Timing matters: tuning the mechanics of a muscle-tendon unit by adjusting stimulation phase during cyclic contractions

Abstract

A growing body of research on the mechanics and energetics of terrestrial locomotion has demonstrated that elastic elements acting in series with contracting muscle are critical components of sustained, stable, and efficient gait. Far fewer studies have examined how the nervous system modulates muscle-tendon interaction dynamics to optimize ‘tuning’ or meet varying locomotor demands. To explore the fundamental neuromechanical rules that govern the interactions between series elastic (SEE) and contractile (CE) elements within a compliant muscle-tendon unit (MTU), we used a novel work loop approach that included implanted sonomicrometry crystals along muscle fascicles. This enabled us to de-couple CE and SEE length trajectories when cyclic strain patterns were applied to an isolated plantaris MTU from the bullfrog (Lithobates catesbeianus). Using this approach, we demonstrate that the onset timing of muscle stimulation (i.e., stimulation phase) that involves a symmetrical MTU stretch-shorten cycle during active force production, results in net zero mechanical power output, and maximal decoupling of CE and MTU length trajectories. We found it difficult to ‘tune’ the muscle-tendon system for strut-like isometric force production by adjusting stimulation phase only, as the zero power output condition involved significant positive and negative mechanical work by the CE. A simple neural mechanism- adjusting muscle stimulation phase- could shift a MTU from performing net zero to net positive (energy producing) or net negative (energy absorbing) mechanical work under conditions of changing locomotor demand. Finally, we show that modifications to the classical work loop paradigm better represent in vivo muscle-tendon function during locomotion.