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PreprintCited by 115Neurobiology and Insect Physiology ResearchNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

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The Neural Basis for a Persistent Internal State in Drosophila Females

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Deutsch, David, Pacheco, Diego A., Encarnacion-Rivera, Lucas J., Pereira, Talmo, Fathy, Ramie, Calhoun, Adam, Ireland, Elise C., Burke, Austin T., Dorkenwald, Sven, McKellar, Claire, Macrina, Thomas, Lu, Ran, Lee, Kisuk, Kemnitz, Nico, Ih, Dodam, Castro, Manuel, Halageri, Akhilesh, Jordan, Chris, Silversmith, William, Wu, Jingpeng, Seung, H. Sebastian, Murthy, Mala·2020·eLife
DOI 10.1101/2020.02.13.947952PMC PMC7787663

Preprint — published as 10.7554/elife.59502 · Paper page

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Abstract

Sustained changes in mood or action require persistent changes in neural activity, but it has been difficult to identify and characterize the neural circuit mechanisms that underlie persistent activity and contribute to long-lasting changes in behavior. Here, we focus on changes in the behavioral state of Drosophila females that persist for minutes following optogenetic activation of a single class of central brain neurons termed pC1. We find that female pC1 neurons drive a variety of persistent behaviors in the presence of males, including increased receptivity, shoving, and chasing. By reconstructing cells in a volume electron microscopic image of the female brain, we classify 7 different pC1 cell types and, using cell type specific driver lines, determine that one of these, pC1-Alpha, is responsible for driving persistent female shoving and chasing. Using calcium imaging, we locate sites of minutes-long persistent neural activity in the brain, which include pC1 neurons themselves. Finally, we exhaustively reconstruct all synaptic partners of a single pC1-Alpha neuron, and find recurrent connectivity that could support the persistent neural activity. 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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Research works printed but not linked: 94

