Linking in vivo muscle dynamics to in situ force-length and force-velocity reveals that guinea fowl lateral gastrocnemius operates at shorter than optimal lengths.

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 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 to 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.

Linking in vivo muscle dynamics to in situ force-length and force-velocity reveals that guinea fowl lateral gastrocnemius operates at shorter than optimal lengths.

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 L0 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.

Kinematic trajectories in response to speed perturbations in walking suggest modular task-level control of leg angle and length.

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.

Bio-inspired swing leg control for spring-mass robots running on ground with unexpected height disturbance.

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.

Running stability is enhanced by a proximo-distal gradient in joint neuromechanical control.

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.

Novel motor gestures for phonation during inspiration enhance the acoustic complexity of birdsong.

Sound generation based on a pulmonary mechanism typically occurs during the expiratory phase of respiration. Phonation during inspiration has been postulated for the calls of some amphibians and for exceptional sounds in some human languages. No direct evidence exists for phonation during inspiration in birds, but such a mechanism has been proposed to explain very long uninterrupted songs. Here, we report the first physiological evidence for inspiratory sound production in the song of the zebra finch (Taeniopygia guttata). Motor gestures of the vocal and respiratory muscles leading to the production of inspiratory phonation differ from those of silent inspirations during song as well as from those leading to phonation during expiration. Inspiratory syllables have a high fundamental frequency, which makes them acoustically distinct from all other zebra finch song syllables. Furthermore, young zebra finches copy these inspiratory syllables from their tutor song, producing them during inspiration. This suggests that physical limitations confine the production of these sounds to the inspiratory phase in zebra finches. These findings directly demonstrate how novel respiratory-vocal coordination can enhance the acoustic structure of birdsong, and thus provide insight into the evolution of song complexity.