Paavo Huoviala, Michael-John Dolan, Fiona M. Love, Philip Myers, Shahar Frechter, Shigehiro Namiki, Lovisa Pettersson, Ruairí J.V. Roberts, Robert Turnbull, Zane Mitrevica, Patrick Breads, Philipp Schlegel, Alexander Shakeel Bates, Tiago Rodrigues, Yoshinori Aso, Davi Bock, Gerald M. Rubin, Marcus Stensmyr, Gwyneth Card, Marta Costa, and Gregory S.X.E. Jefferis
Evolution has shaped nervous systems to produce stereotyped behavioural responses to ethologically relevant stimuli. For example when laying eggs, female Drosophila avoid geosmin, an odorant produced by toxic moulds. Here we identify second, third, and fourth order neurons required for this innate olfactory aversion. Connectomics data place these neurons in a complete synaptic circuit from sensory input to descending output. We find multiple levels of valence-specific convergence, including a novel form of axo-axonic input onto second order neurons conveying another danger signal, the pheromone of parasitoid wasps. However, we also observe extensive divergence: second order geosmin neurons connect with a diverse array of 80 third order cell types. We find a pattern of convergence of aversive odour channels at this level. Crossing one more synaptic layer, we identified descending neurons critical for egg-laying aversion. Our data suggest a transition from a labelled line organisation in the periphery to a highly distributed central brain representation that is then coupled to distinct descending pathways.