Active muscular hydraulics

Abstract

What limits the rate of contraction in muscle? The molecular cycling of actomyosin crossbridges has typically been assumed to be rate limiting, but muscle is a soft, wet and active tissue that is spatially heterogeneous and heirarchically organized. To bridge these multiple scales, we propose a minimal multiscale model that describes muscle as an active sponge and show how contractions generically induce intracellular fluid flow and power active hydraulic oscillations which dictate the ultimate limits of muscle performance. By reanalyzing data from existing experiments across different species and muscle types, we highlight the role of spatially heterogeneous strains and local volumetric deformations. We further demonstrate that the viscoelastic response of muscle is naturally nonreciprocal (or ‘odd’) due to its active and anisotropic nature that shows how periodic cycles in spatial strain alone can produce work, in sharp contrast to previous views that focus 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 implications for physiology, biomechanics and locomotion.