 2024 The Authors.)

Biological springs can be used in nature for energy conservation and ultra-fast motion. The loading and unloading rates of elastic materials can play an important role in determining how the properties of these springs affect movements. We investigate the mechanical energy efficiency of biological springs (American bullfrog plantaris tendons and guinea fowl lateral gastrocnemius tendons) and synthetic elastomers. We measure these materials under symmetric rates (equal loading and unloading durations) and asymmetric rates (unequal loading and unloading durations) using novel dynamic mechanical analysis measurements. We find that mechanical efficiency is highest at symmetric rates and significantly decreases with a larger degree of asymmetry. A generalized one-dimensional Maxwell model with no fitting parameters captures the experimental results based on the independently characterized linear viscoelastic properties of the materials. The model further shows that a broader viscoelastic relaxation spectrum enhances the effect of rate-asymmetry on efficiency. Overall, our study provides valuable insights into the interplay between material properties and unloading dynamics in both biological and synthetic elastic systems.

To celebrate its centenary year, Journal of Experimental Biology (JEB) commissioned a collection of articles examining the past, present and future of experimental biology. This Commentary closes the collection by considering the important research opportunities and challenges that await us in the future. We expect that researchers will harness the power of technological advances, such as '-omics' and gene editing, to probe resistance and resilience to environmental change as well as other organismal responses. The capacity to handle large data sets will allow high-resolution data to be collected for individual animals and to understand population, species and community responses. The availability of large data sets will also place greater emphasis on approaches such as modeling and simulations. Finally, the increasing sophistication of biologgers will allow more comprehensive data to be collected for individual animals in the wild. Collectively, these approaches will provide an unprecedented understanding of 'how animals work' as well as keys to safeguarding animals at a time when anthropogenic activities are degrading the natural environment., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

Force-length (F-L) and force-velocity (F-V) properties characterize skeletal muscle's intrinsic properties under controlled conditions, and it is thought that these properties can inform and predict in vivo muscle function. Here, we map dynamic in vivo operating range and mechanical function during walking and running, to the measured in situ F-L and F-V characteristics of guinea fowl ( Numida meleagris ) lateral gastrocnemius (LG), a primary ankle extensor. We use in vivo patterns of muscle tendon force, fascicle length, and activation to test the hypothesis that muscle fascicles operate at optimal lengths and velocities to maximize force or power production during walking and running. Our findings only partly support our hypothesis: in vivo LG velocities are consistent with optimizing power during work production, and economy of force at higher loads. However, LG does not operate at lengths on the force plateau (±5% Fmax) during force production. LG length was near L 0 at the time of EMG onset but shortened rapidly such that force development during stance occurred almost entirely on the ascending limb of the F-L curve, at shorter than optimal lengths. These data suggest that muscle fascicles shorten across optimal lengths in late swing, to optimize the potential for rapid force development near the swing-stance transition. This may provide resistance against unexpected perturbations that require rapid force development at foot contact. We also found evidence of passive force rise (in absence of EMG activity) in late swing, at lengths where passive force is zero in situ , suggesting that dynamic history dependent and viscoelastic effects may contribute to in vivo force development. Direct comparison of in vivo work loops and physiological operating ranges to traditional measures of F-L and F-V properties suggests the need for new approaches to characterize dynamic muscle properties in controlled conditions that more closely resemble in vivo dynamics.

Animal locomotion is the result of complex and multi-layered interactions between the nervous system, the musculo-skeletal system and the environment. Decoding the underlying mechanisms requires an integrative approach. Comparative experimental biology has allowed researchers to study the underlying components and some of their interactions across diverse animals. These studies have shown that locomotor neural circuits are distributed in the spinal cord, the midbrain and higher brain regions in vertebrates. The spinal cord plays a key role in locomotor control because it contains central pattern generators (CPGs) - systems of coupled neuronal oscillators that provide coordinated rhythmic control of muscle activation that can be viewed as feedforward controllers - and multiple reflex loops that provide feedback mechanisms. These circuits are activated and modulated by descending pathways from the brain. The relative contributions of CPGs, feedback loops and descending modulation, and how these vary between species and locomotor conditions, remain poorly understood. Robots and neuromechanical simulations can complement experimental approaches by testing specific hypotheses and performing what-if scenarios. This Review will give an overview of key knowledge gained from comparative vertebrate experiments, and insights obtained from neuromechanical simulations and robotic approaches. We suggest that the roles of CPGs, feedback loops and descending modulation vary among animals depending on body size, intrinsic mechanical stability, time required to reach locomotor maturity and speed effects. We also hypothesize that distal joints rely more on feedback control compared with proximal joints. Finally, we highlight important opportunities to address fundamental biological questions through continued collaboration between experimentalists and engineers., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

The work loop technique has provided key insights into in vivo muscle work and power during steady locomotion. However, for many animals and muscles, ex vivo experiments are not feasible. In addition, purely sinusoidal strain trajectories lack variations in strain rate that result from variable loading during locomotion. Therefore, it is useful to develop an 'avatar' approach in which in vivo strain and activation patterns from one muscle are replicated in ex vivo experiments on a readily available muscle from an established animal model. In the present study, we used mouse extensor digitorum longus (EDL) muscles in ex vivo experiments to investigate in vivo mechanics of the guinea fowl lateral gastrocnemius (LG) muscle during unsteady running on a treadmill with obstacle perturbations. In vivo strain trajectories from strides down from obstacle to treadmill, up from treadmill to obstacle, strides with no obstacle and sinusoidal strain trajectories at the same amplitude and frequency were used as inputs in work loop experiments. As expected, EDL forces produced with in vivo strain trajectories were more similar to in vivo LG forces (R2=0.58-0.94) than were forces produced with the sinusoidal trajectory (average R2=0.045). Given the same stimulation, in vivo strain trajectories produced work loops that showed a shift in function from more positive work during strides up from treadmill to obstacle to less positive work in strides down from obstacle to treadmill. Stimulation, strain trajectory and their interaction had significant effects on all work loop variables, with the interaction having the largest effect on peak force and work per cycle. These results support the theory that muscle is an active material whose viscoelastic properties are tuned by activation, and which produces forces in response to deformations of length associated with time-varying loads., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

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., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

