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 across 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 fastest rate of muscle contraction. A key feature is the presence of spatially heterogeneous strains and local volumetric deformations, which we validate by reanalyzing data from existing experiments across different species and muscle types. We further demonstrate that the viscoelastic response of muscle is naturally nonreciprocal (or ‘odd’) due to its active and anisotropic nature and highlight a novel consequence, whereby periodic cycles in strain alone can produce work. Our work suggests a revised view of muscle dynamics that emphasizes the multiscale spatial aspects in addition to temporal aspects, with implications for physiology, biomechanics and locomotion.
Competing Interest Statement
The authors have declared no competing interest.
