Cross-Bridges and Sarcomeric Non-cross-bridge Structures Contribute to Increased Work in Stretch-Shortening Cycles

Abstract

Stretch-shortening cycles (SSCs) refer to the muscle action when an active muscle stretch is immediately followed by active muscle shortening. This combination of eccentric and concentric contractions is the most important type of daily muscle action and plays a significant role in natural locomotion such as walking, running or jumping. SSCs are used in human and animal movements especially when a high movement speed or economy is required. A key feature of SSCs is the increase in muscular force and work during the concentric phase of a SSC by more than 50% compared with concentric muscle actions without prior stretch (SSC-effect). This improved muscle capability is related to various mechanisms, including pre-activation, stretch-reflex responses and elastic recoil from serial elastic tissues. Moreover, it is assumed that a significant contribution to enhanced muscle capability lies in the sarcomeres itself. Thus, we investigated the force output and work produced by single skinned fibers of rat soleus muscles during and after ramp contractions at a constant velocity. Shortening, lengthening, and SSCs were performed under physiological boundary conditions with 85% of the maximum shortening velocity and stretch-shortening magnitudes of 18% of the optimum muscle length. The different contributions of cross-bridge (XB) and non-cross-bridge (non-XB) structures to the total muscle force were identified by using Blebbistatin. The experiments revealed three main results: (i) partial detachment of XBs during the eccentric phase of a SSC, (ii) significantly enhanced forces and mechanical work during the concentric phase of SSCs compared with shortening contractions with and without XB-inhibition, and (iii) no residual force depression after SSCs. The results obtained by administering Blebbistatin propose a titin-actin interaction that depends on XB-binding or active XB-based force production. The findings of this study further suggest that enhanced forces generated during the active lengthening phase of SSCs persist during the subsequent shortening phase, thereby contributing to enhanced

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

“…Muscle preparation, storage, and activation techniques for permeabilized single muscle fibers were in line with Tomalka et al (2017Tomalka et al ( , 2020. Briefly, experiments were performed on glycerinated skinned single fiber segments from soleus muscles of six freshly killed female Wistar rats (age: 3 months, weight: 428-520 g, cage-sedentary, 12-12 h light: dark cycle, housingtemperature: 22 • C).…”

“…An SSC-effect of about 30% of work enhancement relative to pure shortening was reported for slow stretch-shortening velocities [about 10% maximum shortening velocity (v 0 )] and long muscle fiber lengths [2.4-3.3 µm, descending limb of the force-length relation (F-lr)] of skinned rabbit soleus muscle fibers (Fukutani et al, 2017a;Fukutani and Herzog, 2019). Tomalka et al (2020) demonstrated that the SSC-effect in skinned rat soleus muscle fibers also occurs in the more physiological working range (plateau region and ascending limb of the F-l-r) at fast contraction velocities (∼85% v 0 ). Mechanisms related to activation dynamics, reflex activity, and elastic recoil from tendons-as discussed for in vivo muscle action-cannot be responsible for the SSC-effect in skinned muscle fiber experiments.…”

Energy Cost of Force Production After a Stretch-Shortening Cycle in Skinned Muscle Fibers: Does Muscle Efficiency Increase?

“…Therefore, an increase in cross-bridge recruitment would not occur in the stretch phase of the SSCs but would have to occur in the shortening phase. A plausible explanation for a reduced inhibition of cross-bridge formation during the shortening phase of SSC was suggested by Fortuna et al (2019) and further supported by Tomalka et al (2020) . These authors argued that in pure shortening contractions, work is produced primarily by cross-bridges, while in SSC contractions, a substantial amount of the shortening work is produced by the recoil of the passive structures that elongated during the stretch phase of the SSCs ( Fortuna et al, 2019 ).…”

Evidence for Muscle Cell-Based Mechanisms of Enhanced Performance in Stretch-Shortening Cycle in Skeletal Muscle

“…Thus, it is reasonable to assume that contributions to the SSC effect not produced by cross-bridges, for example titin, become more prominent in reduced force states. This hypothesis has been tested using a myosin inhibitor, blebbistatin, and it was found that the SSC effect was still observed even though the active force was substantially decreased ( Tomalka et al, 2020 ). Similarly, temperature may affect the SSC effect.…”