The unique synaptic circuitry of specialized olfactory glomeruli in Drosophila melanogaster

In the Drosophila olfactory system, most odorants are encoded in the antennal lobe in a combinatory way, activating several glomerular circuits. However, odorants of particular ecological role for the fly are encoded through activation of a single specialized olfactory pathway. Comparative analyses of densely reconstructed connectomes of one broadly tuned glomerulus (DL5) and one narrowly tuned glomerulus (DA2) gained detailed insight into the variations of synaptic circuitries of glomeruli with different computational tasks. Our approach combined laser branding of glomeruli of interest with volume-based focused ion beam-scanning electron microscopy to enable precise targeting and analysis of the two glomeruli. We discovered differences in their neuronal innervation, synaptic composition, and specific circuitry of their major cell types: olfactory sensory neurons (OSNs), uniglomerular projection neurons, and multiglomerular neurons. By comparing our data with a previously mapped narrowly tuned glomerulus (VA1v), we identified putative generic features of narrowly tuned glomerular circuits, including higher density of neuronal fibers and synapses, lower degree of OSN lateralization, stronger axo-axonic connections between OSNs, dendro-dendritic connections between many uPNs, and lower degree of presynaptic input on OSN axons. In addition, this work revealed that the dendrites of the single uPN in DL5 contain a substantial amount of autapses interconnecting distant regions of the dendritic tree. The comparative analysis of glomeruli allows us to formulate synaptic motifs implemented in olfactory circuits with different computational demands.