Synergistic organization of neural inputs from spinal motor neurons to extrinsic and intrinsic hand muscles

Simone Tanzarella, Silvia Muceli, Marco Santello, Dario Farina

Research output: Contribution to journalArticlepeer-review

Abstract

Our current understanding of synergistic muscle control is based on the analysis of muscle activities. Modules (synergies) in muscle coordination are extracted from electromyographic (EMG) signal envelopes. Each envelope indirectly reflects the neural drive received by a muscle; therefore, it carries information on the overall activity of the innervating motor neurons. However, it is not known whether the output of spinal motor neurons, whose number is orders of magnitude greater than the muscles they innervate, is organized in a low-dimensional fashion when performing complex tasks. Here, we hypothesized that motor neuron activities exhibit a synergistic organization in complex tasks and therefore that the common input to motor neurons results in a large dimensionality reduction in motor neuron outputs. To test this hypothesis, we factorized the output spike trains of motor neurons innervating 14 intrinsic and extrinsic hand muscles and analyzed the dimensionality of control when healthy individuals exerted isometric forces using seven grip types. We identified four motor neuron synergies, accounting for >70% of the variance of the activity of 54.1 ± 12.9 motor neurons, and we identified four functionally similar muscle synergies. However, motor neuron synergies better discriminated individual finger forces than muscle synergies and were more consistent with the expected role of muscles actuating each finger. Moreover, in a few cases, motor neurons innervating the same muscle were active in separate synergies. Our findings suggest a highly divergent net neural inputs to spinal motor neurons from spinal and supraspinal structures, contributing to the dimensionality reduction captured by muscle synergies.

Original languageEnglish (US)
Pages (from-to)6878-6891
Number of pages14
JournalJournal of Neuroscience
Volume41
Issue number32
DOIs
StatePublished - Aug 11 2021

Keywords

  • Electromyography
  • Motor neuron
  • Motor unit
  • Muscle synergies
  • Spinal modules
  • Synergistic motor control

ASJC Scopus subject areas

  • Neuroscience(all)

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