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

Version history

  1. Preprint posted: December 9, 2020 (view preprint)
  2. Received: December 23, 2020
  3. Accepted: September 7, 2021
  4. Accepted Manuscript published: October 26, 2021 (version 1)
  5. Accepted Manuscript updated: October 27, 2021 (version 2)
  6. Accepted Manuscript updated: May 10, 2022 (version 3)
  7. Version of Record published: September 15, 2022 (version 4)

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.

Metrics

  • 16,823
    views
  • 3,993
    downloads
  • 107
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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)

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

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

  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

Share this article

https://doi.org/10.7554/eLife.66039

Further reading

    1. Computational and Systems Biology
    2. Neuroscience
    Louis K Scheffer, C Shan Xu ... Stephen M Plaza
    Research Article Updated

    The neural circuits responsible for animal behavior remain largely unknown. We summarize new methods and present the circuitry of a large fraction of the brain of the fruit fly Drosophila melanogaster. Improved methods include new procedures to prepare, image, align, segment, find synapses in, and proofread such large data sets. We define cell types, refine computational compartments, and provide an exhaustive atlas of cell examples and types, many of them novel. We provide detailed circuits consisting of neurons and their chemical synapses for most of the central brain. We make the data public and simplify access, reducing the effort needed to answer circuit questions, and provide procedures linking the neurons defined by our analysis with genetic reagents. Biologically, we examine distributions of connection strengths, neural motifs on different scales, electrical consequences of compartmentalization, and evidence that maximizing packing density is an important criterion in the evolution of the fly’s brain.

    1. Neuroscience
    Stanley Heinze
    Insight

    Studying neurons and their connections in the central complex of the fruit fly reveals new insights into how their structure and function shape perception and behavior.