History-dependent perturbation response in limb muscle

Abstract

Muscle mediates movement but movement is typically unsteady and perturbed. Muscle is known to behave non-linearly and with history-dependent properties during steady locomotion, but the importance of history dependence in mediating muscle function during perturbations remains less clear. To explore the capacity of muscles to mitigate perturbations during locomotion, we constructed a series of perturbations that varied only in kinematic history, keeping instantaneous position, velocity and time from stimulation constant. We found that the response of muscle to a perturbation is profoundly history dependent, varying 4-fold as baseline frequency changes, and dissipating energy equivalent to ∼6 times the kinetic energy of all the limbs in 5 ms (nearly 2400 W kg−1). Muscle energy dissipation during a perturbation is predicted primarily by the force at the onset of the perturbation. This relationship holds across different frequencies and timings of stimulation. This history dependence behaves like a viscoelastic memory producing perturbation responses that vary with the frequency of the underlying movement.