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

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

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

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

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

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

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

Reviewing Editor

  1. Peggy Mason, University of Chicago, United States

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).

Version 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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  1. Edward Stanek
  2. Steven Cheng
  3. Jun Takatoh
  4. Bao-Xia Han
  5. Fan Wang
(2014)
Monosynaptic premotor circuit tracing reveals neural substrates for oro-motor coordination
eLife 3:e02511.
https://doi.org/10.7554/eLife.02511

Share this article

https://doi.org/10.7554/eLife.02511

Further reading

  1. Why don't we bite our tongues when we chew?

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    Human fetal development has been associated with brain health at later stages. It is unknown whether growth in utero, as indexed by birth weight (BW), relates consistently to lifespan brain characteristics and changes, and to what extent these influences are of a genetic or environmental nature. Here we show remarkably stable and lifelong positive associations between BW and cortical surface area and volume across and within developmental, aging and lifespan longitudinal samples (N = 5794, 4–82 y of age, w/386 monozygotic twins, followed for up to 8.3 y w/12,088 brain MRIs). In contrast, no consistent effect of BW on brain changes was observed. Partly environmental effects were indicated by analysis of twin BW discordance. In conclusion, the influence of prenatal growth on cortical topography is stable and reliable through the lifespan. This early-life factor appears to influence the brain by association of brain reserve, rather than brain maintenance. Thus, fetal influences appear omnipresent in the spacetime of the human brain throughout the human lifespan. Optimizing fetal growth may increase brain reserve for life, also in aging.