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

  1. Giacomo Ariani  Is a corresponding author
  2. J Andrew Pruszynski
  3. Jörn Diedrichsen
  1. Western University, Canada

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

Publication 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.

Metrics

  • 1,433
    Page views
  • 251
    Downloads
  • 6
    Citations

Article citation count generated by polling the highest count across the following sources: PubMed Central, Crossref, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Neuroscience
    2. Physics of Living Systems
    Sabrina A Jones, Jacob H Barfield ... Woodrow L Shew
    Research Article

    Naturally occurring body movements and collective neural activity both exhibit complex dynamics, often with scale-free, fractal spatiotemporal structure. Scale-free dynamics of both brain and behavior are important because each is associated with functional benefits to the organism. Despite their similarities, scale-free brain activity and scale-free behavior have been studied separately, without a unified explanation. Here we show that scale-free dynamics of mouse behavior and neurons in visual cortex are strongly related. Surprisingly, the scale-free neural activity is limited to specific subsets of neurons, and these scale-free subsets exhibit stochastic winner-take-all competition with other neural subsets. This observation is inconsistent with prevailing theories of scale-free dynamics in neural systems, which stem from the criticality hypothesis. We develop a computational model which incorporates known cell-type-specific circuit structure, explaining our findings with a new type of critical dynamics. Our results establish neural underpinnings of scale-free behavior and clear behavioral relevance of scale-free neural activity.

    1. Neuroscience
    Barna Zajzon, David Dahmen ... Renato Duarte
    Research Article

    Information from the sensory periphery is conveyed to the cortex via structured projection pathways that spatially segregate stimulus features, providing a robust and efficient encoding strategy. Beyond sensory encoding, this prominent anatomical feature extends throughout the neocortex. However, the extent to which it influences cortical processing is unclear. In this study, we combine cortical circuit modeling with network theory to demonstrate that the sharpness of topographic projections acts as a bifurcation parameter, controlling the macroscopic dynamics and representational precision across a modular network. By shifting the balance of excitation and inhibition, topographic modularity gradually increases task performance and improves the signal-to-noise ratio across the system. We demonstrate that in biologically constrained networks, such a denoising behavior is contingent on recurrent inhibition. We show that this is a robust and generic structural feature that enables a broad range of behaviorally-relevant operating regimes, and provide an in-depth theoretical analysis unravelling the dynamical principles underlying the mechanism.