  1. 10.1038/nn1877 · DOI · Paper page
  2. 10.1038/nrn.2016.125 · DOI
  3. 10.1016/j.cell.2014.03.003 · DOI · Paper page
  4. 10.1186/1741-7007-11-11 · DOI · Paper page
  5. 10.1016/j.conb.2016.01.004 · DOI
  6. 10.1371/journal.pcbi.0030035 · DOI
  7. 10.1002/bies.201100185 · DOI · Paper page
  8. 10.1038/nmeth.2973 · DOI
  9. 2017, Sperm and sex peptide stimulate aggression in female Drosophila, Nat Ecol Evol, 1, 0154, 10.1038/s41559-017-0154 · DOI
  10. 10.1016/j.physbeh.2004.02.004 · DOI · Paper page
  11. 10.1016/j.cub.2008.11.001 · DOI
  12. 10.1016/j.cub.2014.06.011 · DOI
  13. 10.1016/j.cub.2010.07.045 · DOI · Paper page
  14. Calhoun, A.J. , Pillow, J.W. , and Murthy, M. (2019). Unsupervised identification of the internal states that shape natural behavior. bioRxiv. · DOI
  15. Cao, Z. , Simon, T. , Wei, S.-E. , and Sheikh, Y. (2017). Realtime multi-person 2d pose estimation using part affinity fields. In Proceedings of the IEEE Conference on Computer Vision and Pattern Recognition, pp. 7291–7299. · DOI · Paper page
  16. 2018, Neural Circuit Mechanisms of Social Behavior, Neuron, 98, 16, 10.1016/j.neuron.2018.02.026 · DOI · Paper page
  17. 10.1038/nature12354 · DOI · Paper page
  18. 2017, A Map of Anticipatory Activity in Mouse Motor Cortex, Neuron, 94, 866, 10.1016/j.neuron.2017.05.005 · DOI
  19. 10.1016/j.cub.2010.11.056 · DOI · Paper page
  20. 2015, Connecting Neural Codes with Behavior in the Auditory System of Drosophila, Neuron, 87, 1332, 10.1016/j.neuron.2015.08.014 · DOI · Paper page
  21. 10.1038/nature13131 · DOI · Paper page
  22. 10.1016/j.conb.2017.12.002 · DOI · Paper page
  23. 10.1007/BF00994018 · DOI · Paper page
  24. 10.1016/j.neuron.2016.06.012 · DOI · Paper page
  25. Cristianini, N. , Shawe-Taylor, J. , and Department of Computer Science Royal Holloway John Shawe-Taylor (2000). An Introduction to Support Vector Machines and Other Kernel-based Learning Methods (Cambridge University Press). · DOI · Paper page
  26. 2019, Shared Song Detector Neurons in Drosophila Male and Female Brains Drive Sex-Specific Behaviors, Curr. Biol, 29, 3200, 10.1016/j.cub.2019.08.008 · DOI · Paper page
  27. 10.1534/genetics.118.300682 · DOI · Paper page
  28. 10.1038/nature01171 · DOI · Paper page
  29. 10.1016/j.cell.2018.08.021 · DOI · Paper page
  30. 10.1083/jcb.200812150 · DOI
  31. Giovannucci, A. , Friedrich, J. , Gunn, P. , Kalfon, J. , Brown, B.L. , Koay, S.A. , Taxidis, J. , Najafi, F. , Gauthier, J.L. , Zhou, P. , et al. (2019). CaImAn an open source tool for scalable calcium imaging data analysis. Elife 8. · DOI
  32. 10.1016/j.neuron.2008.12.012 · DOI · Paper page
  33. 10.1016/0896-6273(95)90304-6 · DOI · Paper page
  34. Hoopfer, E.D. , Jung, Y. , Inagaki, H.K. , Rubin, G.M. , and Anderson, D.J. (2015). P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila. Elife 4. · DOI
  35. 10.1016/j.yhbeh.2003.05.001 · DOI · Paper page
  36. 10.1038/nmeth.2765 · DOI · Paper page
  37. 10.1016/j.neuron.2013.12.017 · DOI · Paper page
  38. 2020, Neurons that Function within an Integrator to Promote a Persistent Behavioral State in Drosophila, Neuron, 105, 322, 10.1016/j.neuron.2019.10.028 · DOI
  39. 10.1038/nmeth.2281 · DOI · Paper page
  40. 10.1101/sqb.2014.79.024984 · DOI
  41. 10.1126/science.aal4835 · DOI · Paper page
  42. 10.1016/j.neuron.2008.06.007 · DOI
  43. 10.1371/journal.pone.0126445 · DOI · Paper page
  44. 10.1038/nmeth.2836 · DOI · Paper page
  45. 10.1016/j.cub.2016.04.017 · DOI
  46. 10.1016/j.cell.2013.11.025 · DOI · Paper page
  47. Kunwar, P.S. , Zelikowsky, M. , Remedios, R. , Cai, H. , Yilmaz, M. , Meister, M. , and Anderson, D.J. (2015). Ventromedial hypothalamic neurons control a defensive emotion state. Elife 4. · DOI
  48. 10.1080/01677060216292 · DOI
  49. 10.1038/nature13169 · DOI · Paper page
  50. 2019, Reward signaling in a recurrent circuit of dopaminergic neurons and peptidergic Kenyon cells, Nat. Commun, 10, 3097, 10.1038/s41467-019-11092-1 · DOI
  51. 10.1016/j.cub.2017.06.076 · DOI
  52. 10.1016/j.neuron.2012.09.010 · DOI · Paper page
  53. 10.1038/nn.4086 · DOI · Paper page
  54. 10.1073/pnas.0404693101 · DOI
  55. 2014, Virtual Fly Brain - Using OWL to support the mapping and genetic dissection of the Drosophila brain, CEUR Workshop Proc, 1265, 85
  56. Pacheco, D.A. , Thiberge, S.Y. , Pnevmatikakis, E. , and Murthy, M. (2019). Auditory Activity is Diverse and Widespread Throughout the Central Brain of Drosophila. bioRxiv. · DOI
  57. 10.1073/pnas.1907042116 · DOI
  58. Park, J.C. , Bae, J.W. , Kim, J. , and Jung, M.W. (2019). Dynamically changing neuronal activity supporting working memory for predictable and unpredictable durations. Scientific Reports 9. · DOI
  59. Pavlou, H.J. , Lin, A.C. , Neville, M.C. , Nojima, T. , Diao, F. , Chen, B.E. , White, B.H. , and Goodwin, S.F. (2016). Neural circuitry coordinating male copulation. Elife 5. · DOI · Paper page
  60. 2019, Fast animal pose estimation using deep neural networks, Nat. Methods, 16, 117, 10.1038/s41592-018-0234-5 · DOI
  61. 10.1534/genetics.110.119917 · DOI · Paper page
  62. 10.1016/j.neuron.2011.01.011 · DOI · Paper page
  63. 10.1016/j.jneumeth.2017.07.031 · DOI
  64. 10.1017/S0954579405050340 · DOI · Paper page
  65. 10.1016/j.semcdb.2005.11.010 · DOI
  66. 10.1016/j.cub.2016.07.021 · DOI
  67. 10.1038/nn.2515 · DOI
  68. 2010, Sex and the single cell, II. There is a time and place for sex. PLoS Biol, 8, e1000365
  69. 10.1037/0033-295X.110.1.145 · DOI · Paper page
  70. 10.1210/er.21.1.55 · DOI · Paper page
  71. 2019, A Neural Circuit Arbitrates between Persistence and Withdrawal in Hungry Drosophila, Neuron, 104, 544, 10.1016/j.neuron.2019.07.028 · DOI
  72. 2017, Neural Circuitry of Wakefulness and Sleep, Neuron, 93, 747, 10.1016/j.neuron.2017.01.014 · DOI · Paper page
  73. Scholz, M. , Linder, A.N. , Randi, F. , Sharma, A.K. , Yu, X. , Shaevitz, J.W. , and Leifer, A. (2018). Predicting natural behavior from whole-brain neural dynamics (bioRxiv).
  74. 10.1038/nbt1037 · DOI · Paper page
  75. 10.1126/science.287.5459.1834 · DOI
  76. 10.1016/j.conb.2013.04.006 · DOI · Paper page
  77. 10.1016/j.cell.2005.04.026 · DOI
  78. 10.1111/j.1469-185X.2010.00149.x · DOI
  79. 2016, State-dependent responses to sex pheromones in mouse, Curr. Opin. Neurobiol, 38, 74, 10.1016/j.conb.2016.04.001 · DOI
  80. Wang, F. , Wang, K. , Forknall, N. , Patrick, C. , Yang, T. , Parekh, R. , Bock, D. and Dickson B. J. (2020). Neural circuitry linking mating and egg-laying in Drosophila females. Nature (In press). · DOI · Paper page
  81. 10.1016/j.neuron.2014.12.025 · DOI
  82. 10.1016/S0031-9384(00)00345-0 · DOI
  83. 10.1523/JNEUROSCI.3529-13.2014 · DOI
  84. Wu, Y. , Bidaye, S.S. , and Mahringer, D. (2019). Drosophila female-specific brain neuron elicits persistent position-and direction-selective male-like social behaviors. bioRxiv. · DOI
  85. Xu, C.S. , Januszewski, M. , Lu, Z. , Takemura, S. , and Hayworth, K. (2020). A Connectome of the Adult Drosophila Central Brain. bioRxiv.
  86. 10.1016/j.cub.2010.08.025 · DOI · Paper page
  87. 2018, Motivation, Perception, and Chance Converge to Make a Binary Decision, Neuron, 99, 376, 10.1016/j.neuron.2018.06.014 · DOI
  88. 2019, Recurrent Circuitry Sustains Drosophila Courtship Drive While Priming Itself for Satiety, Curr. Biol, 29, 3216, 10.1016/j.cub.2019.08.015 · DOI
  89. Zhao, X. , Lenek, D. , Dag, U. , Dickson, B.J. , and Keleman, K. (2018). Persistent activity in a recurrent circuit underlies courtship memory in Drosophila. Elife 7. · DOI · Paper page
  90. 10.1016/j.cell.2018.06.019 · DOI · Paper page
  91. 10.1016/j.neuron.2014.05.038 · DOI
  92. 10.7554/eLife.08477 · DOI · Paper page
  93. 10.1016/S0896-6273(00)80409-2 · DOI
  94. 10.1146/annurev-neuro-070815-014006 · DOI

