Skip to main content

Thank you for visiting nature.com. 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.

  • Article
  • Published:

Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe

Nature Neuroscience volume 3, pages 780–785 (2000)Cite this article

Abstract

Candidate Drosophila olfactory receptors (ORs) provide molecular tools to investigate how the organization of the Drosophila olfactory system determines the coding of olfactory stimuli. Neurons in the third antennal segment and maxillary palp appear to express different ORs. Individual olfactory neurons send axonal projections to glomeruli in the antennal lobe. Using transgenic flies, we provide evidence that the neurons expressing a given OR gene, which have cell bodies distributed among neurons expressing other ORs, converge in their projections to topographically fixed glomeruli in the antennal lobe. This convergence allows for the formation of an odotopic map in the antennal lobe whose organization could provide a basis for olfactory discrimination in Drosophila.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Drosophila olfactory system anatomy and ORs.
Figure 2: Expression and convergence of Or47a-GAL4-expressing neurons.
Figure 3: Visualization of Or47a specific glomeruli.
Figure 4: Antennal nerve transection eliminates Or47a-mediated GFP labeling of DM3.
Figure 5: Expression and convergence of Or23a-GAL4-expressing neurons.

Similar content being viewed by others

References

  1. Carlson, J. R. Olfaction in Drosophila: from odor to behavior. Trends Genet. 12, 175–180 ( 1996).

    Article  CAS  Google Scholar 

  2. Smith, D. P. Olfactory mechanisms in Drosophila melanogaster. Curr. Opin. Neurobiol. 6, 500–505 ( 1996).

    Article  CAS  Google Scholar 

  3. Charro, M. J. & Alcorta, E. Quantifying relative importance of maxillary palp information on the olfactory behavior of Drosophila melanogaster . J. Comp. Physiol. A 175, 761– 766 (1994).

    Article  CAS  Google Scholar 

  4. Stocker, R. F. The organization of the chemosensory system in Drosophila melanogaster : a review. Cell Tissue Res. 275, 3– 26 (1994).

    Article  CAS  Google Scholar 

  5. Stocker, R. F., Singh, R. N., Schorderet, M. & Siddiqi, O. Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster. Cell Tissue Res. 232, 237–248 (1983).

    Article  CAS  Google Scholar 

  6. Stocker, R. F., Lienhard, M. C., Borst, A. & Fischbach, K. F. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res. 262, 9–34 (1990).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Rubin, G. M. Comparative genomics of the eukaryotes. Science 287 , 2204–2215 (2000).

    Article  CAS  Google Scholar 

  11. Sengupta, P., Chou, J. H. & Bargmann, C. I. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84, 899–909 (1996).

    Article  CAS  Google Scholar 

  12. Troemel, E. R., Chou, J. H., Dwyer, N. D., Colbert, H. A. & Bargmann, C. I. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83, 207–218 (1995).

  13. Buck, L. & Axel, R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175–187 ( 1991).

    Article  CAS  Google Scholar 

  14. Ngai, J., Dowling, M. M., Buck, L., Axel, R. & Chess, A. The family of genes encoding odorant receptors in the channel catfish. Cell 72, 657–666 ( 1993).

    Article  CAS  Google Scholar 

  15. Ebrahimi, F. A. & Chess, A. The specification of olfactory neurons. Curr. Opin. Neurobiol. 8, 453–457 (1998).

    Article  CAS  Google Scholar 

  16. Ressler, K. J., Sullivan, S. L. & Buck, L. B. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73, 597 –609 (1993).

    Article  CAS  Google Scholar 

  17. Vassar, R., Ngai, J. & Axel, R. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 74, 309– 318 (1993).

    Article  CAS  Google Scholar 

  18. Nef, P. et al. Spatial pattern of receptor expression in the olfactory epithelium . Proc. Natl. Acad. Sci. USA 89, 8948– 8952 (1992).

    Article  CAS  Google Scholar 

  19. Strotmann, J., Wanner, I., Krieger, J., Raming, K. & Breer, H. Expression of odorant receptors in spatially restricted subsets of chemosensory neurones. Neuroreport 3, 1053–1056 (1992).

