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The neural basis for a persistent internal state in Drosophila females

Research Article
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Cite this article as: eLife 2020;9:e59502 doi: 10.7554/eLife.59502

Abstract

Sustained changes in mood or action require persistent changes in neural activity, but it has been difficult to identify the neural circuit mechanisms that underlie persistent activity and contribute to long-lasting changes in behavior. Here, we show that a subset of Doublesex+ pC1 neurons in the Drosophila female brain, called pC1d/e, can drive minutes-long changes in female behavior in the presence of males. Using automated reconstruction of a volume electron microscopic (EM) image of the female brain, we map all inputs and outputs to both pC1d and pC1e. This reveals strong recurrent connectivity between, in particular, pC1d/e neurons and a specific subset of Fruitless+ neurons called aIPg. We additionally find that pC1d/e activation drives long-lasting persistent neural activity in brain areas and cells overlapping with the pC1d/e neural network, including both Doublesex+ and Fruitless+ neurons. Our work thus links minutes-long persistent changes in behavior with persistent neural activity and recurrent circuit architecture in the female brain.

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. David S Deutsch

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8587-2435
  2. Diego A Pacheco

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Lucas Encarnacion-Rivera

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Talmo D Pereira

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9075-8365
  5. Ramie Fathy

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Jan Clemens

    European Neuroscience Institute, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4200-8097
  7. Cyrille Girardin

    Neuroscience, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Adam J Calhoun

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Elise C Ireland

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Austin T Burke

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Sven Dorkenwald

    Princeton Neuroscience Institute and Department of Computer Science, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Claire E McKellar

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3580-7336
  13. Thomas Macrina

    Princeton Neuroscience Institute and Department of Computer Science, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Ran Lu

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Kisuk Lee

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Nico Kemnitz

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  17. Dodham Ih

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  18. Manuel Castro

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  19. Akhilesh Halageri

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  20. Chris Jordan

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  21. William Silversmith

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  22. Jingpeng Wu

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  23. H Sebastian Seung

    Princeton Neuroscience Institute and Department of Computer Science, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  24. Mala Murthy

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    For correspondence
    mmurthy@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3063-3389

Funding

National Institutes of Health (RF1 MH117815-01)

  • Mala Murthy

National Institutes of Health (R01 NS104899)

  • Mala Murthy

Howard Hughes Medical Institute (Faculty Scholar)

  • Mala Murthy

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

Reviewing Editor

  1. Megan R Carey, Champalimaud Foundation, Portugal

Publication history

  1. Received: May 30, 2020
  2. Accepted: November 18, 2020
  3. Accepted Manuscript published: November 23, 2020 (version 1)
  4. Accepted Manuscript updated: November 24, 2020 (version 2)
  5. Version of Record published: January 6, 2021 (version 3)
  6. Version of Record updated: January 14, 2021 (version 4)
  7. Version of Record updated: January 19, 2021 (version 5)
  8. Version of Record updated: May 20, 2021 (version 6)
  9. Version of Record updated: September 29, 2021 (version 7)

Copyright

© 2020, Deutsch 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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