Introduction: Cesarean section deliveries in the U.S. increased from 5% of births in 1970 to 32% in 2020. Little is known about trends in cesarean sections and inductions in low-risk pregnancies (i.e., those for which interventions would not be medically necessary). This study addresses the following questions: (1) what is the prevalence of elective deliveries at the population level?, (2) how has that changed over time?, and (3) to what extent do the rates of elective deliveries vary across the population?, Methods: We first documented long-term trends in cesarean sections in the U.S., California, and New Jersey. We then used linked birth and hospital discharge records and an algorithm based on Joint Commission guidelines to identify low-risk pregnancies and document trends in cesarean sections and inductions in low-risk pregnancies in California and New Jersey over a recent 2-decade period, overall and by maternal characteristics and gestational age., Results: In low-risk pregnancies in California and New Jersey, rates of cesarean sections and inductions increased sharply from the early 1990s through the mid-2000s, peaked at 33% in California and 41% in New Jersey in 2007, and then declined somewhat, and the proportions of inductions that were followed by cesarean sections increased from fewer than 1 in 5 to about 1 in 4. More education, non-Hispanic White race/ethnicity, U.S.-born status, and non-Medicaid were associated with higher rates of interventions. Trends were similar across all socioeconomic groups, but differences have been narrowing in California. Among early-term (gestational age of 37-38 weeks) births in low-risk pregnancies, the rates of elective deliveries increased substantially in both states until the mid/late-2000s, peaked at about 35% in California and over 40% in New Jersey, and then decreased in both states to about 20%., Conclusions: Given established health risks of nonmedically necessary cesarean sections, that a nontrivial share of induced deliveries in low-risk pregnancies result in cesarean sections, and that interventions in low-risk pregnancies have not substantially declined since their peak in the mid-2000s, the trends documented in this paper suggest that sustained, even increased, public health attention is needed to address the still-too-high rates of cesarean sections and inductions in the U.S., (© 2022 The Author(s).)

Navigating complex terrains requires dynamic interactions between the substrate, musculoskeletal and sensorimotor systems. Current perturbation studies have mostly used visible terrain height perturbations, which do not allow us to distinguish among the neuromechanical contributions of feedforward control, feedback-mediated and mechanical perturbation responses. Here, we use treadmill belt speed perturbations to induce a targeted perturbation to foot speed only, and without terrain-induced changes in joint posture and leg loading at stance onset. Based on previous studies suggesting a proximo-distal gradient in neuromechanical control, we hypothesized that distal joints would exhibit larger changes in joint kinematics, compared to proximal joints. Additionally, we expected birds to use feedforward strategies to increase the intrinsic stability of gait. To test these hypotheses, seven adult guinea fowl were video recorded while walking on a motorized treadmill, during both steady and perturbed trials. Perturbations consisted of repeated exposures to a deceleration and acceleration of the treadmill belt speed. Surprisingly, we found that joint angular trajectories and center of mass fluctuations remain very similar, despite substantial perturbation of foot velocity by the treadmill belt. Hip joint angular trajectories exhibit the largest changes, with the birds adopting a slightly more flexed position across all perturbed strides. Additionally, we observed increased stride duration across all strides, consistent with feedforward changes in the control strategy. The speed perturbations mainly influenced the timing of stance and swing, with the largest kinematic changes in the strides directly following a deceleration. Our findings do not support the general hypothesis of a proximo-distal gradient in joint control, as distal joint kinematics remain largely unchanged. Instead, we find that leg angular trajectory and the timing of stance and swing are most sensitive to this specific perturbation, and leg length actuation remains largely unchanged. Our results are consistent with modular task-level control of leg length and leg angle actuation, with different neuromechanical control and perturbation sensitivity in each actuation mode. Distal joints appear to be sensitive to changes in vertical loading but not foot fore-aft velocity. Future directions should include in vivo studies of muscle activation and force-length dynamics to provide more direct evidence of the sensorimotor control strategies for stability in response to belt speed perturbations., (© The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

Designers of legged robots are challenged with creating mechanisms that allow energy-efficient locomotion with robust and minimalistic control. Sources of high energy costs in legged robots include the rapid loading and high forces required to support the robot's mass during stance and the rapid cycling of the leg's state between stance and swing phases. Here, we demonstrate an avian-inspired robot leg design, BirdBot, that challenges the reliance on rapid feedback control for joint coordination and replaces active control with intrinsic, mechanical coupling, reminiscent of a self-engaging and disengaging clutch. A spring tendon network rapidly switches the leg's slack segments into a loadable state at touchdown, distributes load among joints, enables rapid disengagement at toe-off through elastically stored energy, and coordinates swing leg flexion. A bistable joint mediates the spring tendon network's disengagement at the end of stance, powered by stance phase leg angle progression. We show reduced knee-flexing torque to a 10th of what is required for a nonclutching, parallel-elastic leg design with the same kinematics, whereas spring-based compliance extends the leg in stance phase. These mechanisms enable bipedal locomotion with four robot actuators under feedforward control, with high energy efficiency. The robot offers a physical model demonstration of an avian-inspired, multiarticular elastic coupling mechanism that can achieve self-stable, robust, and economic legged locomotion with simple control and no sensory feedback. The proposed design is scalable, allowing the design of large legged robots. BirdBot demonstrates a mechanism for self-engaging and disengaging parallel elastic legs that are contact-triggered by the foot's own lever-arm action.

Peripheral and intraspinal feedback is required to shape and update the output of spinal networks that execute motor behavior. We report that lumbar dI2 spinal interneurons in chicks receive synaptic input from afferents and premotor neurons. These interneurons innervate contralateral premotor networks in the lumbar and brachial spinal cord, and their ascending projections innervate the cerebellum. These findings suggest that dI2 neurons function as interneurons in local lumbar circuits, are involved in lumbo-brachial coupling, and that part of them deliver peripheral and intraspinal feedback to the cerebellum. Silencing of dI2 neurons leads to destabilized stepping in posthatching day 8 hatchlings, with occasional collapses, variable step profiles, and a wide-base walking gait, suggesting that dI2 neurons may contribute to the stabilization of the bipedal gait., Competing Interests: BH, YH, NB, AK, MD, YC, AL, AK none, (© 2021, Haimson et al.)

