Load sharing between synergistic muscles characterized by a ligand-binding approach and elastography

Abstract The skeletal muscle contraction is determined by cross-bridge formation between the myosin heads and the actin active sites. When the muscle contracts, it shortens, increasing its longitudinal shear elastic modulus ( $${\mu }_{L}$$ μ L ). Structurally, skeletal muscle can be considered anal...

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Main Authors: Gustavo A. Grinspan, Liliam Fernandes de Oliveira, Maria Clara Brandao, Andrés Pomi, Nicolás Benech
Format: Article
Language:English
Published: Nature Portfolio 2023-10-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-45037-y
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author Gustavo A. Grinspan
Liliam Fernandes de Oliveira
Maria Clara Brandao
Andrés Pomi
Nicolás Benech
author_facet Gustavo A. Grinspan
Liliam Fernandes de Oliveira
Maria Clara Brandao
Andrés Pomi
Nicolás Benech
author_sort Gustavo A. Grinspan
collection DOAJ
description Abstract The skeletal muscle contraction is determined by cross-bridge formation between the myosin heads and the actin active sites. When the muscle contracts, it shortens, increasing its longitudinal shear elastic modulus ( $${\mu }_{L}$$ μ L ). Structurally, skeletal muscle can be considered analogous to the molecular receptors that form receptor–ligand complexes and exhibit specific ligand-binding dynamics. In this context, this work aims to apply elastography and the ligand-binding framework to approach the possible intrinsic mechanisms behind muscle synergism. Based on the short-range stiffness principle and the acoustic–elasticity theory, we define the coefficient $$C$$ C , which is directly related to the fraction saturation of molecular receptors and links the relative longitudinal deformation of the muscle to its $${\mu }_{L}$$ μ L . We show that such a coefficient can be obtained directly from $${\mu }_{L}$$ μ L estimates, thus calculating it for the biceps brachii, brachioradialis, and brachialis muscles during isometric elbow flexion torque (τ) ramps. The resulting $$C\left(\tau \right)$$ C τ curves were analyzed by conventional characterization methods of receptor–ligand systems to study the dynamical behavior of each muscle. The results showed that, depending on muscle, $$C\left(\tau \right)$$ C τ exhibits typical ligand-binding dynamics during joint torque production. Therefore, the above indicates that these different behaviors describe the longitudinal shortening pattern of each muscle during load sharing. As a plausible interpretation, we suggested that this could be related to the binding kinetics of the cross-bridges during their synergistic action as torque increases. Likewise, it shows that elastography could be useful to assess contractile processes at different scales related to the change in the mechanical properties of skeletal muscle.
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spelling doaj.art-90e3341b261c465dbb34c94f82b9bebb2023-11-20T09:12:34ZengNature PortfolioScientific Reports2045-23222023-10-0113111410.1038/s41598-023-45037-yLoad sharing between synergistic muscles characterized by a ligand-binding approach and elastographyGustavo A. Grinspan0Liliam Fernandes de Oliveira1Maria Clara Brandao2Andrés Pomi3Nicolás Benech4Sección Biofísica y Biología de Sistemas, Facultad de Ciencias, Universidad de la RepúblicaLaboratório de Análise do Movimento e Fisiologia do Exercício, Programa de Engenharia Biomédica, Universidade Federal do Rio de JaneiroLaboratório de Análise do Movimento e Fisiologia do Exercício, Programa de Engenharia Biomédica, Universidade Federal do Rio de JaneiroSección Biofísica y Biología de Sistemas, Facultad de Ciencias, Universidad de la RepúblicaLaboratorio de Acústica Ultrasonora, Facultad de Ciencias, Universidad de la RepúblicaAbstract The skeletal muscle contraction is determined by cross-bridge formation between the myosin heads and the actin active sites. When the muscle contracts, it shortens, increasing its longitudinal shear elastic modulus ( $${\mu }_{L}$$ μ L ). Structurally, skeletal muscle can be considered analogous to the molecular receptors that form receptor–ligand complexes and exhibit specific ligand-binding dynamics. In this context, this work aims to apply elastography and the ligand-binding framework to approach the possible intrinsic mechanisms behind muscle synergism. Based on the short-range stiffness principle and the acoustic–elasticity theory, we define the coefficient $$C$$ C , which is directly related to the fraction saturation of molecular receptors and links the relative longitudinal deformation of the muscle to its $${\mu }_{L}$$ μ L . We show that such a coefficient can be obtained directly from $${\mu }_{L}$$ μ L estimates, thus calculating it for the biceps brachii, brachioradialis, and brachialis muscles during isometric elbow flexion torque (τ) ramps. The resulting $$C\left(\tau \right)$$ C τ curves were analyzed by conventional characterization methods of receptor–ligand systems to study the dynamical behavior of each muscle. The results showed that, depending on muscle, $$C\left(\tau \right)$$ C τ exhibits typical ligand-binding dynamics during joint torque production. Therefore, the above indicates that these different behaviors describe the longitudinal shortening pattern of each muscle during load sharing. As a plausible interpretation, we suggested that this could be related to the binding kinetics of the cross-bridges during their synergistic action as torque increases. Likewise, it shows that elastography could be useful to assess contractile processes at different scales related to the change in the mechanical properties of skeletal muscle.https://doi.org/10.1038/s41598-023-45037-y
spellingShingle Gustavo A. Grinspan
Liliam Fernandes de Oliveira
Maria Clara Brandao
Andrés Pomi
Nicolás Benech
Load sharing between synergistic muscles characterized by a ligand-binding approach and elastography
Scientific Reports
title Load sharing between synergistic muscles characterized by a ligand-binding approach and elastography
title_full Load sharing between synergistic muscles characterized by a ligand-binding approach and elastography
title_fullStr Load sharing between synergistic muscles characterized by a ligand-binding approach and elastography
title_full_unstemmed Load sharing between synergistic muscles characterized by a ligand-binding approach and elastography
title_short Load sharing between synergistic muscles characterized by a ligand-binding approach and elastography
title_sort load sharing between synergistic muscles characterized by a ligand binding approach and elastography
url https://doi.org/10.1038/s41598-023-45037-y
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AT mariaclarabrandao loadsharingbetweensynergisticmusclescharacterizedbyaligandbindingapproachandelastography
AT andrespomi loadsharingbetweensynergisticmusclescharacterizedbyaligandbindingapproachandelastography
AT nicolasbenech loadsharingbetweensynergisticmusclescharacterizedbyaligandbindingapproachandelastography