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Synaptic connectome of a neurosecretory network in the Drosophila brain

View ORCID ProfileTheresa H. McKim, Jayati Gera, Ariana J. Gayban, View ORCID ProfileNils Reinhard, Giulia Manoli, Selina Hilpert, View ORCID ProfileCharlotte Helfrich-Förster, View ORCID ProfileMeet Zandawala
doi: https://doi.org/10.1101/2024.08.28.609616
Theresa H. McKim
1Integrative Neuroscience Program, University of Nevada Reno, Reno, 89557, NV, USA
2Department of Biology, University of Nevada Reno, Reno, 89557, NV, USA
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  • ORCID record for Theresa H. McKim
Jayati Gera
3Neurobiology and Genetics, Theodor-Boveri Institute, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Ariana J. Gayban
1Integrative Neuroscience Program, University of Nevada Reno, Reno, 89557, NV, USA
4Department of Biochemistry and Molecular Biology, University of Nevada Reno, Reno, 89557, NV, USA
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Nils Reinhard
3Neurobiology and Genetics, Theodor-Boveri Institute, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Giulia Manoli
3Neurobiology and Genetics, Theodor-Boveri Institute, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Selina Hilpert
3Neurobiology and Genetics, Theodor-Boveri Institute, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Charlotte Helfrich-Förster
3Neurobiology and Genetics, Theodor-Boveri Institute, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Meet Zandawala
1Integrative Neuroscience Program, University of Nevada Reno, Reno, 89557, NV, USA
3Neurobiology and Genetics, Theodor-Boveri Institute, Biocenter, University of Würzburg, 97074 Würzburg, Germany
4Department of Biochemistry and Molecular Biology, University of Nevada Reno, Reno, 89557, NV, USA
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  • For correspondence: [email protected]
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Abstract

Hormones mediate inter-organ signaling which is crucial in orchestrating diverse behaviors and physiological processes including sleep and activity, feeding, growth, metabolism and reproduction. The pars intercerebralis and pars lateralis in insects represent major hubs which contain neurosecretory cells (NSC) that produce various hormones. To obtain insight into how hormonal signaling is regulated, we have characterized the synaptic connectome of NSC in the adult Drosophila brain. Identification of neurons providing inputs to multiple NSC subtypes implicates diuretic hormone 44-expressing NSC as a major coordinator of physiology and behavior. Surprisingly, despite most NSC having dendrites in the subesophageal zone (primary taste processing center), gustatory inputs to NSC are largely indirect. We also deciphered pathways via which diverse olfactory inputs are relayed to NSC. Further, our analyses revealed substantial inputs from descending neurons to NSC, suggesting that descending neurons regulate both endocrine and motor output to synchronize physiological changes with appropriate behaviors. In contrast to NSC inputs, synaptic output from NSC is sparse and mostly mediated by corazonin NSC. Therefore, we additionally determine putative paracrine interconnectivity between NSC subtypes and hormonal pathways from NSC to peripheral tissues by analyzing single-cell transcriptomic datasets. Our comprehensive characterization of the Drosophila neurosecretory network connectome provides a platform to understand complex hormonal networks and how they orchestrate animal behaviors and physiology.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted August 29, 2024.
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Synaptic connectome of a neurosecretory network in the Drosophila brain
Theresa H. McKim, Jayati Gera, Ariana J. Gayban, Nils Reinhard, Giulia Manoli, Selina Hilpert, Charlotte Helfrich-Förster, Meet Zandawala
bioRxiv 2024.08.28.609616; doi: https://doi.org/10.1101/2024.08.28.609616
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Synaptic connectome of a neurosecretory network in the Drosophila brain
Theresa H. McKim, Jayati Gera, Ariana J. Gayban, Nils Reinhard, Giulia Manoli, Selina Hilpert, Charlotte Helfrich-Förster, Meet Zandawala
bioRxiv 2024.08.28.609616; doi: https://doi.org/10.1101/2024.08.28.609616

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