Power Amplification Increases With Contraction Velocity During Stretch-Shortening Cycles of Skinned Muscle Fibers.

André Tomalka,Tobias Siebert,Wolfgang Seiberl,Daniel Hahn,Sven Weidner

doi:10.3389/fphys.2021.644981

Abstract

Muscle force, work, and power output during concentric contractions (active muscle shortening) are increased immediately following an eccentric contraction (active muscle lengthening). This increase in performance is known as the stretch-shortening cycle (SSC)-effect. Recent findings demonstrate that the SSC-effect is present in the sarcomere itself. More recently, it has been suggested that cross-bridge (XB) kinetics and non-cross-bridge (non-XB) structures (e.g., titin and nebulin) contribute to the SSC-effect. As XBs and non-XB structures are characterized by a velocity dependence, we investigated the impact of stretch-shortening velocity on the SSC-effect. Accordingly, we performed in vitro isovelocity ramp experiments with varying ramp velocities (30, 60, and 85% of maximum contraction velocity for both stretch and shortening) and constant stretch-shortening magnitudes (17% of the optimum sarcomere length) using single skinned fibers of rat soleus muscles. The different contributions of XB and non-XB structures to force production were identified using the XB-inhibitor Blebbistatin. We show that (i) the SSC-effect is velocity-dependent—since the power output increases with increasing SSC-velocity. (ii) The energy recovery (ratio of elastic energy storage and release in the SSC) is higher in the Blebbistatin condition compared with the control condition. The stored and released energy in the Blebbistatin condition can be explained by the viscoelastic properties of the non-XB structure titin. Consequently, our experimental findings suggest that the energy stored in titin during the eccentric phase contributes to the SSC-effect in a velocity-dependent manner.

Highlights

The most common form of muscle action during terrestrial locomotion is characterized by eccentric muscle action immediately followed by concentric muscle action
We show that (i) the stretch-shortening cycle (SSC)-effect is velocity-dependent—since the power output increases with increasing SSC-velocity. (ii) The energy recovery is higher in the Blebbistatin condition compared with the control condition
We found work and power amplification in the shortening phase of SSCs in control- and Blebbistatin conditions

Summary

Introduction

The most common form of muscle action during terrestrial locomotion is characterized by eccentric muscle action (active lengthening) immediately followed by concentric muscle action (active shortening). A large number of experiments at the level of the muscletendon unit have shown an increase in muscle force, work, and power output during the shortening phase of SSCs compared with pure shortening contractions (Cavagna et al, 1968; Bosco et al, 1981; Gregor et al, 1988; Seiberl et al, 2015). This SSCeffect (i.e., increased muscular performance) is further associated with amplified muscular efficiency accompanied by reduced metabolic energy consumption (Cavagna et al, 1968; Holt et al, 2014). Using Blebbistatin for XB-inhibition, Tomalka et al (2020) further showed that both XBs- and non-XB structures contribute to the SSC-effect on the skinned muscle fiber level, which is supported by other studies (Fukutani et al, 2017a; Fukutani and Herzog, 2020a)

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Discussion

Conclusion