Communication from Learned to Innate Olfactory Processing Centers Is Required for Memory Retrieval in Drosophila.

The behavioral response to a sensory stimulus may depend on both learned and innate neuronal representations. How these circuits interact to produce appropriate behavior is unknown. In Drosophila, the lateral horn (LH) and mushroom body (MB) are thought to mediate innate and learned olfactory behavior, respectively, although LH function has not been tested directly. Here we identify two LH cell types (PD2a1 and PD2b1) that receive input from an MB output neuron required for recall of aversive olfactory memories. These neurons are required for aversive memory retrieval and modulated by training. Connectomics data demonstrate that PD2a1 and PD2b1 neurons also receive direct input from food odor-encoding neurons. Consistent with this, PD2a1 and PD2b1 are also necessary for unlearned attraction to some odors, indicating that these neurons have a dual behavioral role. This provides a circuit mechanism by which learned and innate olfactory information can interact in identified neurons to produce appropriate behavior. VIDEO ABSTRACT.This work was supported by MRC LMB graduate studentships and Boehringer Ingelheim Fonds PhD fellowships (to M.-J.D. and A.S.B.) and a Janelia graduate research fellowship (to M.-J.D.), ERC starting (211089) and consolidator (649111) grants and core support from the MRC (MC-U105188491) (to G.S.X.E.J.), Agence Nationale de la Recherche funding of the MemoNetworks and MemoMap projects (to P.-Y.P. and T.P.) and the Labex Memolife PhD fellowship (to G.B.-G.), the Howard Hughes Medical Institute (to A.W. and G.M.R.), a Wellcome Trust collaborative award (203261/Z/16/Z to G.S.X.E.J., D.B., and G.M.R.), and a Cambridge Neuroscience-PSL collaborative grant supported by the Embassy of France in London (to G.S.X.E.J.). This work was also supported by the HHMI Janelia Visiting Scientist Program