Uniform strain in broad muscles: active and passive effects of the twisted tendon of the spotted ratfish Hydrolagus colliei

Abstract

SUMMARY A muscle's force output depends on the range of lengths over which its fibers operate. Regional variation in fiber shortening during muscle contraction may translate into suboptimal force production if a subset of muscle fibers operates outside the plateau of the length–tension curve. Muscles with broad insertions and substantial shortening are particularly prone to heterogeneous strain patterns since fibers from different regions of the muscle vary in their moment arms, with fibers further from the joint exhibiting greater strains. In the present study, we describe a musculotendon morphology that serves to counteract the variation in moment arm and fiber strains that are inherent in broad muscles. The tendon of the anterior jaw adductor of the spotted ratfish Hydrolagus colliei is twisted such that the distal face of the muscle inserts more proximally than the proximal face. Using quantitative geometric models based on this natural morphology, we show that this inversion of insertion points serves to equalize strains across the muscle such that at any gape angle all fibers in the muscle are operating at similar positions on their length–tension curves. Manipulations of this geometric model show that the natural morphology is `ideal' compared to other hypothetical morphologies for limiting fiber strain heterogeneity. The uniform strain patterns predicted for this morphology could increase active force production during jaw closing and also decrease passive resistance to jaw opening. This divergence from `typical' tendon morphology in the jaw adductors of H. colliei may be particularly important given the demands for high force production in durophagy.

The twisted structure of the human Achilles tendon

“…Dean et al. () reported that muscle groups in different sites act within the same range during joint movement and can exhibit force with good efficiency due to the twist of broad muscle tendons. They also stated that the twisted structure is important in order to reduce different strains within a tendon so that the muscle exhibits force efficiently.…”

“…In addition, the triceps surae have a complex three-dimensional structure (Edama et al, 2014), so that elucidation of the three-dimensional structure of the AT will also be necessary. Dean et al (2007) reported that muscle groups in different sites act within the same range during joint movement and can exhibit force with good efficiency due to the twist of broad muscle tendons. They also stated that the twisted structure is important in order to reduce different strains within a tendon so that the muscle exhibits force efficiently.…”

“…In recent years many studies have been reported that focus on the mechanical characteristics produced by this distinguishing structure. Dean et al (2007) reported that, due to the twist in a wide range of muscle tendons, muscle groups in different locations work in the same range during joint movement and display force with good efficiency. They also reported that this is important in reducing various strains within the tendon so that the muscle can displace force efficiently.…”

Myological variability in a decoupled skeletal system: Batoid cranial anatomy

“…In durophagous taxa, however, a more robust jaw skeleton (stiffened by cortical thickening and trabecular internal reinforcement; Summers, ) coupled with fusion of certain skeletal elements (i.e., jaw symphyses) makes aponeurotic insertions unnecessary. These direct tendinous insertions are more amenable to efficient force transfer (Dean et al, ) across a rigid (jaw) structure and reduce the area needed for muscles to attach. Analysis of correlations among muscle activity, skeletal strains during natural feeding behaviors, and muscle attachment morphologies in these animals will help to elucidate basic form‐function relationships in elasmobranch skeletal anatomy, which remain woefully understudied.…”

Regional heterogeneity in muscle fiber strain: the role of fiber architecture

“…Muscles with broad insertions can face large variation in strain if one edge of a muscle acts with a significantly different moment arm relative to the joint's center of rotation. As a result, fibers with smaller moment arms are likely to undergo relatively smaller excursions while fibers further form the joint are likely to undergo relatively large excursions (Herring et al, 1979; Van Der Helm and Veenbaas, 1991; Dean et al, 2007). Variation in fiber strain may also affect muscles with relatively simple architecture.…”