Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe


In the olfactory system of Drosophila melanogaster, axons of olfactory receptor neurons (ORNs) and dendrites of second-order projection neurons typically target 1 of 50 glomeruli. Dscam, an immunoglobulin superfamily protein, acts in ORNs to regulate axon targeting. Here we show that Dscam acts in projection neurons and local interneurons to control the elaboration of dendritic fields. The removal of Dscam selectively from projection neurons or local interneurons led to clumped dendrites and marked reduction in their dendritic field size. Overexpression of Dscam in projection neurons caused dendrites to be more diffuse during development and shifted their relative position in adulthood. Notably, the positional shift of projection neuron dendrites caused a corresponding shift of its partner ORN axons, thus maintaining the connection specificity. This observation provides evidence for a pre- and postsynaptic matching mechanism independent of precise glomerular positioning.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type



Prices may be subject to local taxes which are calculated during checkout

Figure 1: Dscam loss-of-function phenotypes in projection neuron and local interneuron dendrites.
Figure 2: Projection neurons overexpressing Dscam elaborate more diffuse dendrites in the developing antennal lobe.
Figure 3: Dscam overexpression in Mz19+ projection neurons results in specific dendritic position shift in the adult antennal lobe.
Figure 4: MARCM overexpression of the Dscam transgene in projection neuron dendrites and its effect on ORN axons.
Figure 5: Shift of spatial position of projection neuron dendrites causes a corresponding shift of its partner ORN axons.

Similar content being viewed by others


  1. Hildebrand, J.G. & Shepherd, G.M. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20, 595–631 (1997).

    Article  CAS  Google Scholar 

  2. Vosshall, L.B., Amrein, H., Morozov, P.S., Rzhetsky, A. & Axel, R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725–736 (1999).

    Article  CAS  Google Scholar 

  3. Clyne, P.J. et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327–338 (1999).

    Article  CAS  Google Scholar 

  4. Gao, Q. & Chess, A. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60, 31–39 (1999).

    Article  CAS  Google Scholar 

  5. Goldman, A.L., Van der Goes van Naters, W., Lessing, D., Warr, C.G. & Carlson, J.R. Coexpression of two functional odor receptors in one neuron. Neuron 45, 661–666 (2005).

    Article  CAS  Google Scholar 

  6. Couto, A., Alenius, M. & Dickson, B.J. Molecular, anatomical and functional organization of the Drosophila olfactory system. Curr Biol (2005).

  7. Fishilevich, E. & Vosshall, L.B. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548–1553 (2005).

    Article  CAS  Google Scholar 

  8. Vosshall, L.B., Wong, A.M. & Axel, R. An olfactory sensory map in the fly brain. Cell 102, 147–159 (2000).

    Article  CAS  Google Scholar 

  9. Gao, Q., Yuan, B. & Chess, A. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat. Neurosci. 3, 780–785 (2000).

    Article  CAS  Google Scholar 

  10. Marin, E.C., Jefferis, G.S.X.E., Komiyama, T., Zhu, H. & Luo, L. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109, 243–255 (2002).

    Article  CAS  Google Scholar 

  11. Wong, A.M., Wang, J.W. & Axel, R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229–241 (2002).

    Article  CAS  Google Scholar 

  12. Jefferis, G.S., Marin, E.C., Stocker, R.F. & Luo, L. Target neuron prespecification in the olfactory map of Drosophila. Nature 414, 204–208 (2001).

    Article  CAS  Google Scholar 

  13. Komiyama, T., Johnson, W.A., Luo, L. & Jefferis, G.S. From lineage to wiring specificity: POU domain transcription factors control precise connections of Drosophila olfactory projection neurons. Cell 112, 157–167 (2003).

    Article  CAS  Google Scholar 

  14. Marin, E.C., Watts, R.J., Tanaka, N.K., Ito, K. & Luo, L. Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132, 725–737 (2005).

