Humans trade-off whole-body energy cost to avoid overburdening muscles while walking

Abstract

Metabolic cost minimization is widely regarded as the principal optimality criterion that governs walking. Minimizing muscle activation has, nevertheless, outperformed energy optimization in simulating human gait and predicting certain gait behaviors. The highly coupled nature of metabolic and muscle activation costs makes it difficult to empirically discern the interrelationship between these objectives. We implemented a unique experimental design that pits metabolic cost against muscle activation costs estimated from electromyography of seven lower limb muscles. Healthy adults (N=10) selected between walking on a treadmill incline versus walking in a crouched posture (that disproportionately affected activation cost), forcing a choice between minimizing metabolic cost or activation cost. When experiencing these Competing-Cost-Pairs, participants systematically protected their activation cost at the expense of high metabolic power (19% penalty, p<0.05). This held true when activation cost was expressed as the sum of the muscle activations squared (66% saving, p<0.05) and as the maximal activation across muscles (44% saving, p<0.05), both of which penalize overburdening any individual muscle and thus indicate fatigue avoidance. Activation cost, expressed as the sum of muscle volume-normalized activation, more closely models energy use and was also protected by the participants' decision (23% saving, p<0.05) demonstrating that activation was, at best, an inaccurate proxy signal for metabolic energy. Energy minimization was only observed when there was no adverse effect on muscle activation. By decoupling metabolic and activation costs, we provide the first empirical evidence of humans embracing non-energetic optimality in favor of a clearly defined alternate neuromuscular objective.

The interaction between muscle pathophysiology, body mass, walking speed and ankle foot orthosis stiffness on walking energy cost: a predictive simulation study

“…Additionally, in previous work walking speed tended to be slow due to on the inclusion of all muscle activations squared in the cost function [22,27]. Therefore, this factor was replaced by a penalty on activations above 50% of maximum for the Soleus and Gastrocnemius, as humans only tend to minimize energy cost when activations are kept relatively low [43]. This change in cost function increased simulated walking speed while unrealistic compensatory activations were avoided, and none of the muscle activations exceeded 50%.…”

The effects of crank power and cadence on muscle fascicle shortening velocities, muscle activations and joint-powers during cycling

“…This finding might suggest that the cadence selected by riders at submaximal power output (10% and 30% of Pmax) may be a strategy to minimize fatigue, as previous studies suggest in simulated (Neptune and Hull 1999) and endurance cycling (Takaishi et al 1996). These responses may be seen as the nervous system prioritizing the minimization of activation of overburdened muscles to prolong the movement duration (McDonald et al 2022). While at high power pedaling demand landscapes, it appears that other factors might be involved besides minimizing muscle activation.…”