Archosaurian reptiles (including living crocodiles and birds) had an explosive diversification of locomotor form and function since the Triassic approximately 250 million years ago. Their limb muscle physiology and biomechanics are pivotal to our understanding of how their diversity and evolution relate to locomotor function. Muscle contraction velocity, force, and power in extinct archosaurs such as early crocodiles, pterosaurs, or non-avian dinosaurs are not available from fossil material, but are needed for biomechanical modeling and simulation. However, an approximation or range of potential parameter values can be obtained by studying extant representatives of the archosaur lineage. Here, we study the physiological performance of three appendicular muscles in Nile crocodiles ( Crocodylus niloticus ). Nile crocodile musculature showed high power and velocity values-the flexor tibialis internus 4 muscle, a small "hamstring" hip extensor, and knee flexor actively used for terrestrial locomotion, performed particularly well. Our findings demonstrate some physiological differences between muscles, potentially relating to differences in locomotor function, and muscle fiber type composition. By considering these new data from a previously unstudied archosaurian species in light of existing data (e.g., from birds), we can now better bracket estimates of muscle parameters for extinct species and related extant species. Nonetheless, it will be important to consider the potential specialization and physiological variation among muscles, because some archosaurian muscles (such as those with terrestrial locomotor function) may well have close to double the muscle power and contraction velocity capacities of others., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

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., Competing Interests: JG, NH, AB, MD No competing interests declared, (© 2020, Gordon et al.)

Electromyography (EMG) is used to understand muscle activity patterns in animals. Understanding how much variation exists in muscle activity patterns in homologous muscles across animal clades during similar behaviours is important for evaluating the evolution of muscle functions and neuromuscular control. We compared muscle activity across a range of archosaurian species and appendicular muscles, including how these EMG patterns varied across ontogeny and phylogeny, to reconstruct the evolutionary history of archosaurian muscle activation during locomotion. EMG electrodes were implanted into the muscles of turkeys, pheasants, quail, guineafowl, emus (three age classes), tinamous and juvenile Nile crocodiles across 13 different appendicular muscles. Subjects walked and ran at a range of speeds both overground and on treadmills during EMG recordings. Anatomically similar muscles such as the lateral gastrocnemius exhibited similar EMG patterns at similar relative speeds across all birds. In the crocodiles, the EMG signals closely matched previously published data for alligators. The timing of lateral gastrocnemius activation was relatively later within a stride cycle for crocodiles compared to birds. This difference may relate to the coordinated knee extension and ankle plantarflexion timing across the swing-stance transition in Crocodylia, unlike in birds where there is knee flexion and ankle dorsiflexion across swing-stance. No significant effects were found across the species for ontogeny, or between treadmill and overground locomotion. Our findings strengthen the inference that some muscle EMG patterns remained conservative throughout Archosauria: for example, digital flexors retained similar stance phase activity and M. pectoralis remained an 'anti-gravity' muscle. However, some avian hindlimb muscles evolved divergent activations in tandem with functional changes such as bipedalism and more crouched postures, especially M. iliotrochantericus caudalis switching from swing to stance phase activity and M. iliofibularis adding a novel stance phase burst of activity., (© 2019 Wiley Periodicals, Inc.)

Birds are a diverse and agile lineage of vertebrates that all use bipedal locomotion for at least part of their life. Thus birds provide a valuable opportunity to investigate how biomechanics and sensorimotor control are integrated for agile bipedal locomotion. This review summarizes recent work using terrain perturbations to reveal neuromechanical control strategies used by ground birds to achieve robust, stable, and agile running. Early experiments in running guinea fowl aimed to reveal the immediate intrinsic mechanical response to an unexpected drop ("pothole") in terrain. When navigating the pothole, guinea fowl experience large changes in leg posture in the perturbed step, which correlates strongly with leg loading and perturbation recovery. Analysis of simple theoretical models of running has further confirmed the crucial role of swing-leg trajectory control for regulating foot contact timing and leg loading in uneven terrain. Coupling between body and leg dynamics results in an inherent trade-off in swing leg retraction rate for fall avoidance versus injury avoidance. Fast leg retraction minimizes injury risk, but slow leg retraction minimizes fall risk. Subsequent experiments have investigated how birds optimize their control strategies depending on the type of perturbation (pothole, step, obstacle), visibility of terrain, and with ample practice negotiating terrain features. Birds use several control strategies consistently across terrain contexts: (1) independent control of leg angular cycling and leg length actuation, which facilitates dynamic stability through simple control mechanisms, (2) feedforward regulation of leg cycling rate, which tunes foot-contact timing to maintain consistent leg loading in uneven terrain (minimizing fall and injury risks), (3) load-dependent muscle actuation, which rapidly adjusts stance push-off and stabilizes body mechanical energy, and (4) multi-step recovery strategies that allow body dynamics to transiently vary while tightly regulating leg loading to minimize risks of fall and injury. In future work, it will be interesting to investigate the learning and adaptation processes that allow animals to adjust neuromechanical control mechanisms over short and long timescales.

Birds provide an interesting opportunity to study the relationships between body size, limb morphology and bipedal locomotor function. Birds are ecologically diverse and span a large range of body size and limb proportions, yet all use their hindlimbs for bipedal terrestrial locomotion, for at least some part of their life history. Here, we review the scaling of avian striding bipedal gaits to explore how body mass and leg morphology influence walking and running. We collate literature data from 21 species, spanning a 2500× range in body mass from painted quail to ostriches. Using dynamic similarity theory to interpret scaling trends, we find evidence for independent effects of body mass, leg length and leg posture on gait. We find no evidence for scaling of duty factor with body size, suggesting that vertical forces scale with dynamic similarity. However, at dynamically similar speeds, large birds use relatively shorter stride lengths and higher stride frequencies compared with small birds. We also find that birds with long legs for their mass, such as the white stork and red-legged seriema, use longer strides and lower swing frequencies, consistent with the influence of high limb inertia on gait. We discuss the observed scaling of avian bipedal gait in relation to mechanical demands for force, work and power relative to muscle actuator capacity, muscle activation costs related to leg cycling frequency, and considerations of stability and agility. Many opportunities remain for future work to investigate how morphology influences gait dynamics among birds specialized for different habitats and locomotor behaviors., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

