Mesoscale cortex-wide neural dynamics predict goal-directed, but not random actions in mice several seconds prior to movement

  1. Catalin Mitelut  Is a corresponding author
  2. Yongxu Zhang
  3. Yuki Sekino
  4. Jamie D Boyd
  5. Federico Bollanos
  6. Nicholas V Swindale
  7. Greg Silasi
  8. Shreya Saxena
  9. Timothy H Murphy  Is a corresponding author
  1. University of British Columbia, Canada
  2. University of Florida, United States
  3. University of Ottawa, Canada

Abstract

Volition - the sense of control or agency over one's voluntary actions - is widely recognized as the basis of both human subjective experience and natural behavior in non-human animals. Several human studies have found peaks in neural activity preceding voluntary actions, e.g. the readiness potential (RP), and some have shown upcoming actions could be decoded even before awareness. Others propose that random processes underlie and explain pre-movement neural activity. Here we seek to address these issues by evaluating whether pre-movement neural activity in mice contains structure beyond that present in random neural activity. Implementing a self-initiated water-rewarded lever pull paradigm in mice while recording widefield [Ca++] neural activity we find that cortical activity changes in variance seconds prior to movement and that upcoming lever pulls could be predicted between 3 to 5 seconds (or more in some cases) prior to movement. We found inhibition of motor cortex starting at approximately 5sec prior to lever pulls and activation of motor cortex starting at approximately 2sec prior to a random unrewarded left limb movement. We show that mice, like humans, are biased towards commencing self-initiated actions during specific phases of neural activity but that the pre-movement neural code changes over time in some mice and is widely distributed as behavior prediction improved when using all vs single cortical areas. These findings support the presence of structured multi-second neural dynamics preceding self-initiated action beyond that expected from random processes. Our results also suggest that neural mechanisms underlying self-initiated action could be preserved between mice and humans.

Data availability

Code for generating all figures is provided here:https://github.com/catubc/elife_self_init_paperDatasets are provided on Dryad under the information below:Mitelut, Catalin (2022), Mesoscale cortex-wide neural dynamics predict self-initiated actions in mice several seconds prior to movement, Dryad,Dataset, https://doi.org/10.5061/dryad.ttdz08m0z

The following data sets were generated

Article and author information

Author details

  1. Catalin Mitelut

    Department of Psychiatry, University of British Columbia, Vancouver, Canada
    For correspondence
    mitelutco@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0471-9816
  2. Yongxu Zhang

    Department of Engineering, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Yuki Sekino

    Department of Psychiatry, University of British Columbia, Vancouver, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2038-274X
  4. Jamie D Boyd

    Department of Psychiatry, University of British Columbia, Vancouver, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Federico Bollanos

    Department of Psychiatry, University of British Columbia, Vancouver, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Nicholas V Swindale

    Department of Ophthalmology and Visual Sciences, University of British Columbia, Vancouver, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7106-5114
  7. Greg Silasi

    Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
  8. Shreya Saxena

    Department of Engineering, University of Florida, Gainesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Timothy H Murphy

    Department of Psychiatry, University of British Columbia, Vancouver, Canada
    For correspondence
    thmurphy@mail.ubc.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0093-4490

Funding

Canadian Institutes of Health Research (MOP-15360)

  • Catalin Mitelut
  • Yongxu Zhang
  • Yuki Sekino
  • Jamie D Boyd
  • Federico Bollanos
  • Nicholas V Swindale
  • Greg Silasi
  • Timothy H Murphy

Canadian Institutes of Health Research (MOP-12675)

  • Catalin Mitelut
  • Yongxu Zhang
  • Yuki Sekino
  • Jamie D Boyd
  • Federico Bollanos
  • Nicholas V Swindale
  • Greg Silasi
  • Shreya Saxena
  • Timothy H Murphy

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

Ethics

Animal experimentation: Mouse protocols were approved by the University of British Columbia Animal Care Committee and followed the Canadian Council on Animal Care and Use guidelines (protocols A13-0336 and A14-0266).

Copyright

© 2022, Mitelut 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. Catalin Mitelut
  2. Yongxu Zhang
  3. Yuki Sekino
  4. Jamie D Boyd
  5. Federico Bollanos
  6. Nicholas V Swindale
  7. Greg Silasi
  8. Shreya Saxena
  9. Timothy H Murphy
(2022)
Mesoscale cortex-wide neural dynamics predict goal-directed, but not random actions in mice several seconds prior to movement
eLife 11:e76506.
https://doi.org/10.7554/eLife.76506

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https://doi.org/10.7554/eLife.76506