Active hydraulics and odd elasticity of muscle fibres

Abstract

Muscle is a complex hierarchically organized soft contractile engine. To understand the limits on the rate of contraction and muscle energetics, we construct a coarse-grained multiscale model that integrates over molecular details and describes muscle as an active sponge. Our analysis of existing experiments highlights the importance of spatially heterogeneous strains and local volumetric deformations in muscular contractions across species and muscle type. The minimal theoretical model shows how contractions generically induce intracellular fluid flow and power active hydraulic oscillations, which determine the limits of ultrafast muscular contractions. We further demonstrate that the viscoelastic response of muscle is naturally nonreciprocal – or odd – owing to its active and anisotropic nature. This points to an alternate mode of muscular power generation from periodic cycles in spatial strain alone, contrasting with previous descriptions based on temporal cycles. Our work suggests the need for a revised view of muscle dynamics that emphasizes the multiscale spatio-temporal origins of soft hydraulic power, with potential implications for physiology, biomechanics and locomotion.