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Research Articles, Systems/Circuits

The Forces Generated by Agonist Muscles during Isometric Contractions Arise from Motor Unit Synergies

Alessandro Del Vecchio, Carina Marconi Germer, Thomas M. Kinfe, Stefano Nuccio, François Hug, Bjoern Eskofier, Dario Farina and Roger M. Enoka
Journal of Neuroscience 19 April 2023, 43 (16) 2860-2873; DOI: https://doi.org/10.1523/JNEUROSCI.1265-22.2023
Alessandro Del Vecchio
1Department Artificial Intelligence in Biomedical Engineering, Friedrich-Alexander University, 91052 Erlangen, Germany
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Carina Marconi Germer
2Department of Bioengineering, Federal University of Pernambuco, CEP 50670-901 Recife, Brazil
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Thomas M. Kinfe
3Division of Functional Neurosurgery and Stereotaxy, Friedrich-Alexander University, 91052 Erlangen, Germany
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Stefano Nuccio
4Department Human Movement Science, University of Rome Foro Italico, 00185 Rome, Italy
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François Hug
5Le Laboratoire Motricité Humaine Expertise Sport Santé, Université Côte d'Azur, 06103 Nice, France
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Bjoern Eskofier
1Department Artificial Intelligence in Biomedical Engineering, Friedrich-Alexander University, 91052 Erlangen, Germany
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Dario Farina
6Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
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Roger M. Enoka
7Department of Integrative Physiology, University of Colorado Boulder, Boulder, Colorado CO 80309
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Abstract

The purpose of our study was to identify the low-dimensional latent components, defined hereafter as motor unit modes, underlying the discharge rates of the motor units in two knee extensors (vastus medialis and lateralis, eight men) and two hand muscles (first dorsal interossei and thenars, seven men and one woman) during submaximal isometric contractions. Factor analysis identified two independent motor unit modes that captured most of the covariance of the motor unit discharge rates. We found divergent distributions of the motor unit modes for the hand and vastii muscles. On average, 75% of the motor units for the thenar muscles and first dorsal interosseus were strongly correlated with the module for the muscle in which they resided. In contrast, we found a continuous distribution of motor unit modes spanning the two vastii muscle modules. The proportion of the muscle-specific motor unit modes was 60% for vastus medialis and 45% for vastus lateralis. The other motor units were either correlated with both muscle modules (shared inputs) or belonged to the module for the other muscle (15% for vastus lateralis). Moreover, coherence of the discharge rates between motor unit pools was explained by the presence of shared synaptic inputs. In simulations with 480 integrate-and-fire neurons, we demonstrate that factor analysis identifies the motor unit modes with high levels of accuracy. Our results indicate that correlated discharge rates of motor units that comprise motor unit modes arise from at least two independent sources of common input among the motor neurons innervating synergistic muscles.

SIGNIFICANCE STATEMENT It has been suggested that the nervous system controls synergistic muscles by projecting common synaptic inputs to the engaged motor neurons. In our study, we reduced the dimensionality of the output produced by pools of synergistic motor neurons innervating the hand and thigh muscles during isometric contractions. We found two neural modules, each representing a different common input, that were each specific for one of the muscles. In the vastii muscles, we found a continuous distribution of motor unit modes spanning the two synergistic muscles. Some of the motor units from the homonymous vastii muscle were controlled by the dominant neural module of the other synergistic muscle. In contrast, we found two distinct neural modules for the hand muscles.

  • common synaptic input
  • motor neurons
  • motor unit
  • muscle synergies

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The Journal of Neuroscience: 43 (16)
Journal of Neuroscience
Vol. 43, Issue 16
19 Apr 2023
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The Forces Generated by Agonist Muscles during Isometric Contractions Arise from Motor Unit Synergies
Alessandro Del Vecchio, Carina Marconi Germer, Thomas M. Kinfe, Stefano Nuccio, François Hug, Bjoern Eskofier, Dario Farina, Roger M. Enoka
Journal of Neuroscience 19 April 2023, 43 (16) 2860-2873; DOI: 10.1523/JNEUROSCI.1265-22.2023

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The Forces Generated by Agonist Muscles during Isometric Contractions Arise from Motor Unit Synergies
Alessandro Del Vecchio, Carina Marconi Germer, Thomas M. Kinfe, Stefano Nuccio, François Hug, Bjoern Eskofier, Dario Farina, Roger M. Enoka
Journal of Neuroscience 19 April 2023, 43 (16) 2860-2873; DOI: 10.1523/JNEUROSCI.1265-22.2023
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Keywords

  • common synaptic input
  • motor neurons
  • motor unit
  • muscle synergies

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