Nonlinear Muscles, Passive Viscoelasticity and Body Taper Conspire To Create Neuromechanical Phase Lags in Anguilliform Swimmers

Locomotion provides superb examples of cooperation among neuromuscular systems, environmental reaction forces, and sensory feedback. As part of a program to understand the neuromechanics of locomotion, here we construct a model of anguilliform (eel-like) swimming in slender fishes. Building on a continuum mechanical representation of the body as an viscoelastic rod, actuated by a traveling wave of preferred curvature and subject to hydrodynamic reaction forces, we incorporate a new version of a calcium release and muscle force model, fitted to data from the lamprey Ichthyomyzon unicuspis, that interactively generates the curvature wave. We use the model to investigate the source of the difference in speeds observed between electromyographic waves of muscle activation and mechanical waves of body curvature, concluding that it is due to a combination of passive viscoelastic and geometric properties of the body and active muscle properties. Moreover, we find that nonlinear force dependence on muscle length and shortening velocity may reduce the work done by the swimming muscles in steady swimming.