TY - JOUR
T1 - Synergistic organization of neural inputs from spinal motor neurons to extrinsic and intrinsic hand muscles
AU - Tanzarella, Simone
AU - Muceli, Silvia
AU - Santello, Marco
AU - Farina, Dario
N1 - Funding Information:
This work was supported by the European Research Council (ERC) under the European Union's Horizon 2020 Research and Innovation Program (Project NaturalBionicS; Grant Agreement 810 346; to D.F.), the Chalmers Life Science Engineering Area of Advance (S.M.), and the National Science Foundation Grant BCS-1827752 (to M.S.).
Funding Information:
Received Feb. 26, 2021; revised June 2, 2021; accepted June 3, 2021. Author contributions: S.T., S.M., M.S., and D.F. designed research; S.T., S.M., M.S., and D.F. performed research; S.T., S.M., M.S., and D.F. analyzed data; S.T. wrote the first draft of the paper; S.T., S.M., M.S., and D.F. edited the paper. This work was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 Research and Innovation Program (Project NaturalBionicS; Grant Agreement 810 346; to D.F.), the Chalmers Life Science Engineering Area of Advance (S.M.), and the National Science Foundation Grant BCS-1827752 (to M.S.). The authors declare no competing financial interests. Correspondence should be addressed to Dario Farina at d.farina@imperial.ac.uk. https://doi.org/10.1523/JNEUROSCI.0419-21.2021 Copyright © 2021 the authors
Publisher Copyright:
Copyright © 2021 the authors
PY - 2021/8/11
Y1 - 2021/8/11
N2 - 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.
AB - 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.
KW - Electromyography
KW - Motor neuron
KW - Motor unit
KW - Muscle synergies
KW - Spinal modules
KW - Synergistic motor control
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U2 - 10.1523/JNEUROSCI.0419-21.2021
DO - 10.1523/JNEUROSCI.0419-21.2021
M3 - Article
C2 - 34210782
AN - SCOPUS:85112515872
SN - 0270-6474
VL - 41
SP - 6878
EP - 6891
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 32
ER -