Communication from learned to innate olfactory processing centers is required for memory retrieval in Drosophila

Many animals can show either learned or innate behavioural responses to a given stimulus. However, how innate and memory circuits interact to produce an appropriate behavioural response is unknown. The Drosophila olfactory system is an excellent model to study how sensory stimuli are processed, stored and transformed into behaviour. Its numerical simplicity, powerful genetics and similarity to mammalian olfactory circuits have enabled many insights into sensory processing and memory. Two higher brain regions, the lateral horn (LH) and the mushroom body (MB) are thought to mediate innate and learned olfactory behaviour respectively, although the function of the LH has not been directly tested. Here we identify a LH cell-type (PD2a1/b1) that receives input from the MB. In contrast to the above model that LH is only necessary for innate behaviour, this cell-type is required for memory retrieval. Moreover, the activity of this cholinergic cell-type is modulated by training, indicating that memory information is passed to the innate olfactory processing centre. PD2a1/b1 dendrites likely receive input from appetitive olfactory projection neurons while their axons project to convergence zones of the MB extrinsic neurons and interdigitate with MB input and output neurons. This work demonstrates that LH neurons play a role in memory retrieval and illustrates the extensive interconnectivity of these two higher brain regions.