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Target neuron prespecification in the olfactory map of Drosophila

Nature volume 414, pages 204–208 (2001)Cite this article

Abstract

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.

References

  1. Axel, R. The molecular logic of smell. Sci. Am. 273, 154–159 (1995).

    Article  CAS  Google Scholar 

  2. 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 

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

    Article  CAS  Google Scholar 

  4. 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 

  5. 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 

  6. 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 

  7. 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 

  8. 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 

  9. 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 

  10. 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 

  11. Mombaerts, P. Molecular biology of odorant receptors in vertebrates. Annu. Rev. Neurosci. 22, 487–509 (1999).

    Article  CAS  Google Scholar 

  12. Bulfone, A. et al. An olfactory sensory map develops in the absence of normal projection neurons or GABAergic interneurons. Neuron 21, 1273–1282 (1998).

    Article  CAS  Google Scholar 

  13. Lee, T., Lee, A. & Luo, L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126, 4065–4076 (1999).

    Article  CAS  Google Scholar 

  14. 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, 443–452 (1997).

    Article  CAS  Google Scholar 

  15. Jhaveri, D., Sen, A. & Rodrigues, V. Mechanisms underlying olfactory neuronal connectivity in Drosophila-the atonal lineage organizes the periphery while sensory neurons and glia pattern the olfactory lobe. Dev. Biol. 226, 73–87 (2000).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  17. Flanagan, J. G. & Vanderhaeghen, P. The ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 21, 309–345 (1998).

    Article  CAS  Google Scholar 

  18. Crowley, J. C. & Katz, L. C. Early development of ocular dominance columns. Science 290, 1321–1324 (2000).

    Article  ADS  CAS  Google Scholar 

  19. Goodman, C. S. & Shatz, C. J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72, 77–98 (1993).

    Article  Google Scholar 

  20. Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).

    Article  ADS  CAS  Google Scholar 

  21. Wu, Q. & Maniatis, T. A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97, 779–790 (1999).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. McConnell, S. K. Strategies for the generation of neuronal diversity in the developing central nervous system. J. Neurosci. 15, 6987–6998 (1995).

    Article  CAS  Google Scholar 

  24. Edlund, T. & Jessell, T. M. Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system. Cell 96, 211–224 (1999).

    Article  CAS  Google Scholar 

  25. Isshiki, T., Pearson, B., Holbrook, S. & Doe, C. Q. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identify of their neuronal progeny. Cell 106, 511–521 (2001).

    Article  CAS  Google Scholar 

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Acknowledgements

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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Author notes

  1. Gregory S. X. E. Jefferis, Elizabeth C. Marin and Reinhard F. Stocker: These two authors contributed equally to this work

Authors and Affiliations

  1. Neurosciences Program,

    Gregory S. X. E. Jefferis & Liqun Luo

  2. Department of Biological Sciences, Stanford University, Stanford, 94305, California, USA

    Gregory S. X. E. Jefferis, Elizabeth C. Marin & Liqun Luo

  3. Department of Biology and Program in Neuroscience, University of Fribourg, Fribourg, CH-1700, Switzerland

    Gregory S. X. E. Jefferis & Elizabeth C. Marin

Authors
  1. Gregory S. X. E. Jefferis
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  2. Elizabeth C. Marin
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  3. Reinhard F. Stocker
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  4. Liqun Luo
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Corresponding author

Correspondence to Liqun Luo.

Supplementary information

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). https://doi.org/10.1038/35102574

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