The neural basis for a persistent internal state in drosophila females

David Deutsch, Diego A. Pacheco, Lucas Encarnacion-Rivera, Talmo Pereira, Ramie Fathy, Jan Clemens, Cyrille Girardin, Adam Calhoun, Elise C. Ireland, Austin T. Burke, Sven Dorkenwald, Claire McKellar, Thomas Macrina, Ran Lu, Kisuk Lee, Nico Kemnitz, Dodam Ih, Manuel Castro, Akhilesh Halageri, Chris JordanWilliam Silversmith, Jingpeng Wu, H. Sebastian Seung, Mala Murthy

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish
Article numbere59502
Pages (from-to)1-74
Number of pages74
JournaleLife
Volume9
DOIs
StatePublished - 23 Nov 2020
Externally publishedYes

Bibliographical note

Funding Information:
We thank Barry Dickson, David Anderson, Annegret Falkner and Christa Baker for comments on the manuscript and the entire Murthy lab for helpful discussions. We thank Barry Dickson for sharing the pC1-A split GAL4 line ahead of publication. We thank Stephan Thiberge for assistance with two-photon imaging, Nat Tabris for assistance with software development, Josh Shaevitz for development of modifications to LEAP, Shruthi Ravindranath for assistance with identifying neurons in FlyWire, and Junyu Li for assistance with proofreading behavioral data. We thank Joseph Hsu (Janelia) and other members of the Cambridge Drosophila Connectomics Group for contributing to FlyWire tracing of neurons in this study, and Maria Dreher (Janelia) for assistance with matching cell types across datasets. We thank Katie Schretter and Gerry Rubin for exchanging information prior to publication. This study was supported by an NIH BRAIN Initiative RF1 MH117815-01 to MM and HSS and an NIH BRAIN R01 NS104899 and HHMI Faculty Scholar award to MM.

Publisher Copyright:
© 2020, eLife Sciences Publications Ltd. All rights reserved.

ASJC Scopus subject areas

  • Neuroscience (all)
  • Biochemistry, Genetics and Molecular Biology (all)
  • Immunology and Microbiology (all)

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