Wiring olfaction: The cellular and molecular mechanisms that guide the development of synaptic connections from the nose to the cortex

Frontiers in Neuroscience

Volumn 3, Issue DEC, 2009, Pages

  De Castro, Fernando ^a  

^a HOSPITAL NACIONAL DE PARAPLÉJICOS   (Spain)

Author keywords

Anosmin 1; Cell adhesion molecule; Chemotropism; Netrin; Olfactory cortex; Semaphorin; Slit

Indexed keywords

EID: 79955419606     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/neuro.22.004.2009     Document Type: Review

References (228)

1. Akins, M. R., Benson, D. L., and Greer, C. A. (2007). Cadherin expression in the developing mouse olfactory system. J. Comp. Neurol. 501, 483-497.
2. Akins, M. R., and Greer, C. A. (2006). Axon behavior in the olfactory nerve reflects the involvement of catenin-cadherin mediated adhesion. J. Comp. Neurol. 499, 979-989.
3. Alenius, M., and Bohm, S. (2003). Differential function of RNCAM isoforms in precise target selection of olfactory sensory neurons. Development 130, 917-927.
4. Alonso, M., Ortega-Pérez, I., Grubb, M. S., Bourgeois, J. P., Charneau, P., and Lledó, P. M. (2008). Turning astrocytes from the rostral migratory stream into neurons: a role for the olfactory sensory organ. J. Neurosci. 28, 11089-11102.
5. Alonso, M., Viollet, C., Gabellec, M. M., Meas-Yedid, V., Olivo-Marín, J. C., and Lledó, P. M. (2006). Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J. Neurosci. 26, 10508-10513.
6. Aoki, K., Ankara, Y., Yamada, S., and Eto, K. (1999). Role of polysialic acid on outgrowth of rat olfactory receptor neurons. Mech. Dev. 85, 103-110.
7. Ardiles, Y., de la Puente, R., Toledo, R., Isgor, C., and Guthrie, K. (2007). Response of olfactory axons to loss of synaptic targets in the adult mouse. Exp. Neurol. 207, 275-288.
8. Armentano, M., Filosa, A., Andolfi, G., and Studer, M. (2006). COUP-TFI is required for the formation of commissural projections in the forebrain by regulating axonal growth. Development 133, 4151-4162.
9. Astic, L., Pellier-Monnin, V., Saucier, D., Charrier, C., and Mehlen, P. (2002). Expression of netrin-1 and netrin-1 receptor, DCC, in the rat olfactory nerve pathway during development and axonal regeneration. Neuroscience 109, 643-656.
10. Baker, H., Cummings, D. M., Munger, S. D., Margolis, J. W., Franzen, L., Reed, R. R., and Margolis, F. L. (1999). Targeted deletion of a cyclic nucleotide-gated channel subunit (OCNC1): biochemical and morphological consequences in adult mice. J. Neurosci. 19, 9313-9321.
11. Barnea, G., O'Donnell, S., Mancia, F., Sun, X., Nemes, A., Mendelsohn, M., and Axel, R. (2004). Odorant receptors on axon termini in the brain. Science 304, 1468.
12. Barresi, M. J., Hutson, L. D., Chien, C. B., and Karlstrom, R. O. (2005). Hedgehog regulated Slit expression determines commissure and glial cell position in the zebrafish forebrain. Development 132, 3643-3656.
13. Bayer, S. A. (1983). 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp. Brain Res. 50, 329-340.
14. Belluscio, L., Gold, G. H., Nemes, A., and Axel, R. (1998). Mice deficient in G(olf) are anosmic. Neuron 20, 69-81.
15. Belluzzi, O., Benedusi, M., Ackman, J., and LoTurco, J. J. (2003). Electrophysiological differentiation of new neurons in the olfactory bulb. J. Neurosci. 23, 10411-10418.
16. Biju, K. C., Marks, D. R., Mast, T. G., and Fadool, D. A. (2008). Deletion of voltage-gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system. J. Comp. Neurol. 506, 161-179.
17. Blanchart, A., De Carlos, J. A., and López-Mascaraque, L. (2006). Time frame of mitral cell development in the mice olfactory bulb. J. Comp. Neurol. 496, 529-543.