In addition to a vestibular system, birds uniquely have a balance-sensing organ within the pelvis, called the lumbosacral organ (LSO). The LSO is well developed in terrestrial birds, possibly to facilitate balance control in perching and terrestrial locomotion. No previous studies have quantified the functional benefits of the LSO for balance. We suggest two main benefits of hip-localized balance sense: reduced sensorimotor delay and improved estimation of foot-ground acceleration. We used system identification to test the hypothesis that hip-localized balance sense improves estimates of foot acceleration compared to a head-localized sense, due to closer proximity to the feet. We built a physical model of a standing guinea fowl perched on a platform, and used 3D accelerometers at the hip and head to replicate balance sense by the LSO and vestibular systems. The horizontal platform was attached to the end effector of a 6 DOF robotic arm, allowing us to apply perturbations to the platform analogous to motions of a compliant branch. We also compared state estimation between models with low and high neck stiffness. Cross-correlations revealed that foot-to-hip sensing delays were shorter than foot-to-head, as expected. We used multi-variable output error state-space (MOESP) system identification to estimate foot-ground acceleration as a function of hip- and head-localized sensing, individually and combined. Hip-localized sensors alone provided the best state estimates, which were not improved when fused with head-localized sensors. However, estimates from head-localized sensors improved with higher neck stiffness. Our findings support the hypothesis that hip-localized balance sense improves the speed and accuracy of foot state estimation compared to head-localized sense. The findings also suggest a role of neck muscles for active sensing for balance control: increased neck stiffness through muscle co-contraction can improve the utility of vestibular signals. Our engineering approach provides, to our knowledge, the first quantitative evidence for functional benefits of the LSO balance sense in birds. The findings support notions of control modularity in birds, with preferential vestibular sense for head stability and gaze, and LSO for body balance control,respectively. The findings also suggest advantages for distributed and active sensing for agile locomotion in compliant bipedal robots., (Copyright © 2018 Urbina-Meléndez, Jalaleddini, Daley and Valero-Cuevas.)

The ostrich (Struthio camelus) is widely appreciated as a fast and agile bipedal athlete, and is a useful comparative bipedal model for human locomotion. Here, we used GPS-IMU sensors to measure naturally selected gait dynamics of ostriches roaming freely over a wide range of speeds in an open field and developed a quantitative method for distinguishing walking and running using accelerometry. We compared freely selected gait-speed distributions with previous laboratory measures of gait dynamics and energetics. We also measured the walk-run and run-walk transition speeds and compared them with those reported for humans. We found that ostriches prefer to walk remarkably slowly, with a narrow walking speed distribution consistent with minimizing cost of transport (CoT) according to a rigid-legged walking model. The dimensionless speeds of the walk-run and run-walk transitions are slower than those observed in humans. Unlike humans, ostriches transition to a run well below the mechanical limit necessitating an aerial phase, as predicted by a compass-gait walking model. When running, ostriches use a broad speed distribution, consistent with previous observations that ostriches are relatively economical runners and have a flat curve for CoT against speed. In contrast, horses exhibit U-shaped curves for CoT against speed, with a narrow speed range within each gait for minimizing CoT. Overall, the gait dynamics of ostriches moving freely over natural terrain are consistent with previous lab-based measures of locomotion. Nonetheless, ostriches, like humans, exhibit a gait-transition hysteresis that is not explained by steady-state locomotor dynamics and energetics. Further study is required to understand the dynamics of gait transitions., (© 2016. Published by The Company of Biologists Ltd.)

Locomotor control mechanisms must flexibly adapt to both anticipated and unexpected terrain changes to maintain movement and avoid a fall. Recent studies revealed that ground birds alter movement in advance of overground obstacles, but not treadmill obstacles, suggesting context-dependent shifts in the use of anticipatory control. We hypothesized that differences between overground and treadmill obstacle negotiation relate to differences in visual sensory information, which influence the ability to execute anticipatory manoeuvres. We explored two possible explanations: (1) previous treadmill obstacles may have been visually imperceptible, as they were low contrast to the tread, and (2) treadmill obstacles are visible for a shorter time compared with runway obstacles, limiting time available for visuomotor adjustments. To investigate these factors, we measured electromyographic activity in eight hindlimb muscles of the guinea fowl (Numida meleagris, N=6) during treadmill locomotion at two speeds (0.7 and 1.3 m s(-1)) and three terrain conditions at each speed: (i) level, (ii) repeated 5 cm low-contrast obstacles (<10% contrast, black/black), and (iii) repeated 5 cm high-contrast obstacles (>90% contrast, black/white). We hypothesized that anticipatory changes in muscle activity would be higher for (1) high-contrast obstacles and (2) the slower treadmill speed, when obstacle viewing time is longer. We found that treadmill speed significantly influenced obstacle negotiation strategy, but obstacle contrast did not. At the slower speed, we observed earlier and larger anticipatory increases in muscle activity and shifts in kinematic timing. We discuss possible visuomotor explanations for the observed context-dependent use of anticipatory strategies., (© 2015. Published by The Company of Biologists Ltd.)

Cursorial ground birds are paragons of bipedal running that span a 500-fold mass range from quail to ostrich. Here we investigate the task-level control priorities of cursorial birds by analysing how they negotiate single-step obstacles that create a conflict between body stability (attenuating deviations in body motion) and consistent leg force-length dynamics (for economy and leg safety). We also test the hypothesis that control priorities shift between body stability and leg safety with increasing body size, reflecting use of active control to overcome size-related challenges. Weight-support demands lead to a shift towards straighter legs and stiffer steady gait with increasing body size, but it remains unknown whether non-steady locomotor priorities diverge with size. We found that all measured species used a consistent obstacle negotiation strategy, involving unsteady body dynamics to minimise fluctuations in leg posture and loading across multiple steps, not directly prioritising body stability. Peak leg forces remained remarkably consistent across obstacle terrain, within 0.35 body weights of level running for obstacle heights from 0.1 to 0.5 times leg length. All species used similar stance leg actuation patterns, involving asymmetric force-length trajectories and posture-dependent actuation to add or remove energy depending on landing conditions. We present a simple stance leg model that explains key features of avian bipedal locomotion, and suggests economy as a key priority on both level and uneven terrain. We suggest that running ground birds target the closely coupled priorities of economy and leg safety as the direct imperatives of control, with adequate stability achieved through appropriately tuned intrinsic dynamics., (© 2014. Published by The Company of Biologists Ltd.)

