4.8 Article

Valence opponency in peripheral olfactory processing

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2120134119

Keywords

olfactory receptor neurons (ORNs); sensory map; valence opponency; countervailing cues; olfactory sensilla

Funding

  1. University of California San Diego (UCSD) School of Medicine Microscopy Core [NS047101]
  2. UCSD Qualcomm Institute Prototyping Lab
  3. Kavli Institute for Brain and Mind Innovative Research Grant
  4. NIH [R01DC016466, R01DC015519, R21DC108912]
  5. Air Force Office of Scientific Research [FA-9550-18-1-0051, FA-9550-19-10280]
  6. Defense Advanced Research Projects Agency Young Faculty Award [D21AP10162]

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This study reveals the existence of an olfactory valence map in Drosophila sensory hairs, which is organized by ephaptic coupling and plays a crucial role in regulating behavior and processing odor mixtures.
A hallmark of complex sensory systems is the organization of neurons into functionally meaningful maps, which allow for comparison and contrast of parallel inputs via lateral inhibition. However, it is unclear whether such a map exists in olfaction. Here, we address this question by determining the organizing principle underlying the stereotyped pairing of olfactory receptor neurons (ORNs) in Drosophila sensory hairs, wherein compartmentalized neurons inhibit each other via ephaptic coupling. Systematic behavioral assays reveal that most paired ORNs antagonistically regulate the same type of behavior. Such valence opponency is relevant in critical behavioral contexts including place preference, egg laying, and courtship. Odor-mixture experiments show that ephaptic inhibition provides a peripheral means for evaluating and shaping countervailing cues relayed to higher brain centers. Furthermore, computational modeling suggests that this organization likely contributes to processing ratio information in odor mixtures. This olfactory valence map may have evolved to swiftly process ethologically meaningful odor blends without involving costly synaptic computation.

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