A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection

Abstract

Flexible behaviors over long timescales are thought to engage recurrent neural networks in deep brain regions, which are experimentally challenging to study. In insects, recurrent circuit dynamics in a brain region called the central complex (CX) enable directed locomotion, sleep, and context- and experience-dependent spatial navigation. We describe the first complete electron-microscopy-based connectome of the Drosophila CX, including all its neurons and circuits at synaptic resolution. We identified new CX neuron types, novel sensory and motor pathways, and network motifs that likely enable the CX to extract the fly’s head-direction, maintain it with attractor dynamics, and combine it with other sensorimotor information to perform vector-based navigational computations. We also identified numerous pathways that may facilitate the selection of CX-driven behavioral patterns by context and internal state. The CX connectome provides a comprehensive blueprint necessary for a detailed understanding of network dynamics underlying sleep, flexible navigation, and state-dependent action selection.

Data availability

All data are freely available at https://neuprint.janelia.org/

Article and author information

Author details

  1. Brad K Hulse

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    hulseb@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
  2. Hannah Haberkern

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    haberkernh@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6135-131X
  3. Romain Franconville

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    franconviller@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4440-7297
  4. Daniel B Turner-Evans

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    turnerevansd@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8020-0170
  5. Shin-ya Takemura

    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2400-6426
  6. Tanya Wolff

    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:" 0000-0002-8681-1749
  7. Marcella Noorman

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Marisa Dreher

    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:" 0000-0002-0041-9229
  9. Chuntao Dan

    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:" 0000-0002-8951-4248
  10. Ruchi Parekh

    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:" 0000-0002-8060-2807
  11. Ann M Hermundstad

    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0377-0516
  12. Gerald M Rubin

    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:" 0000-0001-8762-8703
  13. Vivek Jayaraman

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    vivek@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3680-7378

Funding

Howard Hughes Medical Institute

  • Romain Franconville

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: December 23, 2020
  2. Accepted: September 7, 2021
  3. Accepted Manuscript published: October 26, 2021 (version 1)
  4. Accepted Manuscript updated: October 27, 2021 (version 2)
  5. Accepted Manuscript updated: May 10, 2022 (version 3)

Copyright

© 2021, Hulse 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. Brad K Hulse
  2. Hannah Haberkern
  3. Romain Franconville
  4. Daniel B Turner-Evans
  5. Shin-ya Takemura
  6. Tanya Wolff
  7. Marcella Noorman
  8. Marisa Dreher
  9. Chuntao Dan
  10. Ruchi Parekh
  11. Ann M Hermundstad
  12. Gerald M Rubin
  13. Vivek Jayaraman
(2021)
A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection
eLife 10:e66039.
https://doi.org/10.7554/eLife.66039

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