18. Bonfanti, L. (2006). PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog. Neurobiol. 80, 129-164.
19. Briançon-Marjollet, A., Ghogha, A., Nawabi, H., Triki, I., Auziol, C., Fromont, S., Piché, C., Enslen, H., Chebli, K., Cloutier, J. F., Castellani, V., Debant, A., and Lamarche-Vane, N. (2008). Trio mediates netrin-1-induced Rac1 activation in axon outgrowth and guidance. Mol. Cell. Biol. 28, 2314-2323.
20. Brodal, P. (2004). The Central Nervous System: Structure and Function. Oxford, Oxford University Press.
21. Buck, L., and Axel, R. (1991). A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175-187.
22. Buck, L. B. (2000). The molecular architecture of odor and pheromone sensing in mammals. Cell 100, 611-618.
23. Bulfone, A., Wang, F., 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.
24. Cajal, S. R. (1890). Origen y terminación de las fibras nerviosas olfatorias. Gac. San. Barcelona. 3, 133-139, 174-181, 206-212.
25. Carleton, A., Petreanu, L. T., Lansford, R., Álvarez-Buylla, A., and Lledó, P. M. (2003). Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6, 507-518.
26. Carson, C., Saleh, M., Fung, F. W., Nicholson, D. W., and Roskams, A. J. (2005). Axonal dynactin p150Glued transports caspase-8 to drive retrograde olfactory receptor neuron apoptosis. J. Neurosci. 25, 6092-6104.
27. Caviness, V. S. Jr., and Sidman, R. L. (1972). Olfactory structures of the forebrain in the reeler mutant mouse. J. Comp. Neurol. 145, 85-104.
28. Chehrehasa, F., St John, J. A., and Key, B. (2006). Implantation of a scaffold following bulbectomy induces laminar organization of regenerating olfactory axons. Brain Res. 1119, 58-64.
29. Chen, Y., and Flanagan, J. G. (2006). Follow your nose: axon pathfinding in olfactory map formation. Cell 127, 881-884.
30. Chen, H., Bagri, A., Zupicich, J. A., Zou, Y., Stoeckli, E., Pleasure, S. J., Lowenstein, D. H., Skarnes, W. C., Chédotal, A., and Tessier-Lavigne, M. (2000). Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 25, 43-56.
31. Chen, L., Liao, G., Waclaw, R. R., Burns, K. A., Linquist, D., Campbell, K., Zheng, Y., and Kuan, C. Y. (2007). Rac1 controls the formation of midline commissures and the competency of tangential migration in ventral telencephalic neurons. J. Neurosci. 27, 3884-3893.
32. Chesler, A. T., Zou, D. J., Le Pichon, C. E., Peterlin, Z. A., Matthews, G. A., Pei, X., Miller, M. C., and Firestein, S. (2007). A G protein/cAMP signal cascade is required for axonal convergence into olfactory glomeruli. Proc. Natl. Acad. Sci. U.S.A. 104, 1039-1044.
33. Cho, H., Lépine, M., Andrews, W., Parnavelas, J., and Cloutier, J. F. (2007). Requirement for Slit-1 and Robo-2 in zonal segregation of olfactory sensory neuron axons in the main olfactory bulb. J. Neurosci. 27, 9094-9104.
34. Cloutier, J. F., Giger, R. J., Koentges, G., Dulac, C., Kolodkin, A. L., and Ginty, D. D. (2002). Neuropilin-2 mediates axonal fasciculation, zonal segregation, but not axonal convergence, of primary accessory olfactory neurons. Neuron 33, 877-892.
35. Cloutier, J. F., Sahay, A., Chang, E. C., Tessier-Lavigne, M., Dulac, C., Kolodkin, A. L., and Ginty, D. D. (2004). Differential requirements for semaphorin 3F and Slit-1 in axonal targeting, fasciculation, and segregation of olfactory sensory neuron projections. J. Neurosci. 24, 9087-9096.
36. Colón-Ramos, D. A., and Shen, K. (2008). Cellular conductors: glial cells as guideposts during neural circuit development. PLoS Biol. 6, e112. doi: 10.1371/journal.pbio.0060112.
37. Conzelmann, S., Malun, D., Breer, H., and Strotmann, J. (2001). Brain targeting and glomerulus formation of two olfactory neuron populations expressing related receptor types. Eur. J. Neurosci. 14, 1623-1632.
