cVA male pheromone has a 5-mm signaling range, activating 2 parallel central pathways
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Pheromone neurons have spatial receptive fields sharpened by contralateral inhibition
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Position (where) and identity (what) are separated at the 3rd layer of cVA processing
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Integrating taste and cVA in sexually dimorphic aSP-g controls female receptivity
Summary
In Drosophila, a dedicated olfactory channel senses a male pheromone, cis-vaccenyl acetate (cVA), promoting female courtship while repelling males. Here, we show that separate cVA-processing streams extract qualitative and positional information. cVA sensory neurons respond to concentration differences in a 5-mm range around a male. Second-order projection neurons encode the angular position of a male by detecting inter-antennal differences in cVA concentration, which are amplified through contralateral inhibition. At the third circuit layer, we identify 47 cell types with diverse input-output connectivity. One population responds tonically to male flies, a second is tuned to olfactory looming, while a third integrates cVA and taste to coincidentally promote female mating. The separation of olfactory features resembles the mammalian what and where visual streams; together with multisensory integration, this enables behavioral responses appropriate to specific ethological contexts.
Graphical abstract
Keywords
social behavior
sexual dimorphism
sensory physiology
pheromones
connectomics
neural circuits
stereo smell
Data and code availability
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Data: This paper contains analyses that used existing, publicly available data. The identifiers for the datasets are also listed in the key resources table. Reconstructed EM skeletons were deposited in http://www.virtualflybrain.org/. Raw image data (confocal stacks, calcium imaging), and behavior videos will be provided upon request from the lead contact.
Additional information: Any additional information required to reanalyze the data reported in this work is available from the lead contact upon request.