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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 Mehari Kinfe, Stefano Nuccio, François Hug, Bjoern Eskofier, Dario Farina and Roger Maro Enoka
Journal of Neuroscience 15 March 2023, JN-RM-1265-22; DOI: https://doi.org/10.1523/JNEUROSCI.1265-22.2023
Alessandro Del Vecchio
1Department Artificial Intelligence in Biomedical Engineering, Friedrich-Alexander University (FAU), Erlangen-Nürnberg, Erlangen, Germany.
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Carina Marconi Germer
2Department of Bioengineering, Federal University of Pernambuco, Recife, Brazil.
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Thomas Mehari Kinfe
3Division of Functional Neurosurgery and Stereotaxy, Friedrich-Alexander University, Erlangen-Nürnberg, Erlangen, Germany.
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Stefano Nuccio
4Department Human Movement Science, University of Rome “Foro Italico”.
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François Hug
5Université Côte d'Azur, LAMHESS, Nice, France.
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Bjoern Eskofier
1Department Artificial Intelligence in Biomedical Engineering, Friedrich-Alexander University (FAU), Erlangen-Nürnberg, Erlangen, Germany.
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Dario Farina
6Department of Bioengineering, Imperial College London, United Kingdom.
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Roger Maro Enoka
7Department of Integrative Physiology, University of Colorado Boulder, CO, United States.
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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.

Footnotes

  • None of the authors declares any conflicts of interests.

  • DF was sponsored by the European Research Council (ERC) under the Synergy Grant Natural BionicS (810346) and the EPSRC Transformative Healthcare for 2050 project NISNEM Technology (EP/T020970/1).

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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 Mehari Kinfe, Stefano Nuccio, François Hug, Bjoern Eskofier, Dario Farina, Roger Maro Enoka
Journal of Neuroscience 15 March 2023, JN-RM-1265-22; 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 Mehari Kinfe, Stefano Nuccio, François Hug, Bjoern Eskofier, Dario Farina, Roger Maro Enoka
Journal of Neuroscience 15 March 2023, JN-RM-1265-22; DOI: 10.1523/JNEUROSCI.1265-22.2023
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