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Muscle preflex response to perturbations in locomotion: In vitro experiments and simulations with realistic boundary conditions

Neuromuscular control loops feature substantial communication delays, but mammals run robustly even in the most adverse conditions. In vivo experiments and computer simulation results suggest that muscles’ preflex—an immediate mechanical response to a perturbation—could be the critical contributor....

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Autores principales: Araz, Matthew, Weidner, Sven, Izzi, Fabio, Badri-Spröwitz, Alexander, Siebert, Tobias, Haeufle, Daniel F. B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10194126/
https://www.ncbi.nlm.nih.gov/pubmed/37214305
http://dx.doi.org/10.3389/fbioe.2023.1150170
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author Araz, Matthew
Weidner, Sven
Izzi, Fabio
Badri-Spröwitz, Alexander
Siebert, Tobias
Haeufle, Daniel F. B.
author_facet Araz, Matthew
Weidner, Sven
Izzi, Fabio
Badri-Spröwitz, Alexander
Siebert, Tobias
Haeufle, Daniel F. B.
author_sort Araz, Matthew
collection PubMed
description Neuromuscular control loops feature substantial communication delays, but mammals run robustly even in the most adverse conditions. In vivo experiments and computer simulation results suggest that muscles’ preflex—an immediate mechanical response to a perturbation—could be the critical contributor. Muscle preflexes act within a few milliseconds, an order of magnitude faster than neural reflexes. Their short-lasting action makes mechanical preflexes hard to quantify in vivo. Muscle models, on the other hand, require further improvement of their prediction accuracy during the non-standard conditions of perturbed locomotion. Our study aims to quantify the mechanical work done by muscles during the preflex phase (preflex work) and test their mechanical force modulation. We performed in vitro experiments with biological muscle fibers under physiological boundary conditions, which we determined in computer simulations of perturbed hopping. Our findings show that muscles initially resist impacts with a stereotypical stiffness response—identified as short-range stiffness—regardless of the exact perturbation condition. We then observe a velocity adaptation to the force related to the amount of perturbation similar to a damping response. The main contributor to the preflex work modulation is not the change in force due to a change in fiber stretch velocity (fiber damping characteristics) but the change in magnitude of the stretch due to the leg dynamics in the perturbed conditions. Our results confirm previous findings that muscle stiffness is activity-dependent and show that also damping characteristics are activity-dependent. These results indicate that neural control could tune the preflex properties of muscles in expectation of ground conditions leading to previously inexplicable neuromuscular adaptation speeds.
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spelling pubmed-101941262023-05-19 Muscle preflex response to perturbations in locomotion: In vitro experiments and simulations with realistic boundary conditions Araz, Matthew Weidner, Sven Izzi, Fabio Badri-Spröwitz, Alexander Siebert, Tobias Haeufle, Daniel F. B. Front Bioeng Biotechnol Bioengineering and Biotechnology Neuromuscular control loops feature substantial communication delays, but mammals run robustly even in the most adverse conditions. In vivo experiments and computer simulation results suggest that muscles’ preflex—an immediate mechanical response to a perturbation—could be the critical contributor. Muscle preflexes act within a few milliseconds, an order of magnitude faster than neural reflexes. Their short-lasting action makes mechanical preflexes hard to quantify in vivo. Muscle models, on the other hand, require further improvement of their prediction accuracy during the non-standard conditions of perturbed locomotion. Our study aims to quantify the mechanical work done by muscles during the preflex phase (preflex work) and test their mechanical force modulation. We performed in vitro experiments with biological muscle fibers under physiological boundary conditions, which we determined in computer simulations of perturbed hopping. Our findings show that muscles initially resist impacts with a stereotypical stiffness response—identified as short-range stiffness—regardless of the exact perturbation condition. We then observe a velocity adaptation to the force related to the amount of perturbation similar to a damping response. The main contributor to the preflex work modulation is not the change in force due to a change in fiber stretch velocity (fiber damping characteristics) but the change in magnitude of the stretch due to the leg dynamics in the perturbed conditions. Our results confirm previous findings that muscle stiffness is activity-dependent and show that also damping characteristics are activity-dependent. These results indicate that neural control could tune the preflex properties of muscles in expectation of ground conditions leading to previously inexplicable neuromuscular adaptation speeds. Frontiers Media S.A. 2023-04-27 /pmc/articles/PMC10194126/ /pubmed/37214305 http://dx.doi.org/10.3389/fbioe.2023.1150170 Text en Copyright © 2023 Araz, Weidner, Izzi, Badri-Spröwitz, Siebert and Haeufle. 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 Bioengineering and Biotechnology
Araz, Matthew
Weidner, Sven
Izzi, Fabio
Badri-Spröwitz, Alexander
Siebert, Tobias
Haeufle, Daniel F. B.
Muscle preflex response to perturbations in locomotion: In vitro experiments and simulations with realistic boundary conditions
title Muscle preflex response to perturbations in locomotion: In vitro experiments and simulations with realistic boundary conditions
title_full Muscle preflex response to perturbations in locomotion: In vitro experiments and simulations with realistic boundary conditions
title_fullStr Muscle preflex response to perturbations in locomotion: In vitro experiments and simulations with realistic boundary conditions
title_full_unstemmed Muscle preflex response to perturbations in locomotion: In vitro experiments and simulations with realistic boundary conditions
title_short Muscle preflex response to perturbations in locomotion: In vitro experiments and simulations with realistic boundary conditions
title_sort muscle preflex response to perturbations in locomotion: in vitro experiments and simulations with realistic boundary conditions
topic Bioengineering and Biotechnology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10194126/
https://www.ncbi.nlm.nih.gov/pubmed/37214305
http://dx.doi.org/10.3389/fbioe.2023.1150170
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