Abstract

How actomyosin crossbridges share and transmit loads between the thick and thin filaments in a sarcomere underlies the emergence of muscle’s stimulus-dependent material properties. Following A.F. Huxley’s work, many sarcomere models treat the thick and thin filaments as rigid and lump their compliance into a single series elastic element. Under this approximation, the crossbridges act as parallel elastic force generators. So their collective dynamics are captured by the ensemble mean. In this work, we investigate the accuracy of this approximation by exactly accounting for the spatially distributed filament and crossbridge compliances. We show that even the small degree of measured filament compliance in a sarcomere leads to a profound deviation of the mechanical behavior from the ensemble mean. The lumped compliance approximation fails to capture a stiction-like state of activated muscle that is thought to underlie how animals are able to stiffen their joints through muscle co-contraction. Further analyses show that crossbridge clusters may be favored because they lower the total system strain energy. We speculate that the spatial inhomogeneity of crossbridges has mechanochemical consequences that affect the development and cycling of crossbridges in actomyosin networks. Specifically, clusters of persistent, stalled crossbridges are predicted to emerge as a stable state for a frustrated ensemble and possibly explain transitions between a fluid-like and solid-like state in muscle.