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Structural Determinants of Muscle Gearing During Dynamic Contractions.

Abstract

In skeletal muscle, interactions between contractile and connective tissue elements at multiple scales result in emergent properties that determine mechanical performance. One of these phenomena is architectural gearing, which is quantified as the ratio of muscle velocity to muscle fiber velocity. Many pennate muscles operate with a gear ratio greater than one because muscles shorten through a combination of muscle fiber shortening and fiber rotation. Within a muscle, gearing is variable across contractions. During low force contractions, muscles operate at high gear while muscles operate at low gear during high force contractions. This variable gearing has a significant impact on muscle performance as muscle architectural changes favor muscle speed during fast contractions and muscle force during slow, high force contractions. We hypothesize that gearing in any given contraction is determined by the dynamic interaction of fiber-generated forces, fluid force transmission, and the elastic behavior of intramuscular connective tissues. Because muscle is isovolumetric, muscle fibers must bulge radially when they shorten. Radial bulging and fiber-generated forces off-axis from the muscle line of action exert forces that load connective tissues that ensheath fibers, fascicles, and the whole muscle. The way in which fluid pressures and fiber forces interact to load connective tissues in three-dimensions remains poorly understood because of the complex and multiscale nature of these interactions. Here we review evidence for variable gearing in pennate muscles, present a conceptual model that describes the fundamental interactions that determine gearing, and discuss where gaps remain in our understanding of the determinants and consequences of muscle shape change and variable gearing.

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