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A Physiology-Guided Classification of Active-Stress and Active-Strain Approaches for Continuum-Mechanical Modeling of Skeletal Muscle Tissue

The well-established sliding filament and cross-bridge theory explain the major biophysical mechanism responsible for a skeletal muscle's active behavior on a cellular level. However, the biomechanical function of skeletal muscles on the tissue scale, which is caused by the complex interplay of...

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Autores principales: Klotz, Thomas, Bleiler, Christian, Röhrle, Oliver
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8365610/
https://www.ncbi.nlm.nih.gov/pubmed/34408657
http://dx.doi.org/10.3389/fphys.2021.685531
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author Klotz, Thomas
Bleiler, Christian
Röhrle, Oliver
author_facet Klotz, Thomas
Bleiler, Christian
Röhrle, Oliver
author_sort Klotz, Thomas
collection PubMed
description The well-established sliding filament and cross-bridge theory explain the major biophysical mechanism responsible for a skeletal muscle's active behavior on a cellular level. However, the biomechanical function of skeletal muscles on the tissue scale, which is caused by the complex interplay of muscle fibers and extracellular connective tissue, is much less understood. Mathematical models provide one possibility to investigate physiological hypotheses. Continuum-mechanical models have hereby proven themselves to be very suitable to study the biomechanical behavior of whole muscles or entire limbs. Existing continuum-mechanical skeletal muscle models use either an active-stress or an active-strain approach to phenomenologically describe the mechanical behavior of active contractions. While any macroscopic constitutive model can be judged by it's ability to accurately replicate experimental data, the evaluation of muscle-specific material descriptions is difficult as suitable data is, unfortunately, currently not available. Thus, the discussions become more philosophical rather than following rigid methodological criteria. Within this work, we provide a extensive discussion on the underlying modeling assumptions of both the active-stress and the active-strain approach in the context of existing hypotheses of skeletal muscle physiology. We conclude that the active-stress approach resolves an idealized tissue transmitting active stresses through an independent pathway. In contrast, the active-strain approach reflects an idealized tissue employing an indirect, coupled pathway for active stress transmission. Finally the physiological hypothesis that skeletal muscles exhibit redundant pathways of intramuscular stress transmission represents the basis for considering a mixed-active-stress-active-strain constitutive framework.
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spelling pubmed-83656102021-08-17 A Physiology-Guided Classification of Active-Stress and Active-Strain Approaches for Continuum-Mechanical Modeling of Skeletal Muscle Tissue Klotz, Thomas Bleiler, Christian Röhrle, Oliver Front Physiol Physiology The well-established sliding filament and cross-bridge theory explain the major biophysical mechanism responsible for a skeletal muscle's active behavior on a cellular level. However, the biomechanical function of skeletal muscles on the tissue scale, which is caused by the complex interplay of muscle fibers and extracellular connective tissue, is much less understood. Mathematical models provide one possibility to investigate physiological hypotheses. Continuum-mechanical models have hereby proven themselves to be very suitable to study the biomechanical behavior of whole muscles or entire limbs. Existing continuum-mechanical skeletal muscle models use either an active-stress or an active-strain approach to phenomenologically describe the mechanical behavior of active contractions. While any macroscopic constitutive model can be judged by it's ability to accurately replicate experimental data, the evaluation of muscle-specific material descriptions is difficult as suitable data is, unfortunately, currently not available. Thus, the discussions become more philosophical rather than following rigid methodological criteria. Within this work, we provide a extensive discussion on the underlying modeling assumptions of both the active-stress and the active-strain approach in the context of existing hypotheses of skeletal muscle physiology. We conclude that the active-stress approach resolves an idealized tissue transmitting active stresses through an independent pathway. In contrast, the active-strain approach reflects an idealized tissue employing an indirect, coupled pathway for active stress transmission. Finally the physiological hypothesis that skeletal muscles exhibit redundant pathways of intramuscular stress transmission represents the basis for considering a mixed-active-stress-active-strain constitutive framework. Frontiers Media S.A. 2021-08-02 /pmc/articles/PMC8365610/ /pubmed/34408657 http://dx.doi.org/10.3389/fphys.2021.685531 Text en Copyright © 2021 Klotz, Bleiler and Röhrle. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Klotz, Thomas
Bleiler, Christian
Röhrle, Oliver
A Physiology-Guided Classification of Active-Stress and Active-Strain Approaches for Continuum-Mechanical Modeling of Skeletal Muscle Tissue
title A Physiology-Guided Classification of Active-Stress and Active-Strain Approaches for Continuum-Mechanical Modeling of Skeletal Muscle Tissue
title_full A Physiology-Guided Classification of Active-Stress and Active-Strain Approaches for Continuum-Mechanical Modeling of Skeletal Muscle Tissue
title_fullStr A Physiology-Guided Classification of Active-Stress and Active-Strain Approaches for Continuum-Mechanical Modeling of Skeletal Muscle Tissue
title_full_unstemmed A Physiology-Guided Classification of Active-Stress and Active-Strain Approaches for Continuum-Mechanical Modeling of Skeletal Muscle Tissue
title_short A Physiology-Guided Classification of Active-Stress and Active-Strain Approaches for Continuum-Mechanical Modeling of Skeletal Muscle Tissue
title_sort physiology-guided classification of active-stress and active-strain approaches for continuum-mechanical modeling of skeletal muscle tissue
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8365610/
https://www.ncbi.nlm.nih.gov/pubmed/34408657
http://dx.doi.org/10.3389/fphys.2021.685531
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