Motor planning brings human primary somatosensory cortex into action-specific preparatory states

Abstract

Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here we used 7T functional magnetic resonance imaging (fMRI) and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger action. Surprisingly, these activity patterns were as informative as those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger press, while activity in both regions is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons.

Data availability

The data used to create the figures in this study can be found on github https://github.com/g14r/single-finger-planning

The following data sets were generated

Article and author information

Author details

  1. Giacomo Ariani

    The Brain and Mind Institute, Western University, London, Canada
    For correspondence
    giacomo.ariani@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9074-1272
  2. J Andrew Pruszynski

    Department of Physiology and Pharmacology, Western University, London, Canada
    Competing interests
    J Andrew Pruszynski, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0786-0081
  3. Jörn Diedrichsen

    The Brain and Mind Institute, Western University, London, Canada
    Competing interests
    Jörn Diedrichsen, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0264-8532

Funding

Canada First Research Excellence Fund (BrainsCAN)

  • Jörn Diedrichsen

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

Ethics

Human subjects: All experimental procedures were approved by the Research Ethics Committee at Western University (HSREB protocol 107061). Participants provided written informed consent to procedures and data usage and received monetary compensation for their participation.

Reviewing Editor

  1. Chris I Baker, National Institute of Mental Health, National Institutes of Health, United States

Version history

  1. Preprint posted: December 18, 2020 (view preprint)
  2. Received: April 17, 2021
  3. Accepted: January 11, 2022
  4. Accepted Manuscript published: January 12, 2022 (version 1)
  5. Version of Record published: January 24, 2022 (version 2)

Copyright

© 2022, Ariani 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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  1. Giacomo Ariani
  2. J Andrew Pruszynski
  3. Jörn Diedrichsen
(2022)
Motor planning brings human primary somatosensory cortex into action-specific preparatory states
eLife 11:e69517.
https://doi.org/10.7554/eLife.69517

Share this article

https://doi.org/10.7554/eLife.69517

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