The organisation of a third-order olfactory brain region in the vinegar fly

Neural representations of the chemosensory world generate both learned and instinctive behaviours. Olfactory systems detect a huge range of volatiles by combining patterns of activity across input channels. The lateral horn of the fly informs innate behaviours by combining patterns of second-order olfactory projection neuron (PN) activity. While most odorants only elicit a strong behavioural response after associative learning, ecologically meaningful and evolutionarily significant odour channels trigger innate behavioural responses, likely through hard-wired, genetically and developmentally pre-programmed circuits. The identity and function of third-order neurons, particularly those outside the mushroom body, the centre for associative learning, are poorly understood. Here I present data and analyses for such third-order neurons as well as the tools I have helped to make my analyses possible. Using full synaptic reconstructions for neurons of the lateral horn, I investigate previously unknown connectivity motifs including local neuron feedback onto PN axons, the synaptic budget of olfactory interneurons, olfactory neurons that actually integrate multiple sensory modalities, and the existence of centrifugal connections from higher brain regions, including those involved in the output of associative learning. These motifs are novel findings for both insect and equivalent mammalian circuits. I attempt to relate my findings to physiological and morphological data collected by light microscopy, probe the correlation between morphology and connectivity, the degree of connection stereotypy within isomorphic cell types, and the developmental origins of neurons and their connections. These observations provide specific insights into the structure of this ‘innate behaviour’ brain region and the statistics of its constituent types’ connectivities, as well as circuit hypotheses for how learned and innate olfactory representations may interact.This work was supported by a Boehringer Ingelheim Fonds PhD Fellowship, a Herchel Smith Studentship and the MRC LMB