The identification of extensive samples of motor units in human muscles reveals diverse effects of neuromodulatory inputs on the rate coding
Movements are performed by motoneurons transforming synaptic inputs into an activation signal that controls muscle force. The control signal emerges from interactions between ionotropic and neuromodulatory inputs to motoneurons. Critically, these interactions vary across motoneuron pools and differ...
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eLife Sciences Publications Ltd
2024-12-01
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| Online Access: | https://elifesciences.org/articles/97085 |
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| author | Simon Avrillon François Hug Roger M Enoka Arnault HD Caillet Dario Farina |
| author_facet | Simon Avrillon François Hug Roger M Enoka Arnault HD Caillet Dario Farina |
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| description | Movements are performed by motoneurons transforming synaptic inputs into an activation signal that controls muscle force. The control signal emerges from interactions between ionotropic and neuromodulatory inputs to motoneurons. Critically, these interactions vary across motoneuron pools and differ between muscles. To provide the most comprehensive framework to date of motor unit activity during isometric contractions, we identified the firing activity of extensive samples of motor units in the tibialis anterior (129 ± 44 per participant; n=8) and the vastus lateralis (130 ± 63 per participant; n=8) muscles during isometric contractions of up to 80% of maximal force. From this unique dataset, the rate coding of each motor unit was characterised as the relation between its instantaneous firing rate and the applied force, with the assumption that the linear increase in isometric force reflects a proportional increase in the net synaptic excitatory inputs received by the motoneuron. This relation was characterised with a natural logarithm function that comprised two stages. The initial stage was marked by a steep acceleration of firing rate, which was greater for low- than medium- and high-threshold motor units. The second stage comprised a linear increase in firing rate, which was greater for high- than medium- and low-threshold motor units. Changes in firing rate were largely non-linear during the ramp-up and ramp-down phases of the task, but with significant prolonged firing activity only evident for medium-threshold motor units. Contrary to what is usually assumed, our results demonstrate that the firing rate of each motor unit can follow a large variety of trends with force across the pool. From a neural control perspective, these findings indicate how motor unit pools use gain control to transform inputs with limited bandwidths into an intended muscle force. |
| format | Article |
| id | doaj-art-5f01b8cb5c604a7297aa9d831e8aeb38 |
| institution | OA Journals |
| issn | 2050-084X |
| language | English |
| publishDate | 2024-12-01 |
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| spelling | doaj-art-5f01b8cb5c604a7297aa9d831e8aeb382025-08-20T02:37:46ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.97085The identification of extensive samples of motor units in human muscles reveals diverse effects of neuromodulatory inputs on the rate codingSimon Avrillon0https://orcid.org/0000-0002-2226-3528François Hug1Roger M Enoka2Arnault HD Caillet3https://orcid.org/0000-0001-6146-1829Dario Farina4https://orcid.org/0000-0002-7883-2697Department of Bioengineering, Faculty of Engineering, Imperial College London, London, United Kingdom; Nantes Université, Laboratory 'Movement, Interactions, Performance', Nantes, FranceUniversité Côte d'Azur, LAMHESS, Nice, France; The University of Queensland, School of Biomedical Sciences, Brisbane, AustraliaDepartment of Integrative Physiology, University of Colorado Boulder, Boulder, United StatesDepartment of Bioengineering, Faculty of Engineering, Imperial College London, London, United KingdomDepartment of Bioengineering, Faculty of Engineering, Imperial College London, London, United KingdomMovements are performed by motoneurons transforming synaptic inputs into an activation signal that controls muscle force. The control signal emerges from interactions between ionotropic and neuromodulatory inputs to motoneurons. Critically, these interactions vary across motoneuron pools and differ between muscles. To provide the most comprehensive framework to date of motor unit activity during isometric contractions, we identified the firing activity of extensive samples of motor units in the tibialis anterior (129 ± 44 per participant; n=8) and the vastus lateralis (130 ± 63 per participant; n=8) muscles during isometric contractions of up to 80% of maximal force. From this unique dataset, the rate coding of each motor unit was characterised as the relation between its instantaneous firing rate and the applied force, with the assumption that the linear increase in isometric force reflects a proportional increase in the net synaptic excitatory inputs received by the motoneuron. This relation was characterised with a natural logarithm function that comprised two stages. The initial stage was marked by a steep acceleration of firing rate, which was greater for low- than medium- and high-threshold motor units. The second stage comprised a linear increase in firing rate, which was greater for high- than medium- and low-threshold motor units. Changes in firing rate were largely non-linear during the ramp-up and ramp-down phases of the task, but with significant prolonged firing activity only evident for medium-threshold motor units. Contrary to what is usually assumed, our results demonstrate that the firing rate of each motor unit can follow a large variety of trends with force across the pool. From a neural control perspective, these findings indicate how motor unit pools use gain control to transform inputs with limited bandwidths into an intended muscle force.https://elifesciences.org/articles/97085motor unitselectromyographyisometric contractions |
| spellingShingle | Simon Avrillon François Hug Roger M Enoka Arnault HD Caillet Dario Farina The identification of extensive samples of motor units in human muscles reveals diverse effects of neuromodulatory inputs on the rate coding eLife motor units electromyography isometric contractions |
| title | The identification of extensive samples of motor units in human muscles reveals diverse effects of neuromodulatory inputs on the rate coding |
| title_full | The identification of extensive samples of motor units in human muscles reveals diverse effects of neuromodulatory inputs on the rate coding |
| title_fullStr | The identification of extensive samples of motor units in human muscles reveals diverse effects of neuromodulatory inputs on the rate coding |
| title_full_unstemmed | The identification of extensive samples of motor units in human muscles reveals diverse effects of neuromodulatory inputs on the rate coding |
| title_short | The identification of extensive samples of motor units in human muscles reveals diverse effects of neuromodulatory inputs on the rate coding |
| title_sort | identification of extensive samples of motor units in human muscles reveals diverse effects of neuromodulatory inputs on the rate coding |
| topic | motor units electromyography isometric contractions |
| url | https://elifesciences.org/articles/97085 |
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