期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：5
DOI：10.1073/pnas.2120134119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Are olfactory receptor neurons (ORNs) arranged in a functionally meaningful manner to facilitate information processing? Here, we address this long-standing question by uncovering a valence map in the olfactory periphery of
Drosophila. Within sensory hairs, we find that neighboring ORNs antagonistically regulate behaviors: stereotypically compartmentalized large- and small-spike ORNs, recognized by their characteristic spike amplitudes, either promote or inhibit the same type of behavior, respectively. Systematic optogenetic and thermogenetic assays—covering the majority of antennal sensilla—highlight a valence-opponent organization. Critically, odor-mixture behavioral experiments show that lateral inhibition between antagonistic ORNs mediates robust behavioral decisions in response to countervailing cues. Computational modeling predicts that the robustness of behavioral output depends on odor mixture ratios.
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.
