Beyond bouncy gaits: The role of multiscale compliance in skeletal muscle performance

McNeill Alexander demonstrated that compliant tendons could improve locomotor performance by decoupling muscle length changes from joint movements and mechanical energy fluctuations. This was revolutionary for our understanding of animal locomotion, but also highlighted the limitations of our understanding of the contractile performance of muscle under the dynamic conditions relevant to movement. This review addresses the potential for biological compliance to not only alter the demands on muscle but also fundamentally change contractile performance. Compliance exists across all spatial scales within the muscle. Molecule scale compliance is observed in the thin filament and the cytoskeletal protein titin likely acts as an activation-dependent variable-stiffness spring. Larger scale connective tissue compliance is found not only in tendons but also the more structurally complex extracellular matrix and aponeuroses. The interaction of the compliance in these structures with the contractile elements of muscle, and the variation in this interaction across physiological conditions, appears to explain muscle phenomena central to locomotion but not readily explained by the crossbridge and sliding filament theories, such as history dependence, the energetics of cyclical contractions, the nonlinear effect of activation level on muscle performance and the effect of age on muscle and locomotor capacity.