Social state alters vision using three circuit mechanisms in Drosophila

Catherine E. Schretter, Tom Hindmarsh Sten, Nathan Klapoetke, Mei Shao, Aljoscha Nern, Marisa Dreher, Daniel Bushey, Alice A. Robie, Adam L. Taylor, Kristin Branson, Adriane Otopalik, Vanessa Ruta and Gerald M. Rubin ()
Additional contact information
Catherine E. Schretter: Howard Hughes Medical Institute
Tom Hindmarsh Sten: The Rockefeller University
Nathan Klapoetke: Howard Hughes Medical Institute
Mei Shao: Howard Hughes Medical Institute
Aljoscha Nern: Howard Hughes Medical Institute
Marisa Dreher: Howard Hughes Medical Institute
Daniel Bushey: Howard Hughes Medical Institute
Alice A. Robie: Howard Hughes Medical Institute
Adam L. Taylor: Howard Hughes Medical Institute
Kristin Branson: Howard Hughes Medical Institute
Adriane Otopalik: Howard Hughes Medical Institute
Vanessa Ruta: The Rockefeller University
Gerald M. Rubin: Howard Hughes Medical Institute

Nature, 2025, vol. 637, issue 8046, 646-653

Abstract: Abstract Animals are often bombarded with visual information and must prioritize specific visual features based on their current needs. The neuronal circuits that detect and relay visual features have been well studied1–8. Much less is known about how an animal adjusts its visual attention as its goals or environmental conditions change. During social behaviours, flies need to focus on nearby flies9–11. Here we study how the flow of visual information is altered when female Drosophila enter an aggressive state. From the connectome, we identify three state-dependent circuit motifs poised to modify the response of an aggressive female to fly-sized visual objects: convergence of excitatory inputs from neurons conveying select visual features and internal state; dendritic disinhibition of select visual feature detectors; and a switch that toggles between two visual feature detectors. Using cell-type-specific genetic tools, together with behavioural and neurophysiological analyses, we show that each of these circuit motifs is used during female aggression. We reveal that features of this same switch operate in male Drosophila during courtship pursuit, suggesting that disparate social behaviours may share circuit mechanisms. Our study provides a compelling example of using the connectome to infer circuit mechanisms that underlie dynamic processing of sensory signals.

Date: 2025
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DOI: 10.1038/s41586-024-08255-6

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