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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Rapid Online Corrections for Proprioceptive and Visual Perturbations Recruit Similar Circuits in Primary Motor Cortex

Kevin P. Cross, Douglas J. Cook and Stephen H. Scott
eNeuro 18 January 2024, 11 (2) ENEURO.0083-23.2024; https://doi.org/10.1523/ENEURO.0083-23.2024
Kevin P. Cross
1Neuroscience Center, University of North Carolina, Chapel Hill, North Carolina 27599
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Douglas J. Cook
2Department of Surgery, Queen’s University, Kingston, Ontario K7L 3N6, Canada
3Centre for Neuroscience Studies, Queen’s University, Kingston, Ontario K7L 3N6, Canada
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Stephen H. Scott
3Centre for Neuroscience Studies, Queen’s University, Kingston, Ontario K7L 3N6, Canada
4Departments of Biomedical and Molecular Sciences, Queen’s University, Kingston, Ontario K7L 3N6, Canada
5Medicine, Queen’s University, Kingston, Ontario K7L 3N6, Canada
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Abstract

An important aspect of motor function is our ability to rapidly generate goal-directed corrections for disturbances to the limb or behavioral goal. The primary motor cortex (M1) is a key region involved in processing feedback for rapid motor corrections, yet we know little about how M1 circuits are recruited by different sources of sensory feedback to make rapid corrections. We trained two male monkeys (Macaca mulatta) to make goal-directed reaches and on random trials introduced different sensory errors by either jumping the visual location of the goal (goal jump), jumping the visual location of the hand (cursor jump), or applying a mechanical load to displace the hand (proprioceptive feedback). Sensory perturbations evoked a broad response in M1 with ∼73% of neurons (n = 257) responding to at least one of the sensory perturbations. Feedback responses were also similar as response ranges between the goal and cursor jumps were highly correlated (range of r = [0.91, 0.97]) as were the response ranges between the mechanical loads and the visual perturbations (range of r = [0.68, 0.86]). Lastly, we identified the neural subspace each perturbation response resided in and found a strong overlap between the two visual perturbations (range of overlap index, 0.73–0.89) and between the mechanical loads and visual perturbations (range of overlap index, 0.36–0.47) indicating each perturbation evoked similar structure of activity at the population level. Collectively, our results indicate rapid responses to errors from different sensory sources target similar overlapping circuits in M1.

  • motor cortex
  • multisensory
  • proprioception
  • vision

Footnotes

  • S.H.S is a cofounder and CSO of Kinarm which commercializes the robotic technology used in the present study.

  • This work was supported by grants from the Canadian Institute of Health Research (PJT-159559). K.P.C. was supported by an OGS scholarship. S.H.S. was supported by a GSK chair in Neuroscience. We thank Kim Moore, Simone Appaqaq, Ethan Heming, and Helen Bretzke for their laboratory and technical assistance and the LIMB lab for helpful discussions.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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February 2024
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Rapid Online Corrections for Proprioceptive and Visual Perturbations Recruit Similar Circuits in Primary Motor Cortex
Kevin P. Cross, Douglas J. Cook, Stephen H. Scott
eNeuro 18 January 2024, 11 (2) ENEURO.0083-23.2024; DOI: 10.1523/ENEURO.0083-23.2024

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Rapid Online Corrections for Proprioceptive and Visual Perturbations Recruit Similar Circuits in Primary Motor Cortex
Kevin P. Cross, Douglas J. Cook, Stephen H. Scott
eNeuro 18 January 2024, 11 (2) ENEURO.0083-23.2024; DOI: 10.1523/ENEURO.0083-23.2024
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Keywords

  • motor cortex
  • multisensory
  • proprioception
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