To achieve robust and stable legged locomotion in uneven terrain, animals must effectively coordinate limb swing and stance phases, which involve distinct yet coupled dynamics. Recent theoretical studies have highlighted the critical influence of swing-leg trajectory on stability, disturbance rejection, leg loading and economy of walking and running. Yet, simulations suggest that not all these factors can be simultaneously optimized. A potential trade-off arises between the optimal swing-leg trajectory for disturbance rejection (to maintain steady gait) versus regulation of leg loading (for injury avoidance and economy). Here we investigate how running guinea fowl manage this potential trade-off by comparing experimental data to predictions of hypothesis-based simulations of running over a terrain drop perturbation. We use a simple model to predict swing-leg trajectory and running dynamics. In simulations, we generate optimized swing-leg trajectories based upon specific hypotheses for task-level control priorities. We optimized swing trajectories to achieve i) constant peak force, ii) constant axial impulse, or iii) perfect disturbance rejection (steady gait) in the stance following a terrain drop. We compare simulation predictions to experimental data on guinea fowl running over a visible step down. Swing and stance dynamics of running guinea fowl closely match simulations optimized to regulate leg loading (priorities i and ii), and do not match the simulations optimized for disturbance rejection (priority iii). The simulations reinforce previous findings that swing-leg trajectory targeting disturbance rejection demands large increases in stance leg force following a terrain drop. Guinea fowl negotiate a downward step using unsteady dynamics with forward acceleration, and recover to steady gait in subsequent steps. Our results suggest that guinea fowl use swing-leg trajectory consistent with priority for load regulation, and not for steadiness of gait. Swing-leg trajectory optimized for load regulation may facilitate economy and injury avoidance in uneven terrain.

We proposed three swing leg control policies for spring-mass running robots, inspired by experimental data from our recent collaborative work on ground running birds. Previous investigations suggest that animals may prioritize injury avoidance and/or efficiency as their objective function during running rather than maintaining limit-cycle stability. Therefore, in this study we targeted structural capacity (maximum leg force to avoid damage) and efficiency as the main goals for our control policies, since these objective functions are crucial to reduce motor size and structure weight. Each proposed policy controls the leg angle as a function of time during flight phase such that its objective function during the subsequent stance phase is regulated. The three objective functions that are regulated in the control policies are (i) the leg peak force, (ii) the axial impulse, and (iii) the leg actuator work. It should be noted that each control policy regulates one single objective function. Surprisingly, all three swing leg control policies result in nearly identical subsequent stance phase dynamics. This implies that the implementation of any of the proposed control policies would satisfy both goals (damage avoidance and efficiency) at once. Furthermore, all three control policies require a surprisingly simple leg angle adjustment: leg retraction with constant angular acceleration.

Walking on uneven terrain is more energetically costly than walking on smooth ground, but the biomechanical factors that contribute to this increase are unknown. To identify possible factors, we constructed an uneven terrain treadmill that allowed us to record biomechanical, electromyographic and metabolic energetics data from human subjects. We hypothesized that walking on uneven terrain would increase step width and length variability, joint mechanical work and muscle co-activation compared with walking on smooth terrain. We tested healthy subjects (N=11) walking at 1.0 m s(-1), and found that, when walking on uneven terrain with up to 2.5 cm variation, subjects decreased their step length by 4% and did not significantly change their step width, while both step length and width variability increased significantly (22 and 36%, respectively; P<0.05). Uneven terrain walking caused a 28 and 62% increase in positive knee and hip work, respectively, and a 26% greater magnitude of negative knee work (0.0106, 0.1078 and 0.0425 J kg(-1), respectively; P<0.05). Mean muscle activity increased in seven muscles in the lower leg and thigh (P<0.05). These changes caused overall net metabolic energy expenditure to increase by 0.73 W kg(-1) (28%; P<0.0001). Much of that increase could be explained by the increased mechanical work observed at the knee and hip. Greater muscle co-activation could also contribute to increased energetic cost but to unknown degree. The findings provide insight into how lower limb muscles are used differently for natural terrain compared with laboratory conditions.

One of the most extraordinary results of selective breeding is the modern broiler chicken, whose phenotypic attributes reflect its genetic success. Unfortunately, leg health issues and poor walking ability are prevalent in the broiler population, with the exact aetiopathogenesis unknown. Here we present a biomechanical analysis of the gait dynamics of the modern broiler and its two pureline commercial broiler breeder lines (A and B) in order to clarify how changes in basic morphology are associated with the way these chickens walk. We collected force plate and kinematic data from 25 chickens (market age), over a range of walking speeds, to quantify the three-dimensional dynamics of the centre of mass (CoM) and determine how these birds modulate the force and mechanical work of locomotion. Common features of their gait include extremely slow walking speeds, a wide base of support and large lateral motions of the CoM, which primarily reflect changes to cope with their apparent instability and large body mass. These features allowed the chickens to keep their peak vertical forces low, but resulted in high mediolateral forces, which exceeded fore-aft forces. Gait differences directly related to morphological characteristics also exist. This was particularly evident in Pureline B birds, which have a more crouched limb posture. Mechanical costs of transport were still similar across all lines and were not exceptional when compared with more wild-type ground-running birds. Broiler chickens seem to have an awkward gait, but some aspects of their dynamics show rather surprising similarities to other avian bipeds.

