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MDN brain descending neurons coordinately activate backward and inhibit forward locomotion

  1. Arnaldo Carreira-Rosario
  2. Aref Arzan Zarin
  3. Matthew Q Clark
  4. Laurina Manning
  5. Richard D Fetter
  6. Albert Cardona
  7. Chris Q Doe  Is a corresponding author
  1. Howard Hughes Medical Institute, University of Oregon, United States
  2. Howard Hughes Medical Institute, University of Oregonof Oregon, United States
  3. Howard Hughes Medical Institute, United States
Research Article
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Cite as: eLife 2018;7:e38554 doi: 10.7554/eLife.38554

Abstract

Command-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming (we define 'command-like neuron' as a neuron whose activation elicits or 'commands' a specific behavior). In most animals it remains unknown how neural circuits switch between antagonistic behaviors: via top-down activation/inhibition of antagonistic circuits or via reciprocal inhibition between antagonistic circuits. Here we use genetic screens, intersectional genetics, circuit reconstruction by electron microscopy, and functional optogenetics to identify a bilateral pair of Drosophila larval 'mooncrawler descending neurons' (MDNs) with command-like ability to coordinately induce backward locomotion and block forward locomotion; the former by stimulating a backward-active premotor neuron, and the latter by disynaptic inhibition of a forward-specific premotor neuron. In contrast, direct monosynaptic reciprocal inhibition between forward and backward circuits was not observed. Thus, MDNs coordinate a transition between antagonistic larval locomotor behaviors. Interestingly, larval MDNs persist into adulthood, where they can trigger backward walking. Thus, MDNs induce backward locomotion in both limbless and limbed animals.

Article and author information

Author details

  1. Arnaldo Carreira-Rosario

    Institute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Aref Arzan Zarin

    Institute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0003-0484-3622
  3. Matthew Q Clark

    Institute of Neuroscience, Howard Hughes Medical Institute, Howard Hughes Medical Institute, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0002-1113-9388
  4. Laurina Manning

    Institute of Neuroscience, Howard Hughes Medical Institute, University of Oregonof Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Richard D Fetter

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0002-1558-100X
  6. Albert Cardona

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0003-4941-6536
  7. Chris Q Doe

    Institute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United States
    For correspondence
    cdoe@uoneuro.uoregon.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0001-5980-8029

Funding

National Institutes of Health (HD27056)

  • Richard D Fetter

Howard Hughes Medical Institute (HHMI)

  • Aref Arzan Zarin

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

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Publication history

  1. Received: May 29, 2018
  2. Accepted: July 28, 2018
  3. Accepted Manuscript published: August 2, 2018 (version 1)
  4. Version of Record published: August 17, 2018 (version 2)

Copyright

© 2018, Carreira-Rosario 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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