Muscle performance during frog jumping: influence of elasticity on muscle operating lengths

Abstract

A fundamental feature of vertebrate muscle is that maximal force can be generated only over a limited range of lengths. It has been proposed that locomotor muscles operate over this range of lengths in order to maximize force production during movement. However, locomotor behaviours like jumping may require muscles to shorten substantially in order to generate the mechanical work necessary to propel the body. Thus, the muscles that power jumping may need to shorten to lengths where force production is submaximal. Here we use direct measurements of muscle length in vivo and muscle force-length relationships in vitro to determine the operating lengths of the plantaris muscle in bullfrogs (Rana catesbeiana) during jumping. We find that the plantaris muscle operates primarily on the descending limb of the force-length curve, resting at long initial lengths (1.3 + 0.06 L o ) before shortening to muscle's optimal length (1.03 + 0.05 L o ). We also compare passive force-length curves from frogs with literature values for mammalian muscle, and demonstrate that frog muscles must be stretched to much longer lengths before generating passive force. The relatively compliant passive properties of frog muscles may be a critical feature of the system, because it allows muscles to operate at long lengths and improves muscles' capacity for force production during a jump.

On the ascent: the soleus operating length is conserved to the ascending limb of the force-length curve across gait mechanics in humans

“…Our results show that the length at which passive SOL forces begin to develop correspond closely to the predicted L 0 , corroborating both standard models (Zajac, 1989) and previous experimental data (Azizi and Roberts, 2010;Winters et al, 2011), and provides further confidence in our estimates of subject-specific F-L data. The close association between the length at the initiation of passive force and L 0 may provide a convenient and less experimentally intensive approach to establishing subject-specific muscle properties for both experimental and computer simulation studies of human muscle function.…”

“…Our estimates of the passive F-L curves of the SOL fascicles were consistently less steep than the theoretical model (Fig.4) and compared to those from other mammalian species (Azizi and Roberts, 2010), despite the peak passive muscle forces and stiffness being commensurate with those reported for the human gastrocnemius muscle (Hoang et al, 2007;Gao et al, 2009) (taking into account muscle cross-sectional area). Our results show that the length at which passive SOL forces begin to develop correspond closely to the predicted L 0 , corroborating both standard models (Zajac, 1989) and previous experimental data (Azizi and Roberts, 2010;Winters et al, 2011), and provides further confidence in our estimates of subject-specific F-L data.…”

Comparison of the validity of Hill and Huxley muscle tendon complex models using experimental data obtained from rat m. soleus in situ

“…in patientspecific modelling). However, Hill models have been successfully applied in musculoskeletal models aimed at addressing conceptual questions regarding design and control of the motor system (Van Soest et al, 1993;Bobbert, 2012;Azizi and Roberts, 2010;Richards and Clemente, 2012;Kistemaker et al, 2007;Lichtwark and Wilson, 2007). Given the similarity in predicted behaviour of the Hill and Huxley MTC models in the present study, it stands to reason that the Huxley model could at least be applied in a similar fashion.…”

“…Musculoskeletal models using the Hill model have been successfully applied to study phenomena in which only mechanical behaviour is considered (e.g. Van Soest et al, 1993;Bobbert, 2012;Azizi and Roberts, 2010;Lai et al, 2014). However, in the Hill model, a direct relationship between metabolic and mechanical behaviour is absent.…”

The extraordinary athletic performance of leaping gibbons

“…the power-amplifying mechanisms of galagos [1], froghoppers [2], fleas [3] and locusts [4]), and the distance over which force is applied (e.g. the elongated distal leg segments of galagos [5] and frogs [6], the manipulation of the force-length characteristics of anuran leg muscle [7]). Adaptations such as these are synonymous with maximizing mechanical work and improving leap performance.…”