Locomotor-respiratory coupling (LRC), phase-locking between breathing and stepping rhythms, occurs in many vertebrates. When quadrupedal mammals gallop, 1∶1 stride per breath coupling is necessitated by pronounced mechanical interactions between locomotion and ventilation. Humans show more flexibility in breathing patterns during locomotion, using LRC ratios of 2∶1, 2.5∶1, 3∶1, or 4∶1 and sometimes no coupling. Previous studies provide conflicting evidence on the mechanical significance of LRC in running humans. Some studies suggest LRC improves breathing efficiency, but others suggest LRC is mechanically insignificant because 'step-driven flows' (ventilatory flows attributable to step-induced forces) contribute a negligible fraction of tidal volume. Yet, although step-driven flows are brief, they cause large fluctuations in ventilatory flow. Here we test the hypothesis that running humans use LRC to minimize antagonistic effects of step-driven flows on breathing. We measured locomotor-ventilatory dynamics in 14 subjects running at a self-selected speed (2.6±0.1 ms(-1)) and compared breathing dynamics in their naturally 'preferred' and 'avoided' entrainment patterns. Step-driven flows occurred at 1-2X step frequency with peak magnitudes of 0.97±0.45 Ls(-1) (mean ±S.D). Step-driven flows varied depending on ventilatory state (high versus low lung volume), suggesting state-dependent changes in compliance and damping of thoraco-abdominal tissues. Subjects naturally preferred LRC patterns that minimized antagonistic interactions and aligned ventilatory transitions with assistive phases of the step. Ventilatory transitions initiated in 'preferred' phases within the step cycle occurred 2x faster than those in 'avoided' phases. We hypothesize that humans coordinate breathing and locomotion to minimize antagonistic loading of respiratory muscles, reduce work of breathing and minimize rate of fatigue. Future work could address the potential consequences of locomotor-ventilatory interactions for elite endurance athletes and individuals who are overweight or obese, populations in which respiratory muscle fatigue can be limiting.

Differences in rhythmicity (relative variance in cycle period) among mammal, fish, and lizard feeding systems have been hypothesized to be associated with differences in their sensorimotor control systems. We tested this hypothesis by examining whether the locomotion of tachymetabolic tetrapods (birds and mammals) is more rhythmic than that of bradymetabolic tetrapods (lizards, alligators, turtles, salamanders). Species averages of intraindividual coefficients of variation in cycle period were compared while controlling for gait and substrate. Variance in locomotor cycle periods is significantly lower in tachymetabolic than in bradymetabolic animals for datasets that include treadmill locomotion, non-treadmill locomotion, or both. When phylogenetic relationships are taken into account the pooled analyses remain significant, whereas the non-treadmill and the treadmill analyses become nonsignificant. The co-occurrence of relatively high rhythmicity in both feeding and locomotor systems of tachymetabolic tetrapods suggests that the anatomical substrate of rhythmicity is in the motor control system, not in the musculoskeletal components., (© 2012 The Author(s). Evolution© 2012 The Society for the Study of Evolution.)

We understand little about how animals adjust locomotor behaviour to negotiate uneven terrain. The mechanical demands and constraints of such behaviours likely differ from uniform terrain locomotion. Here we investigated how common pheasants negotiate visible obstacles with heights from 10 to 50% of leg length. Our goal was to determine the neuro-mechanical strategies used to achieve robust stability, and address whether strategies vary with obstacle height. We found that control of landing conditions was crucial for minimising fluctuations in stance leg loading and work in uneven terrain. Variation in touchdown leg angle (θ(TD)) was correlated with the orientation of ground force during stance, and the angle between the leg and body velocity vector at touchdown (β(TD)) was correlated with net limb work. Pheasants actively targeted obstacles to control body velocity and leg posture at touchdown to achieve nearly steady dynamics on the obstacle step. In the approach step to an obstacle, the birds produced net positive limb work to launch themselves upward. On the obstacle, body dynamics were similar to uniform terrain. Pheasants also increased swing leg retraction velocity during obstacle negotiation, which we suggest is an active strategy to minimise fluctuations in peak force and leg posture in uneven terrain. Thus, pheasants appear to achieve robustly stable locomotion through a combination of path planning using visual feedback and active adjustment of leg swing dynamics to control landing conditions. We suggest that strategies for robust stability are context specific, depending on the quality of sensory feedback available, especially visual input.

Humans and birds both walk and run bipedally on compliant legs. However, differences in leg architecture may result in species-specific leg control strategies as indicated by the observed gait patterns. In this work, control strategies for stable running are derived based on a conceptual model and compared with experimental data on running humans and pheasants (Phasianus colchicus). From a model perspective, running with compliant legs can be represented by the planar spring mass model and stabilized by applying swing leg control. Here, linear adaptations of the three leg parameters, leg angle, leg length and leg stiffness during late swing phase are assumed. Experimentally observed kinematic control parameters (leg rotation and leg length change) of human and avian running are compared, and interpreted within the context of this model, with specific focus on stability and robustness characteristics. The results suggest differences in stability characteristics and applied control strategies of human and avian running, which may relate to differences in leg posture (straight leg posture in humans, and crouched leg posture in birds). It has been suggested that crouched leg postures may improve stability. However, as the system of control strategies is overdetermined, our model findings suggest that a crouched leg posture does not necessarily enhance running stability. The model also predicts different leg stiffness adaptation rates for human and avian running, and suggests that a crouched avian leg posture, which is capable of both leg shortening and lengthening, allows for stable running without adjusting leg stiffness. In contrast, in straight-legged human running, the preparation of the ground contact seems to be more critical, requiring leg stiffness adjustment to remain stable. Finally, analysis of a simple robustness measure, the normalized maximum drop, suggests that the crouched leg posture may provide greater robustness to changes in terrain height., (Copyright © 2011 Elsevier Ltd. All rights reserved.)

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.

Economy is a central principle for understanding animal locomotion. Yet, compared with theoretical predictions concerning economy, animals run with compliant legs that are energetically costly. Here, we address this apparent paradox, highlighting two factors that predict benefits for compliant gaits: (i) minimizing cost of work associated with bouncing viscera; and (ii) leg control for robust stability in uneven terrain. We show that consideration of the effects of bouncing viscera predicts an energetic optimum for relatively compliant legs. To compare stability in uneven terrain, we introduce the normalized maximum drop (NMD), a measure based on simple kinematics, which predicts that compliant legs allow negotiation of relatively larger terrain perturbations without failure. Our model also suggests an inherent trade-off in control of leg retraction velocity (omega) for stability: low omega allows higher NMD, reducing fall risk, whereas high omega minimizes peak forces with terrain drops, reducing injury risk. Optimization for one of these factors explicitly limits the other; however, compliant legs relax this trade-off, allowing greater stability by both measures. Our models suggest compromises in leg control for economy and stability that might explain why animals run with compliant legs.

