The screw-like mechanism of muscle contraction suggested by 3D SHG imaging and computational reconstruction

The classical sliding filament theory describes muscle contraction as a process in which thin actin filaments slide past thick myosin filaments, driven by cyclic interactions between myosin heads and actin. While this model successfully accounts for sarcomere shortening and force generation, it primarily relies on a one-dimensional representation of filament displacement and does not fully capture the three-dimensional organization and dynamics of the contractile apparatus. In particular, the intrinsic helical geometry of both actin and myosin filaments, as well as the spatial arrangement of myosin heads within the thick filament, suggest that additional degrees of freedom may contribute to contraction mechanisms. In this study, we investigate the three-dimensional organization of myosin filament assemblies using second harmonic generation imaging in five mouse lines, including three wild-type controls and two transgenic models exhibiting a hypermuscular phenotype. Quantitative analysis reveals significant differences in filament density and spatial organization that are not readily explained by a purely sliding-based mechanism. These observations motivate the exploration of an alternative framework in which filament interactions incorporate a rotational component. In the proposed screw-like or helical motion model, myosin heads do not simply progress linearly along actin filaments but follow a subtle rotational trajectory around the filament axis, analogous to the motion of a screw. Such a mechanism could provide a structural and mechanical basis for previously reported asymmetries in force generation, as well as micro-rotational behaviours observed in high-resolution imaging studies.