Constructing an adult orofacial premotor atlas in Allen mouse CCF

  1. Jun Takatoh  Is a corresponding author
  2. Jae Hong Park
  3. Jinghao Lu
  4. Shun Li
  5. P M Thompson
  6. Bao-Xia Han
  7. Shengli Zhao
  8. David Kleinfeld
  9. Beth Friedman
  10. Fan Wang  Is a corresponding author
  1. McGovern Institute, Massachusetts Institute of Technology, United States
  2. Duke University, United States
  3. University of California, San Diego, United States

Abstract

Premotor circuits in the brainstem project to pools of orofacial motoneurons to execute essential motor action such as licking, chewing, breathing, and in rodent, whisking. Previous transsynaptic tracing studies only mapped orofacial premotor circuits in neonatal mice, but the adult circuits remain unknown as a consequence of technical difficulties. Here we developed a three-step monosynaptic transsynaptic tracing strategy to identify premotor neurons controlling vibrissa, tongue protrusion, and jaw-closing muscles in the adult mouse. We registered these different groups of premotor neurons onto the Allen mouse brain common coordinate framework (CCF) and consequently generated a combined 3D orofacial premotor atlas, revealing unique spatial organizations of distinct premotor circuits. We further uncovered premotor neurons that simultaneously innervate multiple motor nuclei and, consequently, are likely to coordinate different muscles involved in the same orofacial motor actions. Our method for tracing adult premotor circuits and registering to Allen CCF is generally applicable and should facilitate the investigations of motor controls of diverse behaviors.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Jun Takatoh

    Department of Brain and Cognitive Sciences, McGovern Institute, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    jtakatoh@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0976-7684
  2. Jae Hong Park

    Department of Biomedical Engineering, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jinghao Lu

    Department of Neurobiology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Shun Li

    Department of Neurobiology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8580-3843
  5. P M Thompson

    Department of Biomedical Engineering, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6083-8831
  6. Bao-Xia Han

    Neurobiology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Shengli Zhao

    Department of Neurobiology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. David Kleinfeld

    Department of Physics, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9797-4722
  9. Beth Friedman

    Department of Computer Science and Engineering, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Fan Wang

    Department of Brain and Cognitive Sciences, McGovern Institute, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    fan_wang@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2988-0614

Funding

National Institute of Neurological Disorders and Stroke (NS107466)

  • David Kleinfeld
  • Fan Wang

National Institute of Neurological Disorders and Stroke (NS077986)

  • Fan Wang

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

Reviewing Editor

  1. Alexander Theodore Chesler, National Institutes of Health, United States

Ethics

Animal experimentation: Animal experimentation: All experiments were conducted according to protocols approved by the Duke University Institutional Animal Care and Use Committee protocol (# A143-18-06).

Version history

  1. Received: February 6, 2021
  2. Accepted: April 26, 2021
  3. Accepted Manuscript published: April 27, 2021 (version 1)
  4. Version of Record published: May 20, 2021 (version 2)

Copyright

© 2021, Takatoh 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. Jun Takatoh
  2. Jae Hong Park
  3. Jinghao Lu
  4. Shun Li
  5. P M Thompson
  6. Bao-Xia Han
  7. Shengli Zhao
  8. David Kleinfeld
  9. Beth Friedman
  10. Fan Wang
(2021)
Constructing an adult orofacial premotor atlas in Allen mouse CCF
eLife 10:e67291.
https://doi.org/10.7554/eLife.67291

Share this article

https://doi.org/10.7554/eLife.67291

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