Person:

Biewener, Andrew

The analysis of terrestrial locomotion over the past half century has focused largely on strategies of mechanical energy recovery used during walking and running. In contrast, we describe the underlying mechanics of legged locomotion as a collision-like interaction that redirects the centre of mass (CoM). We introduce the collision angle, determined by the angle between the CoM force and velocity vectors, and show by computing the collision fraction, a ratio of actual to potential collision, that the quadrupedal walk and gallop employ collision-reduction strategies while the trot permits greater collisions. We provide the first experimental evidence that a collision-based approach can differentiate quadrupedal gaits and quantify interspecific differences. Furthermore, we show that this approach explains the physical basis of a commonly used locomotion metric, the mechanical cost of transport. Collision angle and collision fraction provide a unifying analysis of legged locomotion which can be applied broadly across animal size, leg number and gait.

Over the past 30 years, studies of single muscles have revealed complex patterns of regional variation in muscle architecture, activation, strain and force. In addition, muscles are often functionally integrated with other muscles in parallel or in series. Understanding the extent of this complexity and the interactions between muscles will profoundly influence how we think of muscles in relation to organismal function, and will allow us to address questions regarding the functional benefits (or lack thereof) and dynamics of this complexity under in vivo conditions. This paper has two main objectives. First, we present a cohesive and integrative review of regional variation in function within muscles, and discuss the functional ramifications that can stem from this variation. This involves splitting regional variation into passive and active components. Second, we assess the functional integration of muscles between different limb segments by presenting new data involving in vivo measurements of activation and strain from the medial gastrocnemius, iliotibialis cranialis and iliotibialis lateralis pars preacetabularis of the helmeted guinea fowl (Numida meleagris) during level running on a motorized treadmill. Future research directions for both of these objectives are presented.

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 preactivation 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.

Turning is crucial for animals, particularly during predator–prey interactions and to avoid obstacles. For flying animals, turning consists of changes in (i) flight trajectory, or path of travel, and (ii) body orientation, or 3D angular position. Changes in flight trajectory can only be achieved by modulating aerodynamic forces relative to gravity. How birds coordinate aerodynamic force production relative to changes in body orientation during turns is key to understanding the control strategies used in avian maneuvering flight. We hypothesized that pigeons produce aerodynamic forces in a uniform direction relative to their bodies, requiring changes in body orientation to redirect those forces to turn. Using detailed 3D kinematics and body mass distributions, we examined net aerodynamic forces and body orientations in slowly flying pigeons (Columba livia) executing level 90° turns. The net aerodynamic force averaged over the downstroke was maintained in a fixed direction relative to the body throughout the turn, even though the body orientation of the birds varied substantially. Early in the turn, changes in body orientation primarily redirected the downstroke aerodynamic force, affecting the bird’s flight trajectory. Subsequently, the pigeon mainly reacquired the body orientation used in forward flight without affecting its flight trajectory. Surprisingly, the pigeon’s upstroke generated aerodynamic forces that were approximately 50% of those generated during the downstroke, nearly matching the relative upstroke forces produced by hummingbirds. Thus, pigeons achieve low speed turns much like helicopters, by using whole-body rotations to alter the direction of aerodynamic force production to change their flight trajectory.

Muscle fatigue, a reduction in force as a consequence of exercise, is an important factor for any animal that moves, and can result from both peripheral and/or central mechanisms. Although much is known about whole-limb force generation and activation patterns in fatigued muscles under sustained isometric contractions, little is known about the in vivo dynamics of limb muscle function in relation to whole-body fatigue. Here we show that limb kinematics and contractile function in the lateral (LG) and medial (MG) gastrocnemius of helmeted guineafowl (Numida meleagris) are significantly altered following fatiguing exercise at 2 m sK1 on an inclined treadmill. The two most significant findings were that the variation in muscle force generation, measured directly from the muscles’ tendons, increased significantly with fatigue, and fascicle shortening in the proximal MG, but not the distal MG, decreased significantly with fatigue. We suggest that the former is a potential mechanism for decreased stability associated with fatigue. The region-specific alteration of fascicle behaviour within the MG as a result of fatigue suggests a complex response to fatigue that probably depends on muscle–aponeurosis and tendon architecture not previously explored. These findings highlight the importance of studying the integrative in vivo dynamics of muscle function in response to fatigue.

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.