Olfactory systems utilize discrete neural pathways to process and integrate odorant information. In Drosophila, axons of first-order olfactory receptor neurons (ORNs) and dendrites of second-order projection neurons (PNs) form class-specific synaptic connections at ∼50 glomeruli. The mechanisms underlying PN dendrite targeting to distinct glomeruli in a three-dimensional discrete neural map are unclear. We found that the leucine-rich repeat (LRR) transmembrane protein Capricious (Caps) was differentially expressed in different classes of PNs. Loss-of-function and gain-of-function studies indicated that Caps instructs the segregation of Caps-positive and Caps-negative PN dendrites to discrete glomerular targets. Moreover, Caps-mediated PN dendrite targeting was independent of presynaptic ORNs and did not involve homophilic interactions. The closely related protein Tartan was partially redundant with Caps. These LRR proteins are probably part of a combinatorial cell-surface code that instructs discrete olfactory map formation.
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We thank A. Nose (University of Tokyo), S. Cohen (Temasek Life Sciences Laboratory), M. Freeman (Medical Research Council Laboratory of Molecular Biology), S. Hayashi (RIKEN Center for Developmental Biology) and M. Milan (Icrea and Parc Cientific de Barcelona) for fly stocks and reagents; the Bloomington, Szeged, Kyoto and Harvard Stock Centers for fly stocks; M. Spletter for making antennal lobe schemes; and T. Clandinin, K. Miyamichi, M. Spletter, L. Sweeney, J. Wu, X. Yu, D. Berdink and other laboratory members for comments and discussions. This work was supported by US National Institutes of Health grant R01-DC005982. L.L. is an investigator of the Howard Hughes Medical Institute.
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Hong, W., Zhu, H., Potter, C. et al. Leucine-rich repeat transmembrane proteins instruct discrete dendrite targeting in an olfactory map. Nat Neurosci 12, 1542–1550 (2009). https://doi.org/10.1038/nn.2442
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