    Article  CAS  Google Scholar 

  15. Jefferis, G.S. et al. Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 131, 117–130 (2004).

    Article  CAS  Google Scholar 

  16. Zhu, H. & Luo, L. Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron 42, 63–75 (2004).

    Article  CAS  Google Scholar 

  17. Komiyama, T., Carlson, J.R. & Luo, L. Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions. Nat. Neurosci. 7, 819–825 (2004).

    Article  CAS  Google Scholar 

  18. Dobritsa, A.A., van der Goes van Naters, W., Warr, C.G., Steinbrecht, R.A. & Carlson, J.R. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37, 827–841 (2003).

    Article  CAS  Google Scholar 

  19. Wang, J.W., Wong, A.M., Flores, J., Vosshall, L.B. & Axel, R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271–282 (2003).

    Article  CAS  Google Scholar 

  20. Mombaerts, P. et al. Visualizing an olfactory sensory map. Cell 87, 675–686 (1996).

    Article  CAS  Google Scholar 

  21. Wang, F., Nemes, A., Mendelsohn, M. & Axel, R. Odorant receptors govern the formation of a precise topographic map. Cell 93, 47–60 (1998).

    Article  CAS  Google Scholar 

  22. Feinstein, P., Bozza, T., Rodriguez, I., Vassalli, A. & Mombaerts, P. Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell 117, 833–846 (2004).

    Article  CAS  Google Scholar 

  23. Schmucker, D. et al. Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101, 671–684 (2000).

    Article  CAS  Google Scholar 

  24. Hummel, T. et al. Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 37, 221–231 (2003).

    Article  CAS  Google Scholar 

  25. Wang, J., Zugates, C.T., Liang, I.H., Lee, C.H. & Lee, T. Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 33, 559–571 (2002).

    Article  CAS  Google Scholar 

  26. Wang, J. et al. Transmembrane/juxtamembrane domain-dependent Dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 43, 663–672 (2004).

    Article  CAS  Google Scholar 

  27. Zhan, X.L. et al. Analysis of Dscam diversity in regulating axon guidance in Drosophila mushroom bodies. Neuron 43, 673–686 (2004).

    Article  CAS  Google Scholar 

  28. Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451–461 (1999).

    Article  CAS  Google Scholar 

  29. Stocker, R.F., Heimbeck, G., Gendre, N. & de Belle, J.S. Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J. Neurobiol. 32, 443–456 (1997).

    Article  CAS  Google Scholar 

  30. Wojtowicz, W.M., Flanagan, J.J., Millard, S.S., Zipursky, S.L. & Clemens, J.C. Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding. Cell 118, 619–633 (2004).

    Article  CAS  Google Scholar 

  31. Feinstein, P. & Mombaerts, P. A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117, 817–831 (2004).

    Article  CAS  Google Scholar 

  32. Neves, G., Zucker, J., Daly, M. & Chess, A. Stochastic yet biased expression of multiple Dscam splice variants by individual cells. Nat. Genet. 36, 240–246 (2004).

    Article  CAS  Google Scholar 

  33. Jan, Y.N. & Jan, L.Y. The control of dendrite development. Neuron 40, 229–242 (2003).

    Article  CAS  Google Scholar 

  34. Sperry, R.W. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA 50, 703–710 (1963).

    Article  CAS  Google Scholar 

Download references


We thank E. Buchner for antibodies; and T. Komiyama, C. Potter, B. Tasic, T. Clandinin and K. Shen for comments on the manuscript. H.Z. is a recipient of an individual Kirschstein National Research Service Award (NRSA) postdoctoral fellowship. L.L. and S.L.Z. are investigators of the Howard Hughes Medical Institute. This work was supported by the US National Institutes of Health (grants R01-DC005982 to L.L. and R01-DC006485 to S.L.Z.).

Author information

Authors and Affiliations


Corresponding authors

Correspondence to S Lawrence Zipursky or Liqun Luo.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Dscam is expressed in PN dendrites prior to ORN axon arrival. (PDF 4238 kb)

Supplementary Fig. 2

Dscam is requried in PNs for axon branching and terminal arborization. (PDF 2922 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Zhu, H., Hummel, T., Clemens, J. et al. Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nat Neurosci 9, 349–355 (2006).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing