Behaviors resulting from the activation of single olfactory receptor neuron class depends on multiple second-order neuron types

Animals rely on olfactory cues to guide critical behaviors such as foraging, mate selection, and predator avoidance. Animals discriminate between different odors because each odor binds to a distinct set of olfactory receptor neurons (ORNs). The relationship between the activated ORN class and resulting behavior is an intensely studied problem. Genetic tools in the Drosophila olfactory system make it particularly suitable for understanding this relationship. In this study, we investigate how activity in Or7a-expressing ORNs (Or7a-ORNs) which projects to the DL5 glomerulus, is transformed into aversive behavior. We find that optogenetically activating Or7a-ORNs causes an increase in locomotion speed which results in mild aversion. Surprisingly, silencing the synaptically connected second-order neuron called DL5PN increases the aversion. Silencing DL5PN has no effect on the increase in speed. The increased aversion results from the flies returning to the stimulated area less often. When DL5PN is left intact, flies return more frequently to the stimulated area. Patch-clamp recordings from PNs other than DL5PNs suggest they are activated when Or7a-ORNs are activated. These results suggest that the behavioral effect downstream of a given ORN class is mediated by multiple PN classes. This work advances our understanding of how aversion is encoded and transmitted through early sensory circuits to shape behavior.