Developmental origin of wiring specificity in the olfactory system ofDrosophila

Abstract

In both insects and mammals, olfactory receptor neurons (ORNs) expressing specific olfactory receptors converge their axons onto specific glomeruli,creating a spatial map in the brain. We have previously shown that second order projection neurons (PNs) in Drosophila are prespecified by lineage and birth order to send their dendrites to one of ∼50 glomeruli in the antennal lobe. How can a given class of ORN axons match up with a given class of PN dendrites? Here, we examine the cellular and developmental events that lead to this wiring specificity. We find that, before ORN axon arrival,PN dendrites have already created a prototypic map that resembles the adult glomerular map, by virtue of their selective dendritic localization. Positional cues that create this prototypic dendritic map do not appear to be either from the residual larval olfactory system or from glial processes within the antennal lobe. We propose instead that this prototypic map might originate from both patterning information external to the developing antennal lobe and interactions among PN dendrites.

Genetic Control of Wiring Specificity in the Fly Olfactory System

“…The first hypothesis is unlikely because the olfactory receptors that produce sensory activity are not expressed until specific PN-ORN connections are formed (Jefferis et al 2004). The second and the third hypotheses could not be distinguished until the following observation.…”

“…The organization of specific connections between ORNs and PNs emerges from sequential developmental events, which can be roughly divided into three phases ( Figure 2) (Jefferis et al 2004). In the first phase, PNs send dendritic processes to the antennal lobe at the beginning of puparium formation and elaborate diffuse dendritic processes at stereotypical positions in the proto-antennal lobe (Figure 2A).…”

“…Repulsive and attractive forces establish dendritic fields As PNs elaborate dendrites in the proto-antennal lobe, dendrites of the same class are restricted to a subregion within the antennal lobe (Jefferis et al 2004). Meanwhile, dendrites of the same class expand and fully cover this subregion.…”

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

“…In Drosophila AL development, PN dendrites roughly target near the final targeting area before the arrival of ORN axons ( Fig. 2A; Jefferis et al 2004;Jefferis and Hummel 2006;Sakuma et al 2014). Pioneering ORN axons first wrap around the AL and then start invading inside it (∼24 h after puparium formation [APF]) (Fig.…”

Molecular and cellular mechanisms of dendritic morphogenesis

“…In the spinal cord, different pools of motor neurons (MNs) extend their dendrites to different regions in the gray matter [41]. In the Drosophila olfactory system, PNs target their dendrites to each one of 50 glomeruli in the antennal lobe [9], which is lineage and birth-order dependent but is independent on presynaptic input [16,42]. Similarly, zebrafish RGCs show active dendritic growth toward their laminar target zones [40]; although, in mammals, dendritic pruning is thought to be the major mechanism of dendritic targeting.…”