1. Computational and Systems Biology
  2. Neuroscience
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Rotational dynamics in motor cortex are consistent with a feedback controller

  1. Hari Teja Kalidindi
  2. Kevin P Cross  Is a corresponding author
  3. Timothy P Lillicrap
  4. Mohsen Omrani
  5. Egidio Falotico
  6. Philip N Sabes
  7. Stephen H Scott
  1. Scuola Superiore Sant'Anna, Italy
  2. Queen's University, Canada
  3. University College London, United Kingdom
  4. University of California, San Francisco, United States
Research Article
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Cite this article as: eLife 2021;10:e67256 doi: 10.7554/eLife.67256

Abstract

Recent studies have identified rotational dynamics in motor cortex (MC) which many assume arise from intrinsic connections in MC. However, behavioural and neurophysiological studies suggest that MC behaves like a feedback controller where continuous sensory feedback and interactions with other brain areas contribute substantially to MC processing. We investigated these apparently conflicting theories by building recurrent neural networks that controlled a model arm and received sensory feedback from the limb. Networks were trained to counteract perturbations to the limb and to reach towards spatial targets. Network activities and sensory feedback signals to the network exhibited rotational structure even when the recurrent connections were removed. Furthermore, neural recordings in monkeys performing similar tasks also exhibited rotational structure not only in MC but also in somatosensory cortex. Our results argue that rotational structure may also reflect dynamics throughout the voluntary motor system involved in online control of motor actions.

Data availability

Upon publication the neural network code will be made publicly available athttps://github.com/Hteja/CorticalDynamics. Data and analysis code will be made publicly available at https://github.com/kevincross/CorticalDynamicsAnalysis.

The following previously published data sets were used

Article and author information

Author details

  1. Hari Teja Kalidindi

    The BioRobotics Institute, Scuola Superiore Sant'Anna, Pisa, Italy
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2634-7953
  2. Kevin P Cross

    Centre for Neuroscience Studies, Queen's University, Kingston, Canada
    For correspondence
    13kc18@queensu.ca
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9820-1043
  3. Timothy P Lillicrap

    Centre for Computation, Mathematics and Physics, University College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  4. Mohsen Omrani

    Centre for Neuroscience Studies, Queen's University, Kingston, Canada
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0461-1947
  5. Egidio Falotico

    The BioRobotics Institute, Scuola Superiore Sant'Anna, Pisa, Italy
    Competing interests
    No competing interests declared.
  6. Philip N Sabes

    Department of Physiology, University of California, San Francisco, San Francisco, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8397-6225
  7. Stephen H Scott

    Centre for Neuroscience Studies, Queen's University, Kingston, Canada
    Competing interests
    Stephen H Scott, Co-founder and CSO of Kinarm which commercializes the robotic technology used in the present study..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8821-1843

Funding

Canadian Institutes of Health Research (PJT-159559)

  • Stephen H Scott

European Union's Horizon 2020 Framework Programme for Research and Innovation (785907 (Human Brain Project SGA2))

  • Egidio Falotico

European Union's Horizon 2020 Framework Programme for Research and Innovation (945539 (Human Brain Project SGA3).)

  • Egidio Falotico

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Studies were approved by the Queen's University Research Ethics Board and Animal Care Committee (#Scott-2010-035)

Reviewing Editor

  1. Jesse H Goldberg, Cornell University, United States

Publication history

  1. Preprint posted: November 20, 2020 (view preprint)
  2. Received: February 5, 2021
  3. Accepted: October 28, 2021
  4. Accepted Manuscript published: November 3, 2021 (version 1)

Copyright

© 2021, Kalidindi et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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