Developmental origin of writing specificity in the olfactory system of Drosophila

Development

Volumn 131, Issue 1, 2004, Pages 117-130

  Jefferis, Gregory S X E ^a   Vyas, Raj M ^a   Berdnik, Daniela ^a   Ramaekers, Ariane ^b   Stocker, Reinhard F ^b   Tanaka, Nobuaki K ^c,d   Ito, Kei ^c   Luo, Liquin ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

^c UNIVERSITY OF TOKYO   (Japan)

^d GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

Antennal lobe; Dendrites; Dendritic development; Drosophila; Olfaction; Projection neurons

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; BRAIN DEVELOPMENT; BRAIN MAPPING; BRAIN REGION; CELL INTERACTION; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; DROSOPHILA; EMBRYO; EMBRYO PATTERN FORMATION; GLIA; LARVA; NERVE FIBER; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; REVIEW; TISSUE SPECIFICITY; ANIMAL; ANIMAL EMBRYO; ARTICLE; CELL DIFFERENTIATION; CYTOLOGY; DROSOPHILA MELANOGASTER; GROWTH, DEVELOPMENT AND AGING; MORPHOGENESIS; ODOR; PHYSIOLOGY; PRENATAL DEVELOPMENT; SYNAPTOSOME; ULTRASTRUCTURE;

ANIMALIA; ARACHNIDA; HEXAPODA; INSECTA; MAMMALIA;

ANIMALS; AXONS; CELL DIFFERENTIATION; DENDRITES; DROSOPHILA MELANOGASTER; EMBRYO, NONMAMMALIAN; LARVA; MORPHOGENESIS; OLFACTORY RECEPTOR NEURONS; PRESYNAPTIC TERMINALS; SMELL;

EID: 1142289023     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00896     Document Type: Review

References (55)