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 constraints to maximum walking speed and the underlying cause of the walk-run transition remains controversial. However, the motions of the body and legs can be reduced to a few mechanical principles, which, if valid, impose simple physics-based limits to walking speed. Bipedal walking may be viewed as a vaulting gait, with the centre of mass (CoM) passing over a stiff stance leg (an 'inverted pendulum'), while the swing leg swings forward (as a pendulum). At its simplest, this forms a 'compass gait' walker, which has a maximum walking speed constrained by simple mechanics: walk too fast, or with too high a step length, and gravity fails to keep the stance foot attached to the floor. But how useful is such an extremely reductionist model? In the present study, we report measurements on a range of duck breeds as example unspecialized, non-planar, crouch-limbed walkers and contrast these findings with previous measurements on humans, using the theoretical framework of compass gait walking. Ducks walked as inverted pendulums with near-passive swing legs up to relative velocities around 0.5, remarkably consistent with the theoretical model. By contrast, top walking speeds in humans cannot be achieved with passive swing legs: humans, while still constrained by compass gait mechanics, extend their envelope of walking speeds by using relatively high step frequencies. Therefore, the capacity to drive the swing leg forward by walking humans may be a specialization for walking, allowing near-passive vaulting of the CoM at walking speeds 4/3 that possible with a passive (duck-like) swing leg.

When runners encounter a sudden bump in the road, they rapidly adjust leg mechanics to keep from falling. New evidence suggests that they may be able to do this without help from the brain.

The bouncing gaits of terrestrial animals (hopping, running, trotting) can be modeled as a hybrid dynamic system, with spring-mass dynamics during stance and ballistic motion during the aerial phase. We used a simple hopping robot controlled by an artificial neural oscillator to test the ability of the neural oscillator to adaptively drive this hybrid dynamic system. The robot had a single joint, actuated by an artificial pneumatic muscle in series with a tendon spring. We examined how the oscillator-robot system responded to variation in two neural control parameters: descending neural drive and neuromuscular gain. We also tested the ability of the oscillator-robot system to adapt to variations in mechanical properties by changing the series and parallel spring stiffnesses. Across a 100-fold variation in both supraspinal gain and muscle gain, hopping frequency changed by less than 10%. The neural oscillator consistently drove the system at the resonant half-period for the stance phase, and adapted to a new resonant half-period when the muscle series and parallel stiffnesses were altered. Passive cycling of elastic energy in the tendon accounted for 70-79% of the mechanical work done during each hop cycle. Our results demonstrate that hopping dynamics were largely determined by the intrinsic properties of the mechanical system, not the specific choice of neural oscillator parameters. The findings provide the first evidence that an artificial neural oscillator will drive a hybrid dynamic system at partial resonance.

Technological advances in robotic hardware and software have enabled powered exoskeletons to move from science fiction to the real world. The objective of this article is to emphasize two main points for future research. First, the design of future devices could be improved by exploiting biomechanical principles of animal locomotion. Two goals in exoskeleton research could particularly benefit from additional physiological perspective: 1) reduction in the metabolic energy expenditure of the user while wearing the device, and 2) minimization of the power requirements for actuating the exoskeleton. Second, a reciprocal potential exists for robotic exoskeletons to advance our understanding of human locomotor physiology. Experimental data from humans walking and running with robotic exoskeletons could provide important insight into the metabolic cost of locomotion that is impossible to gain with other methods. Given the mutual benefits of collaboration, it is imperative that engineers and physiologists work together in future studies on robotic exoskeletons for human locomotion.

By integrating studies of muscle function with analysis of whole body and limb dynamics, broader appreciation of neuromuscular function can be achieved. Ultimately, such studies need to address non-steady locomotor behaviors relevant to animals in their natural environments. When animals move slowly they likely rely on voluntary coordination of movement involving higher brain centers. However, when moving fast, their movements depend more strongly on responses controlled at more local levels. Our focus here is on control of fast-running locomotion. A key observation emerging from studies of steady level locomotion is that simple spring-mass dynamics, which help to economize energy expenditure, also apply to stabilization of unsteady running. Spring-mass dynamics apply to conditions that involve lateral impulsive perturbations, sudden changes in terrain height, and sudden changes in substrate stiffness or damping. Experimental investigation of unsteady locomotion is challenging, however, due to the variability inherent in such behaviors. Another emerging principle is that initial conditions associated with postural changes following a perturbation define different context-dependent stabilization responses. Distinct stabilization modes following a perturbation likely result from proximo-distal differences in limb muscle architecture, function and control strategy. Proximal muscles may be less sensitive to sudden perturbations and appear to operate, in such circumstances, under feed-forward control. In contrast, multiarticular distal muscles operate, via their tendons, to distribute energy among limb joints in a manner that also depends on the initial conditions of limb contact with the ground. Intrinsic properties of these distal muscle-tendon elements, in combination with limb and body dynamics, appear to provide rapid initial stabilizing mechanisms that are often consistent with spring-mass dynamics. These intrinsic mechanisms likely help to simplify the neural control task, in addition to compensating for delays inherent to subsequent force- and length-dependent neural feedback. Future work will benefit from integrative biomechanical approaches that employ a combination of modeling and experimental techniques to understand how the elegant interplay of intrinsic muscle properties, body dynamics and neural control allows animals to achieve stability and agility over a variety of conditions.

Neuromechanics seeks to understand how muscles, sense organs, motor pattern generators, and brain interact to produce coordinated movement, not only in complex terrain but also when confronted with unexpected perturbations. Applications of neuromechanics include ameliorating human health problems (including prosthesis design and restoration of movement following brain or spinal cord injury), as well as the design, actuation and control of mobile robots. In animals, coordinated movement emerges from the interplay among descending output from the central nervous system, sensory input from body and environment, muscle dynamics, and the emergent dynamics of the whole animal. The inevitable coupling between neural information processing and the emergent mechanical behavior of animals is a central theme of neuromechanics. Fundamentally, motor control involves a series of transformations of information, from brain and spinal cord to muscles to body, and back to brain. The control problem revolves around the specific transfer functions that describe each transformation. The transfer functions depend on the rules of organization and operation that determine the dynamic behavior of each subsystem (i.e., central processing, force generation, emergent dynamics, and sensory processing). In this review, we (1) consider the contributions of muscles, (2) sensory processing, and (3) central networks to motor control, (4) provide examples to illustrate the interplay among brain, muscles, sense organs and the environment in the control of movement, and (5) describe advances in both robotics and neuromechanics that have emerged from application of biological principles in robotic design. Taken together, these studies demonstrate that (1) intrinsic properties of muscle contribute to dynamic stability and control of movement, particularly immediately after perturbations; (2) proprioceptive feedback reinforces these intrinsic self-stabilizing properties of muscle; (3) control systems must contend with inevitable time delays that can simplify or complicate control; and (4) like most animals under a variety of circumstances, some robots use a trial and error process to tune central feedforward control to emergent body dynamics.

