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Monosynaptic premotor circuit tracing reveals neural substrates for oro-motor coordination

  1. Edward Stanek
  2. Steven Cheng
  3. Jun Takatoh
  4. Bao-Xia Han
  5. Fan Wang Is a corresponding author
  1. Duke University Medical Centre, United States
Research Article
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Cite as: eLife 2014;3:e02511 doi: 10.7554/eLife.02511

Abstract

Feeding behaviors require intricately coordinated activation among the muscles of the jaw, tongue, and face, but the neural anatomical substrates underlying such coordination remain unclear. Here we investigate whether the premotor circuitry of jaw and tongue motoneurons contain elements for coordination. Using a modified monosynaptic rabies virus based transsynaptic tracing strategy, we systematically mapped premotor neurons for the jaw-closing masseter muscle and the tongue-protruding genioglossus muscle. The maps revealed that the two groups of premotor neurons are distributed in regions implicated in rhythmogenesis, descending motor control, and sensory feedback. Importantly, we discovered several premotor connection configurations that are ideally suited for coordinating bilaterally symmetric jaw movements, and for enabling co-activation of specific jaw, tongue, and facial muscles. Our findings suggest that shared premotor neurons that form specific multi-target connections with selected motoneurons are a simple and general solution to the problem of orofacial coordination.

Article and author information

Author details

  1. Edward Stanek

    1. Duke University Medical Centre, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Steven Cheng

    1. Duke University Medical Centre, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jun Takatoh

    1. Duke University Medical Centre, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Bao-Xia Han

    1. Duke University Medical Centre, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Fan Wang

    1. Duke University Medical Centre, Durham, United States
    For correspondence
    1. fan.wang@duke.edu
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#A220-12-08) of Duke University. Duke University is fully accredited by the Association for Assessment and Accreditation of Laboratory Animal Care International (AAALAC).

Reviewing Editor

  1. Peggy Mason, Reviewing Editor, University of Chicago, United States

Publication history

  1. Received: February 11, 2014
  2. Accepted: April 24, 2014
  3. Accepted Manuscript published: April 30, 2014 (version 1)
  4. Version of Record published: June 3, 2014 (version 2)

Copyright

© 2014, Stanek et al.

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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