1. Axel, R. (1995). The molecular logic of smell. Sci. Am. 273, 154-159.
2. Belluscio, L., Lodovichi, C., Feinstein, P., Mombaerts, P. and Katz, L. C. (2002). Odorant receptors instruct functional circuitry in the mouse olfactory bulb. Nature 419, 296-300.
3. Boeckh, J. and Tolbert, L. P. (1993). Synaptic organization and development of the antennal lobe in insects. Microsc. Res. Tech. 24, 260-280.
4. Buck, L. B. (2000). The molecular architecture of odor and pheromone sensing in mammals. Cell 100, 611-618.
5. Bulfone, A., Wang, E., Hevner, R., Anderson, S., Cutforth, T., Chen, S., Meneses, J., Pedersen, R., Axel, R. and Rubenstein, J. L. (1998). An olfactory sensory map develops in the absence of normal projection neurons or GABAergic interneurons. Neuron 21, 1273-1282.
6. Clandinin, T. R. and Zipursky, S. L. (2000). Afferent growth cone interactions control synaptic specificity in the Drosophila visual system. Neuron 28, 427-436.
7. Cline, H. T. (2001). Dendritic arbor development and synaptogenesis. Curr. Opin. Neurobiol. 11, 118-126.
8. Clyne, P. J., Warr, C. G., Freeman, M. R., Lessing, D., Kim, J. and Carlson, J. R. (1999). A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327-338.
9. Cobb, M. (1999). What and how do maggots smell? Biol. Rev. Cambridge Philos. Soc. 74, 425-459.
10. Devaud, J. M., Acebes, A., Ramaswami, M. and Ferrus, A. (2003). Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age. J. Neurobiol. 56, 13-23.
11. Freeman, M. R., Delrow, J., Kim, J., Johnson, E. and Doe, C. Q. (2003). Unwrapping glial biology. Gcm target genes regulating glial development, diversification, and function. Neuron 38, 567-580.
12. 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.
13. Grueber, W. B., Jan, L. Y. and Jan, Y. N. (2002). Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129, 2867-2878.
14. Grueber, W. B., Ye, B., Moore, A. W., Jan, L. Y. and Jan, Y. N. (2003). Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Curr. Biol. 13, 618-626.
15. Hayashi, S., Ito, K., Sado, Y., Taniguchi, M., Akimoto, A., Takeuchi, H., Aigaki, T., Matsuzaki, F., Nakagoshi, H., Tanimura, T. et al. (2002). GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 34, 58-61.
16. Hummel, T., Vasconcelos, M. L., Clemens, J. C., Fishilevich, Y., Vosshall, L. B. and Zipursky, S. L. (2003). Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 37, 221-231.
17. Ito, K., Suzuki, K., Estes, P., Ramaswami, M., Yamamoto, D. and Struasfeld, N. J. (1998). 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.
18. Jefferis, G. S. X. E., Marin, E. C., Stocker, R. E. and Luo, L. (2001). Target neuron prespecification in the olfactory map of Drosophila. Nature 414, 204-208.
19. Jhaveri, D. and Rodrigues, V. (2002). Sensory neurons of the Atonal lineage pioneer the formation of glomeruli within the adult Drosophila olfactory lobe. Development 129, 1251-1260.
20. Jhaveri, D., Sen, A. and Rodrigues, V. (2000). 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.
21. Joiner, M. A. and Griffith, L. C. (1999). Mapping of the anatomical circuit of CaM kinase-dependent courtship conditioning in Drosophila. Learn. Mem. 6, 177-192.
22. Katz, L. C. and Shatz, C. J. (1996). Synaptic activity and the construction of cortical circuits. Science 274, 1133-1138.
23. 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.
24. Kondoh, Y., Kaneshiro, K. Y., Kimura, K. and Yamamoto, D. (2003). Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc. R. Soc. London B Biol. Sci. 270, 1005-1013.
25. Laissue, P. P., Reiter, C., Hiesinger, P. R., Halter, S., Fischback, K. F. and Stocker, R. F. (1999). Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405, 543-552.
26. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
27. Lin, D. M., Wang, F., Lowe, G., Gold, G. H., Axel, R., Ngai, J. and Brunet, L. (2000). Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity. Neuron 26, 69-80.
28. Malun, D. and Brunjes, P. C. (1996). Development of olfactory glomeruli: temporal and spatial interactions between olfactory receptor axons and mitral cells in opossums and rats. J. Comp. Neurol. 368, 1-16.
29. Malun, D., Oland, L. A. and Tolbert, L. P. (1994). Uniglomerular projection neurons participate in early development of ofactory glomeruli in the moth Manduca sexta. J. Comp. Neurol. 350, 1-22.
30. 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.
31. 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.
32. Newsome, T., Schmidt, S., Dietzl, G., Keleman, K., Asling, B., Debant, A. and Dickson, B. (2000). Trio combines with dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell 101, 283-294.
33. Ng, M., Roorda, R. D., Lima, S. Q., Zemelman, B. V., Morcillo, P. and Miesenbock, G. (2002). Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463-474.
34. Oland, L. A. and Tolbert, L. P. (1998). Glomerulus development in the absence of a set of mitral-like neurons in the insect olfactory lobe. J. Neurobiol. 36, 41-52.
35. Oland, L. A., Orr, G. and Tolbert, L. P. (1990). Construction of a protoglomerular template by olfactory axons initiates the formation of olfactory glomeruli in the insect brain. J. Neurosci. 10, 2096-2112.
36. Python, F. and Stocker, R. F. (2002). Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J. Comp. Neurol. 445, 374-387.
37. 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.
38. Robinow, S. and White, K. (1988). The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev. Biol. 126, 294-303.
39. Shen, K. and Bargmann, C. I. (2003). The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans. Cell 112, 619-630.
40. Simon, D. K. and O'Leary, D. D. (1992). Development of topographic order in the mammalian retinocollicular projection. J. Neurosci. 12, 1212-1232.
41. Stocker, R. F., Lienhard, M. C., Borst, A. and Fischbach, K.-F. (1990). Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res. 262, 9-34.
42. Stocker, R. E., Heimbeck, G., Gendre, N. and de Belle, J. S. (1997). Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J. Neurobiol. 32, 443-452.
43. Strausfeld, N. J. and Hildebrand, J. G. (1999). Olfactory systems: common design, uncommon origins? Curr. Opin. Neurobiol. 9, 634-639.
44. Tissot, M., Gendre, N., Hawken, A., Stortkuhl, K. F. and Stocker, R. F. (1997). Larval chemosensory projections and invasion of adult afferents in the antennal lobe of Drosophila. J. Neurobiol. 32, 281-297.
45. Treloar, H. B., Purcell, A. L. and Greer, C. A. (1999). Glomerular formation in the developing rat olfactory bulb. J. Comp. Neurol. 413, 289-304.
46. Valverde, F., Santacana, M. and Heredia, M. (1992). Formation of an olfactory glomerulus: morphological aspects of development and organization. Neuroscience 49, 255-275.
47. Vassalli, A., Rothman, A., Feinstein, P., Zapotocky, M. and Mombaerts, P. (2002). Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb. Neuron 35, 681-696.
48. 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.
49. Vosshall, L. B., Wong, A. M. and Axel, R. (2000). An olfactory sensory map in the fly brain. Cell 102, 147-159.
50. Wang, F., Nemes, A., Mendelsohn, M. and Axel, R. (1998). Odorant receptors govern the formation of a precise topographic map. Cell 93, 47-60.
51. Wassle, H., Peichl, L. and Boycott, B. B. (1981). Dendritic territories of cat retinal ganglion cells. Nature 292, 344-345.
52. Wong, A. M., Wang, J. W. and Axel, R. (2002). Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229-241.
53. Xiong, W. C., Okano, H., Patel, N. H., Blendy, J. A. and Montell, C. (1994). repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 8, 981-994.
54. Yates, P. A., Roskies, A. L., McLaughlin, T. and O'Leary, D. D. (2001). Topographic-specific axon branching controlled by ephrin-As is the critical event in retinotectal map development. J. Neurosci. 21, 8548-8563.
55. Zheng, C., Feinstein, P., Bozza, T., Rodriguez, I. and Mombaerts, P. (2000). Peripheral olfactory projections are differentially affected in mice deficient in a cyclic nucleotide-gated channel subunit. Neuron 26, 81-91.