Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Development of Wiring Specificity of the Drosophila Olfactory System
Department of Biological Sciences, Stanford University, Stanford, CA 94305, USA
Correspondence to be sent to: Liqun Luo, e-mail: lluo{at}stanford.edu
Key words: Drosophila, olfactory system, wiring specificity
The central problem of neural circuit assembly is how wiring specificity is
achieved. The Drosophila olfactory neural circuit presents a fascinating system
to attack this problem. As in mammals, the Drosophila olfactory receptor neurons
(ORNs) that express a given receptor converge their axons onto a common glomerulus in the
antennal lobe, creating an odor map in this first olfactory structure of the central
nervous system (Ressler et al.,
1994
;
Vassar et al., 1994;
Mombaerts et al., 1996;
Gao et al., 2000;
Vosshall et al., 2000).
Antennal lobe projection neurons (PNs) send their dendrites into glomeruli and axons to
higher brain centers including the mushroom body and the lateral horn (Stocker, 1994). Using MARCM-based systematic
clonal analysis, we found that PNs are prespecified by lineage and birth order to send
dendrites to specific glomeruli and thereby carry specific olfactory information
(Jefferis et al., 2001).
Further, we demonstrated that according to glomerular class, PNs have stereotyped axon
branching patterns and terminal fields in the lateral horn (Marin et al., 2002;
Wong et al., 2002). Thus
during the construction of the fly olfactory system, a given ORN must target its axons to
one of 
50 glomeruli, while a given PN must also target its dendrites to one of
50 glomeruli and furthermore the PN must coordinate its dendritic target choice with
its axon terminal arborization pattern in higher olfactory centers.
Our developmental and genetic analyses have begun to shed light on how wiring
specificity in the antennal lobe is achieved. Surprisingly, PN dendrites and ORN axons
appear to have substantial self-organizing properties. For instance, we found that,
before ORN axon arrival, PN dendrites have already created a prototypic dendritic map by
virtue of their selective and stereotyped localization of dendritic processes within the
developing antennal lobe (Jefferis et
al., 2004) and that dendrite-dendrite interactions are essential for the
formation and refinement of the PN dendritic map (Zhu and Luo, 2004). On the ORN side, genetic mosaic
analyses revealed cooperative interactions between axon terminals of the same ORN classes
and hierarchical interdependence among different ORN classes (Komiyama et al., 2004). Thus the precise
wiring of the olfactory system likely relies on extensive PN–PN and ORN–ORN
interactions to create two prototypic maps, which then come into register through
ORN–PN interaction.
We are using both a candidate gene and forward genetic approach to identify genes
that direct the establishment of wiring specificity of the olfactory system. For example,
we have identified a set of POU-domain transcription factors that are expressed in a
lineage-specific fashion in PNs and instruct lineage-specific dendritic targeting
(Komiyama et al., 2003). One
of these POU factors also control ORN axon targeting (Komiyama et al., 2004). We are also analyzing a
number of candidate cell-surface proteins such as N-cadherin (Zhu and Luo, 2004) for their contribution to
wiring specificity. Our ongoing forward genetic screen has yielded a number of
interesting mutants that block different aspects of dendritic targeting, including
glomerular choice, terminal elaboration and uni-glomerular restriction. By continuing
these approaches, we expect to make substantial progress in the near future in
deciphering the molecular logic that underlies the development of wiring specificity in
the antennal lobe.
Many of these genes may be used in projection neurons for both dendritic targeting
and axon terminal arborization (e.g.
Komiyama et al., 2003;
Zhu and Luo, 2004), providing a means
to coordinate the wiring specificity in two olfactory centers.
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References |
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 Top References |
|---|
Gao, Q., Yuan, B. and Chess, A. (2000) Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat. Neurosci., 3, 780–785.[CrossRef][Web of Science][Medline]
Jefferis, G.S.X.E., Marin, E.C., Stocker, R.F. and Luo, L. (2001) Target neuron prespecification in the olfactory map of Drosophila. Nature, 414, 204–208.[CrossRef][Medline]
Jefferis, G.S., Vyas, R.M., Berdnik, D., Ramaekers, A., Stocker, R.F., Tanaka, N.K., Ito, K. and Luo, L. (2004) Developmental origin of wiring specificity in the olfactory system of Drosophila. Development, 131, 117–130.
Komiyama, T., Johnson, W.A., Luo, L. and Jefferis, G.S. (2003) From lineage to wiring specificity: POU domain transcription factors control precise connections of Drosophila olfactory projection neurons. Cell, 112, 157–167.[CrossRef][Medline]
Komiyama, T., Carlson, J.R. and Luo, L. (2004) Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions. Nat. Neurosci., 7, 819–825.[CrossRef][Web of Science][Medline]
Marin, E.C., Jefferis, G.S.X.E., Komiyama, T., Zhu, H. and Luo, L. (2002) Representation of the glomerular olfactory map in the Drosophila brain. Cell, 109, 243–255.[CrossRef][Web of Science][Medline]
Mombaerts, P., Wang, F., Dulac, C., Chao, S.K., Nemes, A., Mendelsohn, M., Edmondson, J. and Axel, R. (1996) Visualizing an olfactory sensory map. Cell, 87, 675–686.[CrossRef][Web of Science][Medline]
Ressler, K.J., Sullivan, S.L. and Buck, L.B. (1994) Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell, 79, 1245–1255.[CrossRef][Web of Science][Medline]
Stocker, R.F. (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res., 275, 3–26.[CrossRef][Web of Science][Medline]
Vassar, R., Chao, S.K., Sitcheran, R., Nunez, J.M., Vosshall, L.B. and Axel, R. (1994) Topographic organization of sensory projections to the olfactory bulb. Cell, 79, 981–991.[CrossRef][Web of Science][Medline]
Vosshall, L.B., Wong, A.M. and Axel, R. (2000) An olfactory sensory map in the fly brain. Cell, 102, 147–159.[CrossRef][Web of Science][Medline]
Wong, A.M., Wang, J.W. and Axel, R. (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell, 109, 229–241.[CrossRef][Web of Science][Medline]
Zhu, H. and Luo, L. (2004) Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron, 42, 63–75.[CrossRef][Medline]
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