Unsteady locomotion: integrating muscle function with whole body dynamics and neuromuscular control

Abstract

SUMMARY 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.

Structured variability of steady-speed locomotion in rats

“…during running, it is widely accepted that they cannot be actively controlled only by the nervous system (e.g. Biewener and Daley, 2007;Blickhan et al, 2007;Hooper, 2012). During perturbed locomotion, animals instead rely on passive dynamic mechanisms that include spring-mass mechanics and intrinsic mechanisms (see also Biewener and Daley, 2007).…”

“…Biewener and Daley, 2007;Blickhan et al, 2007;Hooper, 2012). During perturbed locomotion, animals instead rely on passive dynamic mechanisms that include spring-mass mechanics and intrinsic mechanisms (see also Biewener and Daley, 2007). In humans and birds, simple spring-mass mechanics mitigate sudden changes in terrain height (Daley and Biewener, 2006;Geyer et al, 2005;Grimmer et al, 2008;Seyfarth et al, 2002).…”

“…Interestingly, bipeds maintain passive spring-mass dynamics when limb contact angle, effective limb length and limb stiffness exhibit particularly limited ranges (Seyfarth et al, 2002;Geyer et al, 2005;Grimmer et al, 2008). In addition, intrinsic mechanisms, including force-length, force-velocity and history-dependent properties as well as postural effects on joint dynamics at the musculoskeletal level help to reduce the control effort and consequently the complexity of the nervous system (see also Biewener and Daley, 2007).…”

“…Importantly, control mechanisms greatly depend on locomotor speed and body size (e.g. Biewener and Daley, 2007;Hooper, 2012). During fast locomotion such as running, mechanical control mechanisms likely play a predominant role in locomotor stability due to neural transmission delays that could be destabilizing (e.g.…”

“…During fast locomotion such as running, mechanical control mechanisms likely play a predominant role in locomotor stability due to neural transmission delays that could be destabilizing (e.g. Full and Koditschek, 1999;Full et al, 2002;Biewener and Daley, 2007). Walking gaits, which occur at slower speeds, are likely to be more actively than passively controlled.…”