Influence of internal muscle properties on muscle shape change and gearing in the human gastrocnemii.

Abstract

Skeletal muscles bulge when they contract. These three-dimensional shape changes, coupled with fiber rotation, influence a muscle's mechanical performance by uncoupling fiber velocity from muscle belly velocity (i.e., gearing). Muscle shape change and gearing are likely mediated by the interaction between internal muscle properties and contractile forces. Muscles with greater stiffness and intermuscular fat, due to aging or disuse, may limit a muscle's ability to bulge in width, subsequently causing higher gearing. The aim of this study was to determine the influence of internal muscle properties on shape change, fiber rotation, and gearing in the medial (MG) and lateral gastrocnemii (LG) during isometric plantar flexion contractions. Multimodal imaging techniques were used to measure muscle shear modulus, intramuscular fat, and fat-corrected physiological cross-sectional area (PCSA) at rest, as well as synchronous muscle architecture changes during submaximal and maximal contractions in the MG and LG of 20 young (24 ± 3 yr) and 13 older (70 ± 4 yr) participants. Fat-corrected PCSA was positively associated with fiber rotation, gearing, and changes in thickness during submaximal contractions, but it was negatively associated with changes in thickness at maximal contractions. Muscle stiffness and intramuscular fat were related to muscle bulging and reduced fiber rotation, respectively, but only at high forces. Furthermore, the MG and LG had varied internal muscle properties, which may relate to the differing shape changes, fiber rotations, and gearing behaviors observed at each contraction level. These results indicate that internal muscle properties may play an important role in mediating in vivo muscle shape change and gearing, especially during high-force contractions.NEW & NOTEWORTHY Here, we measured internal muscle properties in vivo to determine their influence on the varying shape change and gearing behaviors in the synergistic gastrocnemii muscles. These relationships have previously only been hypothesized or examined within isolated muscles during supramaximal contractions. Our results contribute to a more comprehensive understanding of the factors that influence a muscle's mechanical response to force with implications for preventing or treating muscle deficits associated with aging, disease, and disuse.