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Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics

Despite decades of research, we lack a mechanistic framework capable of predicting how movement-related signals are transformed into the diversity of muscle spindle afferent firing patterns observed experimentally, particularly in naturalistic behaviors. Here, a biophysical model demonstrates that w...

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Detalles Bibliográficos
Autores principales: Blum, Kyle P, Campbell, Kenneth S, Horslen, Brian C, Nardelli, Paul, Housley, Stephen N, Cope, Timothy C, Ting, Lena H
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7769569/
https://www.ncbi.nlm.nih.gov/pubmed/33370235
http://dx.doi.org/10.7554/eLife.55177
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author Blum, Kyle P
Campbell, Kenneth S
Horslen, Brian C
Nardelli, Paul
Housley, Stephen N
Cope, Timothy C
Ting, Lena H
author_facet Blum, Kyle P
Campbell, Kenneth S
Horslen, Brian C
Nardelli, Paul
Housley, Stephen N
Cope, Timothy C
Ting, Lena H
author_sort Blum, Kyle P
collection PubMed
description Despite decades of research, we lack a mechanistic framework capable of predicting how movement-related signals are transformed into the diversity of muscle spindle afferent firing patterns observed experimentally, particularly in naturalistic behaviors. Here, a biophysical model demonstrates that well-known firing characteristics of mammalian muscle spindle Ia afferents – including movement history dependence, and nonlinear scaling with muscle stretch velocity – emerge from first principles of muscle contractile mechanics. Further, mechanical interactions of the muscle spindle with muscle-tendon dynamics reveal how motor commands to the muscle (alpha drive) versus muscle spindle (gamma drive) can cause highly variable and complex activity during active muscle contraction and muscle stretch that defy simple explanation. Depending on the neuromechanical conditions, the muscle spindle model output appears to ‘encode’ aspects of muscle force, yank, length, stiffness, velocity, and/or acceleration, providing an extendable, multiscale, biophysical framework for understanding and predicting proprioceptive sensory signals in health and disease.
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spelling pubmed-77695692020-12-30 Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics Blum, Kyle P Campbell, Kenneth S Horslen, Brian C Nardelli, Paul Housley, Stephen N Cope, Timothy C Ting, Lena H eLife Computational and Systems Biology Despite decades of research, we lack a mechanistic framework capable of predicting how movement-related signals are transformed into the diversity of muscle spindle afferent firing patterns observed experimentally, particularly in naturalistic behaviors. Here, a biophysical model demonstrates that well-known firing characteristics of mammalian muscle spindle Ia afferents – including movement history dependence, and nonlinear scaling with muscle stretch velocity – emerge from first principles of muscle contractile mechanics. Further, mechanical interactions of the muscle spindle with muscle-tendon dynamics reveal how motor commands to the muscle (alpha drive) versus muscle spindle (gamma drive) can cause highly variable and complex activity during active muscle contraction and muscle stretch that defy simple explanation. Depending on the neuromechanical conditions, the muscle spindle model output appears to ‘encode’ aspects of muscle force, yank, length, stiffness, velocity, and/or acceleration, providing an extendable, multiscale, biophysical framework for understanding and predicting proprioceptive sensory signals in health and disease. eLife Sciences Publications, Ltd 2020-12-28 /pmc/articles/PMC7769569/ /pubmed/33370235 http://dx.doi.org/10.7554/eLife.55177 Text en © 2020, Blum et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Computational and Systems Biology
Blum, Kyle P
Campbell, Kenneth S
Horslen, Brian C
Nardelli, Paul
Housley, Stephen N
Cope, Timothy C
Ting, Lena H
Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics
title Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics
title_full Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics
title_fullStr Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics
title_full_unstemmed Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics
title_short Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics
title_sort diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics
topic Computational and Systems Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7769569/
https://www.ncbi.nlm.nih.gov/pubmed/33370235
http://dx.doi.org/10.7554/eLife.55177
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