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Metadata

Authors
Deutsch, D., Pacheco, D. A., Encarnacion-Rivera, L. J., Pereira, T., Fathy, R., 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., Jordan, C., Silversmith, W., Wu, J., Seung, H. S., & Murthy, M.
Affiliations
Princeton University (US)
Corresponding author
Murthy, Mala
ORCID
Venue
eLife
Publisher
openRxiv
Published
2020-02-13
Volume
9
ISSN
2050-084X (ISSN-L)
DOI
10.1101/2020.02.13.947952
PMC
PMC7787663
OpenAlex
W3110215284
Cited by
115
References
0
Citations by year
2026: 12 · 2025: 27 · 2024: 21 · 2023: 23 · 2022: 16 · 2021: 11 · 2020: 5
FWCI
6.30
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Howard Hughes Medical Institute
  • National Institutes of Health (NS104899)
  • National Institute of Mental Health (RF1MH117815)
  • National Institute of Neurological Disorders and Stroke (R01NS104899, R35NS111580)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
persistent activity, doublesex, fruitless, recurrent connectivity, neural circuit mapping, female behavior, courtship behavior
MeSH terms
Animals, Brain, Courtship, Drosophila melanogaster, Female, Male, Microscopy, Electron, Motor Activity, Neural Pathways, Neurons

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