Most sensory systems are organized into parallel neuronal pathways that process distinct aspects of incoming stimuli. In the insect olfactory system, second order projection neurons target both the mushroom body, required for learning, and the lateral horn (LH), proposed to mediate innate olfactory behavior. Mushroom body neurons form a sparse olfactory population code, which is not stereotyped across animals. In contrast, odor coding in the LH remains poorly understood. We combine genetic driver lines, anatomical and functional criteria to show that the Drosophila LH has ~1400 neurons and >165 cell types. Genetically labeled LHNs have stereotyped odor responses across animals and on average respond to three times more odors than single projection neurons. LHNs are better odor categorizers than projection neurons, likely due to stereotyped pooling of related inputs. Our results reveal some of the principles by which a higher processing area can extract innate behavioral significance from sensory stimuli.

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 15 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 20 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.