Functional and Anatomical Specificity in a Higher Olfactory Centre

Most sensory systems are organized into parallel neuronal pathways that process distinct aspects of incoming stimuli. For example, second order olfactory neurons make divergent projections onto functionally distinct brain areas relevant to different behaviors. In insects, one area, the mushroom body has been intensively studied for its role in olfactory learning while the lateral horn is proposed to mediate innate olfactory behavior. Some lateral horn neurons (LHNs) show selective responses to sex pheromones but its functional principles remain poorly understood. We have carried out a comprehensive anatomical analysis of the Drosophila lateral horn and identified genetic driver lines targeting many LHNs. We find that the lateral horn contains >1300 neurons and by combining genetic, anatomical and functional criteria, we identify >150 cell types. In particular we show that genetically labeled LHNs show stereotyped odor responses from one animal to the next. Although LHN tuning can be ultra-sparse (1/40 odors tested), as a population they respond to three times more odors than their inputs; this coding change can be rationalized by our observation that LHNs are better odor categorizers. Our results reveal some of the principles by which a higher sensory processing area can extract innate behavioral significance from sensory stimuli.