A multilayer circuit architecture for the generation of distinct locomotor behaviors in Drosophila

  1. Aref Arzan Zarin  Is a corresponding author
  2. Brandon Mark
  3. Albert Cardona
  4. Ashok Litwin-Kumar
  5. Chris Q Doe  Is a corresponding author
  1. Howard Hughes Medical Institute, University of Oregon, United States
  2. Janelia Research Campus, Howard Hughes Medical Institute, United States
  3. Columbia University, United States

Abstract

Animals generate diverse motor behaviors, yet how the same motor neurons (MNs) generate two distinct or antagonistic behaviors remains an open question. Here we characterize Drosophila larval muscle activity patterns and premotor/motor circuits to understand how they generate forward and backward locomotion. We show that all body wall MNs are activated during both behaviors, but a subset of MNs change recruitment timing for each behavior. We used TEM to reconstruct a full segment of all 60 MNs and 236 premotor neurons (PMNs), including differentially-recruited MNs. Analysis of this comprehensive connectome identified PMN-MN ‘labeled line’ connectivity; PMN-MN combinatorial connectivity; asymmetric neuronal morphology; and PMN-MN circuit motifs that could all contribute to generating distinct behaviors. We generated a recurrent network model that reproduced the observed behaviors, and used functional optogenetics to validate selected model predictions. This PMN-MN connectome will provide a foundation for analyzing the full suite of larval behaviors.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source code is available at https://github.com/alitwinkumar/larval_locomotion_rnn

Article and author information

Author details

  1. Aref Arzan Zarin

    Institute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United States
    For correspondence
    azarin@bio.tamu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0484-3622
  2. Brandon Mark

    Institute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Albert Cardona

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ashok Litwin-Kumar

    Department of Neuroscience, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2422-6576
  5. Chris Q Doe

    Institute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United States
    For correspondence
    cdoe@uoregon.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5980-8029

Funding

Howard Hughes Medical Institute

  • Aref Arzan Zarin
  • Albert Cardona
  • Chris Q Doe

National Institutes of Health (HD27056)

  • Brandon Mark
  • Chris Q Doe

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

Reviewing Editor

  1. Kristin Scott, University of California, Berkeley, United States

Version history

  1. Received: September 11, 2019
  2. Accepted: December 22, 2019
  3. Accepted Manuscript published: December 23, 2019 (version 1)
  4. Version of Record published: January 31, 2020 (version 2)
  5. Version of Record updated: June 15, 2021 (version 3)

Copyright

© 2019, Zarin 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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  1. Aref Arzan Zarin
  2. Brandon Mark
  3. Albert Cardona
  4. Ashok Litwin-Kumar
  5. Chris Q Doe
(2019)
A multilayer circuit architecture for the generation of distinct locomotor behaviors in Drosophila
eLife 8:e51781.
https://doi.org/10.7554/eLife.51781

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https://doi.org/10.7554/eLife.51781

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