The Organization of Projections from Olfactory Glomeruli onto Higher-Order Neurons

Abstract

Each odorant receptor corresponds to a unique glomerulus in the brain. Projections from different glomeruli then converge in higher brain regions, but we do not understand the logic governing which glomeruli converge and which do not. Here, we use two-photon optogenetics to map glomerular connections onto neurons in the lateral horn, the region of the Drosophila brain that receives the majority of olfactory projections. We identify 39 morphological types of lateral horn neurons (LHNs) and show that different types receive input from different combinations of glomeruli. We find that different LHN types do not have independent inputs; rather, certain combinations of glomeruli converge onto many of the same LHNs and so are over-represented. Notably, many over-represented combinations are composed of glomeruli that prefer chemically dissimilar ligands whose co-occurrence indicates a behaviorally relevant "odor scene." The pattern of glomerulus-LHN connections thus represents a prediction of what ligand combinations will be most salient.

Complete connectomic reconstruction of olfactory projection neurons in the fly brain

“…( Figure S4B). This is similar to reports from light microscopy data for both KCs and LHNs [18,48] ( Figure S4B). On average, there is little GABAergic compared with cholinergic or mPN input ( Figure 4D), although LHLN axons receive more feedforward inhibition than their dendrites or LHON dendrites.…”

“…In addition, they do not show GABA immuno-reactivity [81]. In electrophysiological experiments neurons in this lineage excite downstream neurons in the lateral horn [18,20]. We therefore assigned Acetylcholine as putative neurotransmitter.…”

“…We found that an average of~2.5% (which can rise as high as~25%) of inputs to uPN axons is supplied by a hereto undescribed class of neuron. We termed these cells LH 'centrifugal neurons' because they feedback to the LH, and often CA, from the LH's target regions in the superior protocerebrum [5,15,18]. We identified and named 10 LH centrifugal neurons as a byproduct of reconstructing PNs' upstream partners ( Figure 6D, Figure S6D).…”

“…However, the organisation of other third-order olfactory areas that instigate innate behaviours is not well understood. Headway has been made in elucidating architectural and functional aspects across higher-order, insect olfactory circuits [5,13,[15][16][17][18][19][20]. Currently, we lack a framework for the olfactory system to help contextualise these results.…”

Modular structure of human olfactory receptor codes reflects the bases of odor perception

“…Here we take a viewpoint that the coarsegrained olfactory features (labeled by a small number of odor categories) are the "lines and edges" of the perceptual odor space, and that receptor groups represent the receptive fields for these features, with correlated response patterns. Whereas feature-extracting coding was thought to be the realm of higher-level neurons [28,29], here we found a concrete evidence that it already starts at the level of receptors. It remains an open question to study how the encoded information is further organized through the downstream interaction between the OR neurons [30,31].…”