38. Costanzo, R. M. (2000). Rewiring the olfactory bulb: changes in odor maps following recovery from nerve transection. Chem. Senses 25, 199-205.
39. Cummings, D. M., Malun, D., and Brunjes, P. C. (1997). Development of the anterior commissure in the opossum: midline extracellular space and glia coincide with early axon decussation. J. Neurobiol. 32, 403-414
40. Cutforth, T., Moring, L., Mendelsohn, M., Nemes, A., Shah, N. M., Kim, M. M., Frisén, J., and Axel, R. (2003). Axonal ephrin-As and odorant receptors: coordinate determination of the olfactory sensory map. Cell 114, 311-322.
41. Dal Col, J. A., Matsuo, T., Storm, D. R., and Rodriguez, I. (2007). Adenylyl cyclase-dependent axonal targeting in the olfactory system. Development 134, 2481-2489.
42. De Castro, F. (2001). Moléculas quimiotrópicas como mecanismo de orientación del crecimiento axonal y de la migración neuronal durante el desarrollo del sistema nervioso de los mamíferos. Rev. Neurol. 33, 54-68.
43. de Castro, F., Hu, L., Drabkin, H., Sotelo, C., and Chédotal, A. (1999). Chemoattraction and chemorepulsion of olfactory bulb axons by different secreted semaphorins. J. Neurosci. 19, 4428-4436.
44. Derer, P., Caviness, V.S. Jr., and Sidman, R. L. (1977). Early cortical histogenesis in the primary olfactory cortex of the mouse. Brain Res. 123, 27-40.
45. Devor, M. (1976). Fiber trajectories of olfactory bulb efferents in the hamster. J. Comp. Neurol. 166, 31-48.
46. Dodé, C., and Hardelin, J. P. (2009). Kallmann syndrome. Eur. J. Hum. Genet. 17, 139-146.
47. Dottori, M., Hartley, L., Galea, M., Paxinos, G., Polizzotto, M., Kilpatrick, T., Bartlett, P. F., Murphy, M., Köntgen, F., and Boyd, A. W. (1998). EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract. Proc. Natl. Acad. Sci. U.S.A. 95, 13248-13253.
48. Doucette, R. (1989). Development of the nerve fiber layer in the olfactory bulb of mouse embryos. J. Comp. Neurol. 285, 514-527.
49. Dulac, C., and Torello, A. T. (2003). Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat. Rev. Neurosci. 7, 551-562.
50. Elsaesser, R., and Paysan, J. (2007). The sense of smell, its signalling pathways, and the dichotomy of cilia and microvilli in olfactory sensory cells. BMC Neurosci. 8, S1.
51. Falk, J., Bechara, A., Fiore, R., Nawabi, H., Zhou, H., Hoyo-Becerra, C., Bozon, M., Rougon, G., Grumet, M., Püschel, A. W., Sanes, J. R., and Castellani, V. (2005). Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 48, 63-75.
52. Fantana, A. L., Soucy, E. R., and Meister, M. (2008). Rat olfactory bulb mitral cells receive sparse glomerular inputs. Neuron 59, 802-814.
53. Fazeli, A., Dickinson, S. L., Hermiston, M. L., Tighe, R. V., Steen, R. G., Small, C. G., Stoeckli, E. T., Keino-Masu, K., Masu, M., Rayburn, H., Simons, J., Bronson, R. T., Gordon, J. I., Tessier-Lavigne, M., and Weinberg, R. A. (1997). Phenotype of mice lacking functional deleted in colorectal cancer (Dcc) gene. Nature 386, 796-804.
54. Feinstein, P., Bozza, T., Rodriguez, I., Vassalli, A., and Mombaerts, P. (2004). Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell 117, 833-846.
55. Feinstein, P., and Mombaerts, P. (2004). A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117, 817-831.
56. Feldheim, D. A., Kim, Y. I., Bergemann, A. D., Frisén, J., Barbacid, M., and Flanagan, J. G. (2000). Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25, 563-574.
57. Firestein, S. (2001). How the olfactory system makes sense of scents. Nature 413, 211-218.
58. Fleischmann, A., Shykind, B. M., Sosulski, D. L., Franks, K. M., Glinka, M. E., Mei, D. F., Sun, Y., Kirkland, J., Mendelsohn, M., Albers, M. W., and Axel, R. (2008). Mice with a "monoclonal nose": perturbations in an olfactory map impair odor discrimination. Neuron 60, 1068-1681.
