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.

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).

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.

Metrics

  • 5,360
    views
  • 854
    downloads
  • 95
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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?

    1. Neuroscience
    Rongxin Fang, Aaron Halpern ... Xiaowei Zhuang
    Tools and Resources

    Multiplexed error-robust fluorescence in situ hybridization (MERFISH) allows genome-scale imaging of RNAs in individual cells in intact tissues. To date, MERFISH has been applied to image thin-tissue samples of ~10 µm thickness. Here, we present a thick-tissue three-dimensional (3D) MERFISH imaging method, which uses confocal microscopy for optical sectioning, deep learning for increasing imaging speed and quality, as well as sample preparation and imaging protocol optimized for thick samples. We demonstrated 3D MERFISH on mouse brain tissue sections of up to 200 µm thickness with high detection efficiency and accuracy. We anticipate that 3D thick-tissue MERFISH imaging will broaden the scope of questions that can be addressed by spatial genomics.