A multiscale chemo-electro-mechanical skeletal muscle model to analyze muscle contraction and force generation for different muscle fiber arrangements.

Thomas Heidlauf,Oliver Röhrle

doi:10.3389/fphys.2014.00498

Thomas Heidlauf, Oliver Röhrle

Open Access

https://doi.org/10.3389/fphys.2014.00498

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Abstract

The presented chemo-electro-mechanical skeletal muscle model relies on a continuum-mechanical formulation describing the muscle's deformation and force generation on the macroscopic muscle level. Unlike other three-dimensional models, the description of the activation-induced behavior of the mechanical model is entirely based on chemo-electro-mechanical principles on the microscopic sarcomere level. Yet, the multiscale model reproduces key characteristics of skeletal muscles such as experimental force-length and force-velocity data on the macroscopic whole muscle level. The paper presents the methodological approaches required to obtain such a multiscale model, and demonstrates the feasibility of using such a model to analyze differences in the mechanical behavior of parallel-fibered muscles, in which the muscle fibers either span the entire length of the fascicles or terminate intrafascicularly. The presented results reveal that muscles, in which the fibers span the entire length of the fascicles, show lower peak forces, more dispersed twitches and fusion of twitches at lower stimulation frequencies. In detail, the model predicted twitch rise times of 38.2 and 17.2 ms for a 12 cm long muscle, in which the fibers span the entire length of the fascicles and with twelve fiber compartments in series, respectively. Further, the twelve-compartment model predicted peak twitch forces that were 19% higher than in the single-compartment model. The analysis of sarcomere lengths during fixed-end single twitch contractions at optimal length predicts rather small sarcomere length changes. The observed lengths range from 75 to 111% of the optimal sarcomere length, which corresponds to a region with maximum filament overlap. This result suggests that stability issues resulting from activation-induced stretches of non-activated sarcomeres are unlikely in muscles with passive forces appearing at short muscle length.

Highlights

The fascicles in parallel-fibered muscle are aligned with the muscle’s line of action and run almost the entire length of the muscle (Loeb et al, 1987)
To investigate the effect of different fiber arrangements, one requires a model that unifies the following features: (i) The dynamics of the active force generation are determined at discrete locations (“sarcomeres”) along a muscle fiber. (ii) The model takes into account the subsequent activation of adjacent “sarcomeres” through the propagation of action potentials (APs) along the fibers
The multiscale model proved to be able to reveal differences in the muscle contraction and force generation that result from the muscle fiber arrangement

Summary

Introduction

The fascicles in parallel-fibered muscle are aligned with the muscle’s line of action and run almost the entire length of the muscle (Loeb et al, 1987). (ii) The model takes into account the subsequent activation of adjacent “sarcomeres” through the propagation of action potentials (APs) along the fibers. To investigate the effect of different fiber arrangements, one requires a model that unifies the following features: (i) The dynamics of the active force generation are determined at discrete locations (“sarcomeres”) along a muscle fiber. This is required since the AP propagation speed is rather slow, and sarcomere activation is non-synchronized along a muscle fiber, and the asynchronism increases with increasing fiber length. This is required since the AP propagation speed is rather slow, and sarcomere activation is non-synchronized along a muscle fiber, and the asynchronism increases with increasing fiber length. (iii) The model accounts www.frontiersin.org

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