    Article  CAS  Google Scholar 

  20. Dulac, C. & Axel, R. A novel family of genes encoding putative pheromone receptors in mammals. Cell 83, 195–206 (1995).

    Article  CAS  Google Scholar 

  21. Matsunami, H. & Buck, L. B. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 90, 775–784 (1997).

    Article  CAS  Google Scholar 

  22. Herrada, G. & Dulac, C. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell 90, 763– 773 (1997).

    Article  CAS  Google Scholar 

  23. Ryba, N. J. & Tirindelli, R. A new multigene family of putative pheromone receptors. Neuron 19, 371– 379 (1997).

    Article  CAS  Google Scholar 

  24. Rodrigues, V. Spatial coding of olfactory information in the antennal lobe of Drosophila melanogaster. Brain Res. 453, 299– 307 (1988).

    Article  CAS  Google Scholar 

  25. Joerges, J., Kuttner, A., Galizia, C. & Menzel, R. Presentations of odours and odour mixtures visualized in the honeybee brain. Nature 387, 285–288 ( 1997).

    Article  CAS  Google Scholar 

  26. Faber, T., Joerges, J. & Menzel, R. Associative learning modifies neural representations of odors in the insect brain. Nat. Neurosci. 2, 74–78 (1999).

    Article  CAS  Google Scholar 

  27. Galizia, C. G., Sachse, S., Rappert, A. & Menzel, R. The glomerular code for odor representation is species specific in the honeybee Apis mellifera . Nat. Neurosci. 2, 473– 478 (1999).

    Article  CAS  Google Scholar 

  28. Adams, M. et al. The genome sequence of Drosophila melanogaster. Science 287, 2185–2195 ( 2000).

    Article  Google Scholar 

  29. Callahan, C. A. & Thomas, J. B. Tau-beta-galactosidase, an axon-targeted fusion protein. Proc. Natl. Acad. Sci. USA 91, 5972–5976 (1994).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  31. Ito, K. et al. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn. Mem. 5, 52– 77 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Laissue, P. P. et al. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405, 543–552 (1999).

    Article  CAS  Google Scholar 

  33. Chess, A., Simon, I., Cedar, H. & Axel, R. Allelic inactivation regulates olfactory receptor gene expression. Cell 78, 823–834 (1994).

    Article  CAS  Google Scholar 

  34. Rodriguez, I., Feinstein, P. & Mombaerts, P. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97, 199–208 (1999).

    Article  CAS  Google Scholar 

  35. Belluscio, L., Koentges, G., Axel, R. & Dulac, C. A map of pheromone receptor activation in the mammalian brain. Cell 97 , 209–220 (1999).

    Article  CAS  Google Scholar 

  36. Vassar, R. et al. Topographic organization of sensory projections to the olfactory bulb. Cell 79, 981–991 (1994).

    Article  CAS  Google Scholar 

  37. Ressler, K. J., Sullivan, S. L. & Buck, L. B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79, 1245–1255 ( 1994).

    Article  CAS  Google Scholar 

  38. Hafen, E. & Levine, M. in Drosophila: A Practical Approach (ed. Roberts, D.) 139–157 (IRL, Oxford, 1986).

    Google Scholar 

Download references

Acknowledgements

We thank P. Qi and I. Van Wesep for technical assistance, N. Watson for help with confocal analyses, F. Lewitter for help with database analyses, J. Cook-Chrysos for artwork and A. Harry for preparation of the manuscript. We thank F. Ebrahimi, P. Garrity, I. Rebay, P. Sklar and members of the Chess laboratory for advice and critical comments. A.C. is a Rita Allen Foundation Scholar. This work was done in the W.M. Keck Foundation Biological Imaging Facility at the Whitehead Institute.

Author information

Authors and Affiliations

  1. Whitehead Institute for Biomedical Research, Nine Cambridge Center,, Cambridge, 02142, Massachusetts, USA

    Qian Gao, Bingbing Yuan & Andrew Chess

  2. Department of Biology,, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA

    Andrew Chess

Authors
  1. Qian Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bingbing Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrew Chess
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew Chess.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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). https://doi.org/10.1038/77680

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/77680

This article is cited by

Search

Advanced search

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