Effects of cross-bridge compliance on the force-velocity relationship and muscle power output

Abstract

Muscles produce force and power by utilizing chemical energy through ATP hydrolysis. During concentric contractions (shortening), muscles generate less force compared to isometric contractions, but consume greater amounts of energy as shortening velocity increases. Conversely, more force is generated and less energy is consumed during eccentric muscle contractions (lengthening). This relationship between force, energy use, and the velocity of contraction has important implications for understanding muscle efficiency, but the molecular mechanisms underlying this behavior remain poorly understood. Here we used spatially-explicit, multi-filament models of Ca2+-regulated force production within a half-sarcomere to simulate how force production, energy utilization, and the number of bound cross-bridges are affected by dynamic changes in sarcomere length. These computational simulations show that cross-bridge binding increased during slow-velocity concentric and eccentric contractions, compared to isometric contractions. Over the full ranges of velocities that we simulated, cross-bridge cycling and energy utilization (i.e. ATPase rates) increased during shortening, and decreased during lengthening. These findings are consistent with the Fenn effect, but arise from a complicated relationship between velocity-dependent cross-bridge recruitment and cross-bridge cycling kinetics. We also investigated how force production, power output, and energy utilization varied with cross-bridge and myofilament compliance, which is impossible to address under typical experimental conditions. These important simulations show that increasing cross-bridge compliance resulted in greater cross-bridge binding and ATPase activity, but less force was generated per cross-bridge and throughout the sarcomere. These data indicate that the efficiency of force production decreases in a velocity-dependent manner, and that this behavior is sensitive to cross-bridge compliance. In contrast, significant effects of myofilament compliance on force production were only observed during isometric contractions, suggesting that changes in myofilament compliance may not influence power output during non-isometric contractions as greatly as changes in cross-bridge compliance. These findings advance our understanding of how cross-bridge and myofilament properties underlie velocity-dependent changes in contractile efficiency during muscle movement.

Dietary nitrate supplementation increases diaphragm peak power in old mice

“…Interestingly, the increase in cross‐bridge compliance results in higher efficiency of cross‐bridge cycling and muscle shortening with no effect on maximal specific force (Fenwick et al . 2017); these observations are in line with the nitrate supplementation effects on exercise efficiency (Bailey et al . 2009; Larsen et al .…”

“…A compromise of increased cross‐bridge compliance is a decrease in the force per cross‐bridge at submaximal shortening velocity, but to a lesser extent than the rise in number of attached cross‐bridges (Fenwick et al . 2017). The net effect is an increased overall force and mechanical power for a given submaximal velocity of shortening.…”

Sprint force-velocity profiles in soccer players: impact of sex and playing level

“…Ideally, both high forces and high velocities are generated to maximise Pmax. However, the ability of the muscles to generate force decreases at high velocities (Fenwick, Wood & Tanner, 2017). Measurements of force and velocity outputs during sprinting show that at the beginning of a maximal sprint, the sprinter generates high amounts of force at a low velocity to accelerate the body forwards (Morin, Edouard & Samozino, 2011), while as the running velocity increases over time, the force output decreases.…”

Neural/Bayes network predictor for inheritable cardiac disease pathogenicity and phenotype

“…The recognition that cardiac myosin is to a large extent autonomous implies that consequential myosin characteristics embodied in a structure/function model are contained within the macromolecule such that myosin structure is the sole determinate of function. In this case, a specific missense SNP performs a predictable functional modification independent of the context like striated muscle [33], focal adhesion [34], or in vitro motility [35]. Unlike myosin, mybpc3 is not believed to function outside the sarcomere and its structure/function model implicitly includes sarcomeric constraints.…”