The sarcomere force-length relationship in an intact muscle-tendon unit

Abstract

The periodic striation pattern in skeletal muscle reflects the length of the basic contractile unit: the sarcomere. More than half a century ago, Gordon, Huxley and Julian provided strong support for the 'sliding filament' theory through experiments with single muscle fibres. The sarcomere force-length (FL) relationship has since been extrapolated to whole muscles in an attempt to unravel in vivo muscle function. However, these extrapolations were frequently associated with nontrivial assumptions, such as muscle length changes corresponding linearly to SL changes. Here, we determined the in situ sarcomere FL relationship in a whole muscle preparation by simultaneously measuring muscle force and individual SLs in an intact muscle-tendon unit (MTU) using state-of-the-art multi-photon excitation microscopy. We found that despite great SL non-uniformity, the mean value of SLs measured from a minute volume of the mid-belly, equivalent to about 5×10 −6 % of the total muscle volume, agrees well with the theoretically predicted FL relationship, but only if the precise contractile filament lengths are known, and if passive forces from parallel elastic components and activation-associated sarcomere shortening are considered properly. As SLs are not uniformly distributed across the whole muscle and changes in SL with muscle length are location dependent, our results may not be valid for the proximal or distal parts of the muscle. The approach described here, and our findings, may encourage future studies to determine the role of SL non-uniformity in influencing sarcomere FL properties in different muscles and for different locations within single muscles.

A data-driven analysis of fiber type architecture over the entire muscle

“…The observed asymmetry of geometrical features of myo bers along the entire muscle is consistent with biomechanical models of the TA muscle (Heemskerk et al, 2005;Lovering et al, 2013;Moo et al, 2016). Moo et al, also measured sarcomere force at the median region of a muscle and stressed that their ndings may not be valid to other muscle regions, especially where myo ber lengths in not uniform (Moo et al, 2020). Under the assumption that we aim to describe major changes along the muscle, we applied a smoothed regression line to describe changes in myo ber features along the muscle.…”

“…The impact of myo ber type on muscle physiology and function has been mostly interpreted from cross sections at the median part of the muscle. Several reports reinforced the importance to sample the entire muscle in order to understand how myo ber architecture affects muscle function (Moo et al, 2020;Stark and Schilling, 2010). In contrast to previous studies (Dickinson et al, 2018;Heemskerk et al, 2005; Moo et al, 2020; Nyakatura et al, 2019; Stark and Schilling, 2010), we also considered the spatial organization of myo ber types over the entire muscle.…”

“…This indicates an asymmetric myo ber architecture along the muscle. Ex-vivo measurements of sarcomere force-length demonstrated that the muscle ber architecture affects its biomechanical properties (Moo et al, 2020). Ex-vivo procedures of muscle architecture can in uence the shape of the muscle during the following procedures: 1. pulling when dissecting the muscle out of the mouse.…”

“…A simulation of muscle movement has been suggested using architectural models, suggested that even in a muscle with a parallel muscle ber arrangement, as the tibialis anterior (TA), the contraction is not symmetric along the muscle longitudinal axis (Moo et al, 2016;Moo et al, 2020;Otten, 1988; Leeuwen and Spoor, 1992). The tibialis anterior (TA) connects the knee to the foot, mobilizing the lower leg (Mathewson et al, 2012).…”

Sarcomere Lengths Become More Uniform Over Time in Intact Muscle-Tendon Unit During Isometric Contractions

“…The analysis of the current study was based on a data set previously published for a different purpose and using different analysis procedures (Moo et al, 2020).…”