59. Fouquet, C., Di Meglio, T., Ma, L., Kawasaki, T., Long, H., Hirata, T., Tessier-Lavigne, M., Chédotal, A., and N'Guyen-Ba-Charvet, K. T. (2007). Robo1 and robo2 control the development of the lateral olfactory tract. J. Neurosci. 27, 3037-3045.
60. Fukuchi-Shimogori, T., and Grove, E. A. (2001). Neocortex patterning by the secreted signaling molecule FGF8. Science 294, 1071-1074.
61. Geffen, M. N., Broome, B. M., Laurent, G., and Meister, M. (2009). Neural encoding of rapidly fluctuating odors. Neuron 61, 570-586.
62. Giacobini, P., Messina, A., Wray, S., Giampietro, C., Crepaldi, T., Carmeliet, P., and Fasolo, A. (2007). Hepatocyte growth factor acts as a motogen and guidance signal for gonadotropin hormone-releasing hormone-1 neuronal migration. J. Neurosci. 27, 431-445.
63. Gianola, S., de Castro, F., and Rossi, F. (2009). Anosmin-1 stimulates outgrowth and branching of developing Purkinje axons. Neuroscience 158, 570-584.
64. Giger, R. J., Cloutier, J. F., Sahay, A., Prinjha, R. K., Levengood, D. V., Moore, S. E., Pickering, S., Simmons, D., Rastan, S., Walsh, F. S., Kolodkin, A. L., Ginty, D. D., and Geppert, M. (2000). Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins. Neuron 25, 29-41.
65. Gogos, J. A., Osborne, J., Nemes, A., Mendelsohn, M., and Axel, R. (2000). Genetic ablation and restoration of the olfactory topographic map. Cell 103, 609-620.
66. Goldman, S. A., and Luskin, M. B. (1998). Strategies utilized by migrating neurons of the postnatal vertebrate forebrain. Trends Neurosci. 21, 107-114.
67. Gong, Q., and Shipley, M. T. (1996). Expression of extracellular matrix molecules and cell surface molecules in the olfactory nerve pathway during early development. J. Comp. Neurol. 366, 1-14.
68. Graziadei, P. P., and Monti-Graziadei, G. A. (1980). Neurogenesis and neuron regeneration in the olfactory system of mammals. III. Deafferentation and reinnervation of the olfactory bulb following section of the fila olfactoria in rat. J. Neurocytol. 9, 145-162.
69. Graziadei, P. P., and Monti Graziadei, G. A. (1986). Neuronal changes in the forebrain of mice following penetration by regenerating olfactory axons. J. Comp. Neurol. 247, 344-356.
70. Greer, C. A. (1991). Structural organization of the olfactory system. In Smell and Taste in Health and Disease, T.V. Getchell, R.L. Doty, L.M. Bartoshuk and J.B. Snow Jr., eds (New York, Raven), pp. 65-81.
71. Greferath, U., Canty, A. J. Messenger, J., and Murphy, M. (2002). Developmental expression of EphA4-tyrosine kinase receptor in the mouse brain and spinal cord. Mech. Dev. 119, S231-S238.
72. Grubb, M. S., Nissant, A., Murray, K., and Lledó, P. M. (2008). Functional maturation of the first synapse in olfaction: development and adult neurogenesis. J. Neurosci. 28, 2919-2932.
73. Ha, H. Y., Cho, I. H., Lee, K. W., Lee, K. W., Song, J. Y., Kim, K. S., Yu, Y. M., Lee, J. K., Song, J. S., Yang, S. D., Shin, H. S., and Han, P. L. (2005). The axon guidance defect of the telencephalic commissures of the JSAP1-deficient brain was partially rescued by the transgenic expression of JIP1. Dev. Biol. 277, 184-199.
74. Halpern, M. (1987). The organization and function of the vomeronasal system. Annu. Rev. Neurosci. 10, 325-362.
75. Henion, T. R., and Schwarting, G. A. (2007). Patterning the developing and regenerating olfactory system. J. Cell. Physiol. 210, 290-297.
76. Henion, T. R., Raitcheva, D., Grosholz, R., Biellmann, F., Skarnes, W. C., Hennet, T., and Schwarting, G. A. (2005). Beta1,3-N-acetylglucosaminyltransferase 1 glycosylation is required for axon pathfinding by olfactory sensory neurons. J. Neurosci. 25, 1894-1903.