We currently know little about how animals achieve dynamic stability when running over uneven and unpredictable terrain, often characteristic of their natural environment. Here we investigate how limb and joint mechanics of an avian biped, the helmeted guinea fowl Numida meleagris, respond to an unexpected drop in terrain during running. In particular, we address how joint mechanics are coordinated to achieve whole limb dynamics. Based on muscle-tendon architecture and previous studies of steady and incline locomotion, we hypothesize a proximo-distal gradient in joint neuromechanical control. In this motor control strategy, (1) proximal muscles at the hip and knee joints are controlled primarily in a feedforward manner and exhibit load-insensitive mechanical performance, and (2) distal muscles at the ankle and tarsometatarso-phalangeal (TMP) joints are highly load-sensitive, due to intrinsic mechanical effects and rapid, higher gain proprioceptive feedback. Limb kinematics and kinetics during the unexpected perturbation reveal that limb retraction, controlled largely by the hip, remains similar to level running throughout the perturbed step, despite altered limb loading. Individual joints produce or absorb energy during both level and perturbed running steps, such that the net limb work depends on the balance of energy among the joints. The hip maintains the same mechanical role regardless of limb loading, whereas the ankle and TMP switch between spring-like or damping function depending on limb posture at ground contact. Initial knee angle sets limb posture and alters the balance of work among the joints, although the knee contributes little work itself. This distribution of joint function results in posture-dependent changes in work performance of the limb, which allow guinea fowl to rapidly produce or absorb energy in response to the perturbation. The results support the hypothesis that a proximo-distal gradient exists in limb neuromuscular performance and motor control. This control strategy allows limb cycling to remain constant, whereas limb posture, loading and energy performance are interdependent. We propose that this control strategy provides simple, rapid mechanisms for managing energy and controlling velocity when running over rough terrain.

Legged animals routinely negotiate rough, unpredictable terrain with agility and stability that outmatches any human-built machine. Yet, we know surprisingly little about how animals accomplish this. Current knowledge is largely limited to studies of steady movement. These studies have revealed fundamental mechanisms used by terrestrial animals for steady locomotion. However, it is unclear whether these models provide an appropriate framework for the neuromuscular and mechanical strategies used to achieve dynamic stability over rough terrain. Perturbation experiments shed light on this issue, revealing the interplay between mechanics and neuromuscular control. We measured limb mechanics of helmeted guinea fowl (Numida meleagris) running over an unexpected drop in terrain, comparing their response to predictions of the mass-spring running model. Adjustment of limb contact angle explains 80% of the variation in stance-phase limb loading following the perturbation. Surprisingly, although limb stiffness varies dramatically, it does not influence the response. This result agrees with a mass-spring model, although it differs from previous findings on humans running over surfaces of varying compliance. However, guinea fowl sometimes deviate from mass-spring dynamics through posture-dependent work performance of the limb, leading to substantial energy absorption following the perturbation. This posture-dependent actuation allows the animal to absorb energy and maintain desired velocity on a sudden substrate drop. Thus, posture-dependent work performance of the limb provides inherent velocity control over rough terrain. These findings highlight how simple mechanical models extend to unsteady conditions, providing fundamental insights into neuromuscular control of movement and the design of dynamically stable legged robots and prosthetic devices.

In the natural world, animals must routinely negotiate varied and unpredictable terrain. Yet, we know little about the locomotor strategies used by animals to accomplish this while maintaining dynamic stability. In this paper, we perturb the running of guinea fowl with an unexpected drop in substrate height (DeltaH). The drop is camouflaged to remove any visual cue about the upcoming change in terrain that would allow an anticipatory response. To maintain stability upon a sudden drop in substrate height and prevent a fall, the bird must compensate by dissipating energy or converting it to another form. The aim of this paper is to investigate the control strategies used by birds in this task. In particular, we assess the extent to which guinea fowl maintain body weight support and conservative spring-like body dynamics in the perturbed step. This will yield insight into how animals integrate mechanics and control to maintain dynamic stability in the face of real-world perturbations. Our results show that, despite altered body dynamics and a great deal of variability in the response, guinea fowl are quite successful in maintaining dynamic stability, as they stumbled only once (without falling) in the 19 unexpected perturbations. In contrast, when the birds could see the upcoming drop in terrain, they stumbled in 4 of 20 trials (20%, falling twice), and came to a complete stop in an additional 6 cases (30%). The bird's response to the unexpected perturbation fell into three general categories: (1) conversion of vertical energy (EV=EP+EKv) to horizontal kinetic energy (EKh), (2) absorption of EV through negative muscular work (-DeltaEcom), or (3) converting EP to vertical kinetic energy (EKv), effectively continuing the ballistic path of the animal's center of mass (COM) from the prior aerial phase. However, the mechanics that distinguish these categories actually occur along a continuum with varying degrees of body weight support and actuation by the limb, related to the magnitude and direction of the ground reaction force (GRF) impulse, respectively. In most cases, the muscles of the limb either produced or absorbed energy during the response, as indicated by net changes in COM energy (Ecom). The limb likely begins stance in a more retracted, extended position due to the 26 ms delay in ground contact relative to that anticipated by the bird. This could explain the diminished decelerating force during the first half of stance and the exchange between EP and EK during stance as the body vaults over the limb. The varying degree of weight support and energy absorption in the perturbed step suggests that variation in the initial limb configuration leads to different intrinsic dynamics and reflex action. Future investigation into the limb and muscle mechanics underlying these responses could yield further insight into the control mechanisms that allow such robust dynamic stability of running in the face of large, unexpected perturbations.