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 describes muscle as an active sponge. Our analysis of existing experiments across species and muscle types highlights the importance of spatially heterogeneous strains and local volumetric deformations. Our minimal theoretical model shows how contractions induce intracellular fluid flow and power active hydraulic oscillations, yielding the limits of ultrafast muscular contractions. We further demonstrate that the viscoelastic response of muscle is naturally non-reciprocal—or odd—owing to its active and anisotropic nature. This enables 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 a revised view of muscle dynamics that emphasizes the multiscale spatiotemporal origins of soft hydraulic power, with potential implications for physiology, biomechanics and locomotion. A multiscale model of muscle as a fluid-filled sponge suggests that hydraulics limits rapid contractions and that the mechanical response of muscle is non-reciprocal.