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

Abstract

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.