Pupal behavior emerges from unstructured muscle activity in response to neuromodulation in Drosophila

  1. Amicia D Elliott
  2. Adama Berndt
  3. Matthew Houpert
  4. Snehashis Roy
  5. Robert L Scott
  6. Carson C Chow
  7. Hari Shroff
  8. Benjamin H White  Is a corresponding author
  1. National Institute of General Medical Sciences, United States
  2. National Institute of Mental Health, United States
  3. National Institutes of Health, United States
  4. National Institute of Biomedical Imaging and Bioengineering, United States

Abstract

Identifying neural substrates of behavior requires defining actions in terms that map onto brain activity. Brain and muscle activity naturally correlate via the output of motor neurons, but apart from simple movements it has been difficult to define behavior in terms of muscle contractions. By mapping the musculature of the pupal fruit fly and comprehensively imaging muscle activation at single cell resolution, we here describe a multiphasic behavioral sequence in Drosophila. Our characterization identifies a previously undescribed behavioral phase and permits extraction of major movements by a convolutional neural network. We deconstruct movements into a syllabary of co-active muscles and identify specific syllables that are sensitive to neuromodulatory manipulations. We find that muscle activity shows considerable variability, with sequential increases in stereotypy dependent upon neuromodulation. Our work provides a platform for studying whole-animal behavior, quantifying its variability across multiple spatiotemporal scales, and analyzing its neuromodulatory regulation at cellular resolution.

Data availability

The source data for the figures and tables in this study are available at figshare (https://figshare.com/collections/Pupal_behavior_emerges_from_unstructured_muscle_activity_in_response_to_neuromodulation_in_Drosophila/5489637) and computer code is posted to https://github.com/BenjaminHWhite.

The following data sets were generated

Article and author information

Author details

  1. Amicia D Elliott

    National Institute of General Medical Sciences, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Adama Berndt

    Laboratory of Molecular Biology, National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Matthew Houpert

    Laboratory of Molecular Biology, National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Snehashis Roy

    Laboratory of Molecular Biology, National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Robert L Scott

    Laboratory of Molecular Biology, National Institute of Mental Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Carson C Chow

    National Institute of Diabetes and Kidney and Digestive Diseases, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1463-9553
  7. Hari Shroff

    National Institute of Biomedical Imaging and Bioengineering, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Benjamin H White

    Laboratory of Molecular Biology, National Institute of Mental Health, Bethesda, United States
    For correspondence
    benjaminwhite@mail.nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0612-8075

Funding

National Institute of General Medical Sciences (F12-GM117582)

  • Amicia D Elliott

National Institute of Mental Health (ZIA-MH002800)

  • Benjamin H White

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

Reviewing Editor

  1. Chris Q Doe, Howard Hughes Medical Institute, University of Oregon, United States

Publication history

  1. Preprint posted: March 11, 2021 (view preprint)
  2. Received: March 22, 2021
  3. Accepted: July 6, 2021
  4. Accepted Manuscript published: July 8, 2021 (version 1)
  5. Version of Record published: August 3, 2021 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Amicia D Elliott
  2. Adama Berndt
  3. Matthew Houpert
  4. Snehashis Roy
  5. Robert L Scott
  6. Carson C Chow
  7. Hari Shroff
  8. Benjamin H White
(2021)
Pupal behavior emerges from unstructured muscle activity in response to neuromodulation in Drosophila
eLife 10:e68656.
https://doi.org/10.7554/eLife.68656

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