Optimal workloop energetics of muscle-actuated systems: an impedance matching view

Integrative approaches to studying the coupled dynamics of skeletal muscles with their loads while under neural control have focused largely on questions pertaining to the postural and dynamical stability of animals and humans. Prior studies have focused on how the central nervous system actively modulates muscle mechanical impedance to generate and stabilize motion and posture. However, the question of whether muscle impedance properties can be neurally modulated to create favorable mechanical energetics, particularly in the context of periodic tasks, remains open. Through muscle stiffness tuning, we hypothesize that a pair of antagonist muscles acting against a common load may produce significantly more power synergistically than individually when impedance matching conditions are met between muscle and load. Since neurally modulated muscle stiffness contributes to the coupled muscle-load stiffness, we further anticipate that power-optimal oscillation frequencies will occur at frequencies greater than the natural frequency of the load. These hypotheses were evaluated computationally by applying optimal control methods to a bilinear muscle model, and also evaluated through in vitro measurements on frog Plantaris longus muscles acting individually and in pairs upon a mass-spring-damper load. We find a 7-fold increase in mechanical power when antagonist muscles act synergistically compared to individually at a frequency higher than the load natural frequency. These observed behaviors are interpreted in the context of resonance tuning and the engineering notion of impedance matching. These findings suggest that the central nervous system can adopt strategies to harness inherent muscle impedance in relation to external loads to attain favorable mechanical energetics.