UC San Diego

In most sensory systems, neurons are organized into topographic maps which allow for comparison of adjacent inputs via lateral inhibition to selectively propagate salient information. However, in olfaction, it is unclear whether a sensory map exists. Here we address this question by examining the organizing principle underlying the stereotyped pairing of olfactory receptor neurons (ORNs) in Drosophila sensory hairs (sensilla), where the compartmentalized ORNs can inhibit each other via non-synaptic lateral inhibition. By selectively activating individual ORN types, we found that paired neurons in the same sensillum regulate the same behavior but mediate opposing hedonic value—large-spike neurons convey positive valence whereas small-spike neurons convey negative valence. Remarkably, our behavioral assays reveal that the valence-opponent organization is broadly observed between different sensillum types and is relevant in critical behaviors including place preference, egg-laying, and courtship. In addition, pheromone perfuming experiments show that detection of antagonistic cues by neighboring ORNs can more profoundly modulate courtship than that by non-neighboring ORNs. Therefore, lateral inhibition between the antagonistic ORNs can evaluate countervailing olfactory inputs and thereby facilitate behavioral decisions. Our study uncovers a valence map in olfaction, whereby environmental cues are processed by simple circuits at the earliest stage.