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Target neuron prespecification in the olfactory map of Drosophila


In Drosophila and mice, olfactory receptor neurons (ORNs) expressing the same receptors have convergent axonal projections to specific glomerular targets in the antennal lobe/olfactory bulb, creating an odour map in this first olfactory structure of the central nervous system1,2,3. Projection neurons of the Drosophila antennal lobe send dendrites into glomeruli and axons to higher brain centres4, thereby transferring this odour map further into the brain. Here we use the MARCM method5 to perform a systematic clonal analysis of projection neurons, allowing us to correlate lineage and birth time of projection neurons with their glomerular choice. We demonstrate that projection neurons are prespecified by lineage and birth order to form synapses with specific incoming ORN axons, and therefore to carry specific olfactory information. This prespecification could be used to hardwire the fly's olfactory system, enabling stereotyped behavioural responses to odorants. Developmental studies lead us to hypothesize that recognition molecules ensure reciprocally specific connections of ORNs and projection neurons. These studies also imply a previously unanticipated role for precise dendritic targeting by postsynaptic neurons in determining connection specificity.

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Figure 1: Three mechanisms of establishing a neural map between two classes of neurons in different fields (d).
Figure 2: Organization of the antennal lobe.
Figure 4: Single-cell clone analysis.
Figure 3: Dorsal and lateral neuroblast clones contain projection neurons with stereotypical and complementary glomerular projections.
Figure 5: Ordered generation of projection neurons derived from neuroblast clone analysis.


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We thank members of the Luo laboratory and B. Baker, S. McConnell, W. Newsome, J. Ngai, C. Niell and D. Hoeppner for comments on the manuscript. G.S.X.E.J. and E.C.M. are HHMI pre-doctoral fellows. This work was supported by a Swiss National Funds grant to R.F.S; and NIH grants and a Terman Fellowship to L.L.

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Correspondence to Liqun Luo.

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Figure 1

(JPG 30.2 KB)

Projection neurons of different ages show similar differentiation at the time of the arrival of the adult olfactory receptor axons. A single cell clone induced at 2-6h after larval hatching (a) and two single cell clones induced at 66-68h after larval hatching (b), imaged at 22±2h after puparium formation. Arrowheads indicate dendritic processes. Arrows indicate mushroom body calyx / lateral horn area. Anti-Fas II (red) labels developing axon tracts. Dotted lines: midlines.

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Jefferis, G., Marin, E., Stocker, R. et al. Target neuron prespecification in the olfactory map of Drosophila. Nature 414, 204–208 (2001).

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