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 Jordan; William Silversmith; Jingpeng Wu; H. Sebastian Seung; Mala Murthy

doi:10.7554/eLife.59502

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 journal › Article › peer-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 language	English
Article number	e59502
Pages (from-to)	1-74
Number of pages	74
Journal	eLife
Volume	9
DOIs	https://doi.org/10.7554/eLife.59502
State	Published - 23 Nov 2020
Externally published	Yes

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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10.7554/eLife.59502

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Deutsch, D., Pacheco, D. A., Encarnacion-Rivera, L., Pereira, T., Fathy, R., Clemens, J., Girardin, C., Calhoun, A., Ireland, E. C., Burke, A. T., Dorkenwald, S., McKellar, C., Macrina, T., Lu, R., Lee, K., Kemnitz, N., Ih, D., Castro, M., Halageri, A., ... Murthy, M. (2020). The neural basis for a persistent internal state in drosophila females. eLife, 9, 1-74. [e59502]. https://doi.org/10.7554/eLife.59502

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title = "The neural basis for a persistent internal state in drosophila females",

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.",

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

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: {\textcopyright} 2020, eLife Sciences Publications Ltd. All rights reserved.",

year = "2020",

month = nov,

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doi = "10.7554/eLife.59502",

language = "English",

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Deutsch, D, Pacheco, DA, Encarnacion-Rivera, L, Pereira, T, Fathy, R, Clemens, J, Girardin, C, Calhoun, A, Ireland, EC, Burke, AT, Dorkenwald, S, McKellar, C, Macrina, T, Lu, R, Lee, K, Kemnitz, N, Ih, D, Castro, M, Halageri, A, Jordan, C, Silversmith, W, Wu, J, Seung, HS & Murthy, M 2020, 'The neural basis for a persistent internal state in drosophila females', eLife, vol. 9, e59502, pp. 1-74. https://doi.org/10.7554/eLife.59502

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T1 - The neural basis for a persistent internal state in drosophila females

AU - Deutsch, David

AU - Pacheco, Diego A.

AU - Encarnacion-Rivera, Lucas

AU - Pereira, Talmo

AU - Fathy, Ramie

AU - Clemens, Jan

AU - Girardin, Cyrille

AU - Calhoun, Adam

AU - Ireland, Elise C.

AU - Burke, Austin T.

AU - Dorkenwald, Sven

AU - McKellar, Claire

AU - Macrina, Thomas

AU - Lu, Ran

AU - Lee, Kisuk

AU - Kemnitz, Nico

AU - Ih, Dodam

AU - Castro, Manuel

AU - Halageri, Akhilesh

AU - Jordan, Chris

AU - Silversmith, William

AU - Wu, Jingpeng

AU - Seung, H. Sebastian

AU - Murthy, Mala

N1 - 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.

PY - 2020/11/23

Y1 - 2020/11/23

N2 - 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.

AB - 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.

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U2 - 10.7554/eLife.59502

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JO - eLife

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ER -

The neural basis for a persistent internal state in drosophila females

Abstract

Bibliographical note

ASJC Scopus subject areas

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