Temporal identity establishes columnar neuron morphology, connectivity, and function in a Drosophila navigation circuit

  1. Luis F Sullivan
  2. Timothy L Warren
  3. Chris Q Doe  Is a corresponding author
  1. Howard Hughes Medical Institute, University of Oregon, United States

Abstract

The insect central complex (CX) is a conserved brain region containing 60+ neuronal subtypes, several of which contribute to navigation. It is not known how CX neuronal diversity is generated or how developmental origin of subtypes relates to function. We mapped the developmental origin of four key CX subtypes and found that neurons with similar origin have similar axon/dendrite targeting. Moreover, we found that the temporal transcription factor (TTF) Eyeless/Pax6 regulates the development of two recurrently-connected CX subtypes: Eyeless loss simultaneously produces ectopic P-EN neurons with normal axon/dendrite projections, and reduces the number of E-PG neurons. Furthermore, transient loss of Eyeless during development impairs adult flies' capacity to perform celestial navigation. We conclude that neurons with similar developmental origin have similar connectivity, that Eyeless maintains equal E-PG and P-EN neuron number, and that Eyeless is required for the development of circuits that control adult navigation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Luis F Sullivan

    Institute of Neuroscience, Howard Hughes Medical Institute, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0149-0999
  2. Timothy L Warren

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

  • Chris Q Doe

National Institutes of Health (T32HD007348)

  • Chris Q Doe

National Institutes of Health (HD27058)

  • 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. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Publication history

  1. Received: November 21, 2018
  2. Accepted: January 31, 2019
  3. Accepted Manuscript published: February 1, 2019 (version 1)
  4. Accepted Manuscript updated: February 6, 2019 (version 2)
  5. Version of Record published: February 22, 2019 (version 3)
  6. Version of Record updated: March 11, 2019 (version 4)

Copyright

© 2019, Sullivan 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. Luis F Sullivan
  2. Timothy L Warren
  3. Chris Q Doe
(2019)
Temporal identity establishes columnar neuron morphology, connectivity, and function in a Drosophila navigation circuit
eLife 8:e43482.
https://doi.org/10.7554/eLife.43482

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