1. Neuroscience
Download icon

Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila

  1. Anita Burgos  Is a corresponding author
  2. Ken Honjo
  3. Tomoko Ohyama
  4. Cheng Sam Qian
  5. Grace Ji-eun Shin
  6. Daryl M Gohl
  7. Marion Silies
  8. W Daniel Tracey
  9. Marta Zlatic
  10. Albert Cardona
  11. Wesley B Grueber  Is a corresponding author
  1. Columbia University Medical Center, United States
  2. University of Tsukuba, Japan
  3. McGill University, Canada
  4. University of Minnesota Genomics Center, United States
  5. European Neuroscience Institute, Germany
  6. Indiana University, United States
  7. Janelia Research Campus, Howard Hughes Medical Institute, United States
Research Article
  • Cited 7
  • Views 3,190
  • Annotations
Cite this article as: eLife 2018;7:e26016 doi: 10.7554/eLife.26016

Abstract

Rapid and efficient escape behaviors in response to noxious sensory stimuli are essential for protection and survival. Yet, how noxious stimuli are transformed to coordinated escape behaviors remains poorly understood. In Drosophila larvae, noxious stimuli trigger sequential body bending and corkscrew-like rolling behavior. We identified a population of interneurons in the nerve cord of Drosophila, termed Down-and-Back (DnB) neurons, that are activated by noxious heat, promote nociceptive behavior, and are required for robust escape responses to noxious stimuli. Electron microscopic circuit reconstruction shows that DnBs are targets of nociceptive and mechanosensory neurons, are directly presynaptic to pre-motor circuits, and link indirectly to Goro rolling command-like neurons. DnB activation promotes activity in Goro neurons, and coincident inactivation of Goro neurons prevents the rolling sequence but leaves intact body bending motor responses. Thus, activity from nociceptors to DnB interneurons coordinates modular elements of nociceptive escape behavior.

Article and author information

Author details

  1. Anita Burgos

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    For correspondence
    ab3271@columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Ken Honjo

    Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Tomoko Ohyama

    Department of Biology, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Cheng Sam Qian

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Grace Ji-eun Shin

    Department of Physiology and Cellular Biophysics, Columbia University Medical Center, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Daryl M Gohl

    University of Minnesota Genomics Center, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Marion Silies

    European Neuroscience Institute, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. W Daniel Tracey

    The Linda and Jack Gill Center for Biomolecular Science, Indiana University, Bloomington, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4666-8199
  9. Marta Zlatic

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Albert Cardona

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4941-6536
  11. Wesley B Grueber

    Department of Neuroscience, Columbia University Medical Center, New York, United States
    For correspondence
    wg2135@columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6751-256X

Funding

National Science Foundation (Graduate Research Fellowship)

  • Anita Burgos

National Institutes of Health (NS090909-01)

  • Anita Burgos

Howard Hughes Medical Institute

  • Marta Zlatic

National Institutes of Health (NS061908)

  • Wesley B Grueber

National Institutes of Health (GM086458)

  • W Daniel Tracey

National Institutes of Health (NS086564)

  • Wesley B Grueber

Howard Hughes Medical Institute

  • Albert Cardona

Thompson Family Foundation (Innovation Award)

  • Grace Ji-eun Shin
  • Wesley B Grueber

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

Reviewing Editor

  1. David D Ginty, Harvard Medical School, United States

Publication history

  1. Received: February 23, 2017
  2. Accepted: March 9, 2018
  3. Accepted Manuscript published: March 12, 2018 (version 1)
  4. Version of Record published: March 26, 2018 (version 2)
  5. Version of Record updated: July 9, 2018 (version 3)

Copyright

© 2018, Burgos 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.

Metrics

  • 3,190
    Page views
  • 508
    Downloads
  • 7
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

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)

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

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