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

Abstract

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.

Thermal robustness of biomechanical processes

“…For example, some animals rely on biting rather than fleeing as an anti-predator behavior at low body temperatures, presumably because bite force is determined by muscle force generation which has a relatively low Q 10 compared with the strong thermal effects on muscle power generation during running (Herrel et al, 2007;Hertz et al, 1982). Muscle rates that rely on physical properties, such as breaking cross-bridge bonds or stretching titin proteins within sarcomeres during eccentric activity (Holt, 2020;Lindstedt and Nishikawa, 2017), should be robust, whereas chemical processes that convert chemical to mechanical energy will be more thermally sensitive. Relatively low effects of temperature on isometric muscle force production (Berman, 1979) may also mean that behaviors that require muscle to act as a cable (Dickinson et al, 2000) are thermally robust.…”

Effects of Surface Properties on Gastrocnemius Medialis and Vastus Lateralis Fascicle Mechanics During Maximal Countermovement Jumping

“…Maximal vertical jumping performance mainly depends on the mechanical power generated by the lower limb muscle-tendon units (MTU) during the push-off phase ( Bobbert et al, 1986 ; Anderson and Pandy, 1993 ; Kurokawa et al, 2003 ; Farris et al, 2016 ; Nikolaidou et al, 2017 ; Wade et al, 2019 ). As such, jumping movement has been analyzed in light of muscle and tendon behaviors ( Bobbert et al, 1986 ; Anderson and Pandy, 1993 ; Kurokawa et al, 2003 ; Farris et al, 2016 ; Nikolaidou et al, 2017 ; Wade et al, 2019 ) and there is evidence for a decoupling mechanism between muscle fascicles and joint motion thanks to the compliance of the tendinous tissues ( Alexander, 1974 ; Holt, 2019 ). Specifically, tendinous tissues (connective tissues: extracellular matrix, aponeurosis, tendon) can act like springs by storing elastic strain energy and rapidly releasing it to power body movements ( Alexander and Bennet-Clark, 1977 ; Roberts, 2016 ).…”