Dendritic Eph organizes dendrodendritic segregation in discrete olfactory map formation in Drosophila

Abstract

Proper function of the neural network results from the precise connections between axons and dendrites of presynaptic and postsynaptic neurons, respectively. In the Drosophila olfactory system, the dendrites of projection neurons (PNs) stereotypically target one of ∼50 glomeruli in the antennal lobe (AL), the primary olfactory center in the brain, and form synapses with the axons of olfactory receptor neurons (ORNs). Here, we show that Eph and Ephrin, the well-known axon guidance molecules, instruct the dendrodendritic segregation during the discrete olfactory map formation. The Eph receptor tyrosine kinase is highly expressed and localized in the glomeruli related to reproductive behavior in the developing AL. In one of the pheromone-sensing glomeruli (DA1), the Eph cell-autonomously regulates its dendrites to reside in a single glomerulus by interacting with Ephrins expressed in adjacent PN dendrites. Our data demonstrate that the trans interaction between dendritic Eph and Ephrin is essential for the PN dendritic boundary formation in the DA1 olfactory circuit, potentially enabling strict segregation of odor detection between pheromones and the other odors.

Eph Receptor Effector Ephexin Mediates Olfactory Dendrite Targeting in Drosophila

“…). In summary, our data strengthen and significantly extend previous reports on Eph and ephrin‐mediated PN targeting (Sekine et al, ; Anzo et al, ) by showing how Eph forward signaling and Exn shape specific PN dendrites and subsequently influence ORN targeting. They appear to regulate local PN patterning of distinct glomeruli, possibly by using dendrite‐dendrite interaction, to prevent ectopic innervation of glomeruli of a different class.…”

“…C,D). Taken together, these results along with the already published studies (Sekine et al, ; Anzo et al, ) strongly suggest that Exn similar to Eph is required in PNs during olfactory map development.…”

“…The repulsive signaling of Eph receptor is well suited as repulsion cue for ORN axon and PN dendrite sorting. In addition, two recent publications found a role of Eph in Drosophila olfactory map formation (Sekine et al, ; Anzo et al, ). We initially also tested a previously published null mutant of Eph receptor, eph x652 , for mistargeting of five ORN types in the AL (Boyle et al, ).…”

“…Eph and ephrin were shown to play a role in the guidance of PNs through RNAi and MARCM studies (Sekine et al, ; Anzo et al, ). To test the cell‐type‐specific requirement during olfactory map formation of Exn, we used three different approaches: (i) cell‐type specific rescue, (ii) cell‐type specific RNAi knock‐down, and (iii) mosaic analysis.…”

“…Singh et al () show that Eph in ORNs determines the arborization pattern of a large ephrin‐expressing serotonergic neuron within the AL. Moreover, Anzo et al found that trans‐interaction between Eph and ephrin is required for PN dendritic boundary formation in pheromone sensing glomeruli (Anzo et al, ). Yet, the role and the molecular components of Eph/ephrin‐mediated signaling in this system remain unclear.…”