Interhemispherically dynamic representation of an eye movement-related activity in mouse frontal cortex

  1. Takashi R Sato  Is a corresponding author
  2. Takahide Itokazu
  3. Hironobu Osaki
  4. Makoto Ohtake
  5. Tetsuya Yamamoto
  6. Kazuhiro Sohya
  7. Takakuni Maki
  8. Tatsuo K Sato  Is a corresponding author
  1. Medical University of South Carolina, United States
  2. Osaka University, Japan
  3. Tokyo Women's Medical University, Japan
  4. Yokohama City University Graduate School of Medicine, Japan
  5. National Center of Neurology and Psychiatry, Japan
  6. Kyoto University Graduate School of Medicine, Japan
  7. Monash University, Australia

Abstract

Cortical plasticity is fundamental to motor recovery following cortical perturbation. However, it is still unclear how this plasticity is induced at a functional circuit level. Here, we investigated motor recovery and underlying neural plasticity upon optogenetic suppression of a cortical area for eye movement. Using a visually-guided eye movement task in mice, we suppressed a portion of the secondary motor cortex (MOs) that encodes contraversive eye movement. Optogenetic unilateral suppression severely impaired contraversive movement on the first day. However, on subsequent days the suppression became inefficient and capability for the movement was restored. Longitudinal two-photon calcium imaging revealed that the regained capability was accompanied by an increased number of neurons encoding for ipsiversive movement in the unsuppressed contralateral MOs. Additional suppression of the contralateral MOs impaired the recovered movement again, indicating a compensatory mechanism. Our findings demonstrate that repeated optogenetic suppression leads to functional recovery mediated by the contralateral hemisphere.

Data availability

The source data are included in the manuscript and supporting files.

Article and author information

Author details

  1. Takashi R Sato

    Department of Neuroscience, Medical University of South Carolina, Charleston, United States
    For correspondence
    satot@musc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7623-9021
  2. Takahide Itokazu

    Department of Neuro-Medical Science, Osaka University, Suita, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Hironobu Osaki

    Department of Physiology, Tokyo Women's Medical University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9780-0810
  4. Makoto Ohtake

    Department of Neuroscience, Medical University of South Carolina, Charleston, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Tetsuya Yamamoto

    Department of Neurosurgery, Yokohama City University Graduate School of Medicine, Yokohama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Kazuhiro Sohya

    Department of Mental Disorder Research, National Center of Neurology and Psychiatry, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Takakuni Maki

    Department of Neurology, Kyoto University Graduate School of Medicine, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Tatsuo K Sato

    Department of Physiology, Biomedicine Discovery Institute, Monash University, Clayton, Australia
    For correspondence
    tatsuo.sato@monash.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

Japan Science and Technology Agency (PRESTO)

  • Takashi R Sato

Deutsche Forschungsgemeinschaft (SA 2575/2-1)

  • Takashi R Sato

Japan Science and Technology Agency (PRESTO)

  • Tatsuo K Sato

Deutsche Forschungsgemeinschaft (SA 2575/3-1)

  • Takashi R Sato

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

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Ethics

Animal experimentation: All experimental procedures were approved by the University of Tuebingen (IN4/11) Medical University of South Carolina (IACUC-2018-00352), and National Center of Neurology and Psychiatry (2014005).

Version history

  1. Received: August 5, 2019
  2. Accepted: November 4, 2019
  3. Accepted Manuscript published: November 5, 2019 (version 1)
  4. Version of Record published: December 4, 2019 (version 2)

Copyright

© 2019, Sato 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. Takashi R Sato
  2. Takahide Itokazu
  3. Hironobu Osaki
  4. Makoto Ohtake
  5. Tetsuya Yamamoto
  6. Kazuhiro Sohya
  7. Takakuni Maki
  8. Tatsuo K Sato
(2019)
Interhemispherically dynamic representation of an eye movement-related activity in mouse frontal cortex
eLife 8:e50855.
https://doi.org/10.7554/eLife.50855

Share this article

https://doi.org/10.7554/eLife.50855

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