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.
Highlights
During concentric muscle contraction, the force generated during shortening decreases nonlinearly as the shortening velocity increases
Force increased with increasingly faster lengthening velocities up to ~0.75 muscle lengths/second (ML/s), above which force plateaued at values 40–50% greater than isometric force
Force decreased in a hyperbolic manner until the maximal unloaded shortening velocity reached -3.31 ML/s (Fig 3A, Table 1)
Summary
The force generated during shortening decreases nonlinearly as the shortening velocity increases. Forced-lengthening of a contracting muscle (i.e. eccentric contraction) at loads that are greater than that of isometric contraction results in a rapid rise in force [1]. This classic signature of muscle contraction is known as the force-velocity relationship [2,3]. While no external work is performed by the muscle at Vmax, the continued consumption of chemical energy means that the system efficiency approaches zero [5] These observations suggest that contracting muscles must balance power output and efficiency during lengthening and shortening transients that facilitate locomotion. The molecular mechanisms that underlie these coupled relationships of force, velocity, and energy utilization remain unclear
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