77. Henkemeyer, M., Orioli, D., Henderson, J. T., Saxton, T. M., Roder, J., Pawson, T., and Klein, R. (1996). Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86, 35-46.
78. Heyden, A., Angenstein, F., Sallaz, M., Seidenbecher, C., and Montag, D. (2008). Abnormal axonal guidance and brain anatomy in mouse mutants for the cell recognition molecules close homolog of L1 and NgCAM-related cell adhesion molecule. Neuroscience 155, 221-233.
79. Hinds, J. W. (1968). Autoradiographic study of histogenesis in the mouse olfactory bulb. II. Cell proliferation and migration. J. Comp. Neurol. 134, 305-322.
80. Hirata, T., and Fujisawa, H. (1997). Cortex-specific distribution of membrane-bound factors that promote neurite outgrowth of mitral cells in culture. J. Neurobiol. 32, 415-425.
81. Hirata, T., and Fujisawa, H. (1999). Environmental control of collateral branching and target invasion of mitral cell axons during development. J. Neurobiol. 38, 93-104.
82. Hirata, T., Fujisawa, H., Wu, J. Y., and Rao, Y. (2001). Short-range guidance of olfactory bulb axons is independent of repulsive factor slit. J. Neurosci. 21, 2373-2379.
83. Ho, S. K., Kovacevic, N., Henkelman, R. M., Boyd, A., Pawson, T., and Henderson, J. T. (2009). EphB2 and EphA4 receptors regulate formation of the principal inter-hemispheric tracts of the mammalian forebrain. Neuroscience 160, 784-795.
84. Holmberg, J., and Frisén, J. (2002). Ephrins are not only unattractive. Trends Neurosci. 25, 239-243.
85. Imai, T., and Sakano, H. (2008). Interhemispheric olfactory circuit and the memory beyond. Neuron 58, 465-467.
86. Imai, T., Suzuki, M., and Sakano, H. (2006). Odorant receptor-derived cAMP signals direct axonal targeting. Science 314, 657-661.
87. Inaki, K., Nishimura, S., Nakashiba, T., Itohara, S., and Yoshihara, Y. (2004). Laminar organization of the developing lateral olfactory tract revealed by differential expression of cell recognition molecules. J. Comp. Neurol. 479, 243-256.
88. Ito, K., Kawasaki, T., Takashima, S., Matsuda, I., Aiba, A., and Hirata, T. (2008). Semaphorin 3F confines ventral tangential migration of lateral olfactory tract neurons onto the telencephalon surface. J. Neurosci. 28, 4414-4422.
89. Iwema, C. L., and Schwob, J. E. (2003). Odorant receptor expression as a function of neuronal maturity in the adult rodent olfactory system. J. Comp. Neurol. 459, 209-222.
90. Jhaveri, D., Saharan, S., Sen, A., and Rodrigues, V. (2003). Positioning sensory terminals in the olfactory lobe of Drosophila by Robo signalling. Development 131, 1903-1912.
91. Jiménez, D., García, C., de Castro, F., Chédotal, A., Sotelo, C., De Carlos, J. A., Valverde, F., and López-Mascaraque, L. (2000). Evidence for intrinsic development of olfactory structures in Pax-6 mutant mice. J. Comp. Neurol. 428, 511-526.
92. Kalil, K., Szebenyi, G., and Dent, E. W. (2000). Common mechanisms underlying growth cone guidance and axon branching. J. Neurobiol. 44, 145-158.
93. Kaneko-Goto, T., Yoshihara, S., Miyazaki, H., and Yoshihara, Y. (2008). BIG-2 mediates olfactory axon convergence to target glomeruli. Neuron 57, 834-846.
94. Kassai, H., Terashima, T., Fukaya, M., Nakao, K., Sakahara, M., Watanabe, M., and Aiba, A. (2008). Rac1 in cortical projection neurons is selectively required for midline crossing of commissural axonal formation. Eur. J. Neurosci. 28, 257-267.
95. Kawakami, A., Kitsukawa, T., Takagi, S., and Fujisawa, H. (1996). Developmentally regulated expression of a cell surface protein neuropilin in the mouse nervous system. J. Neurobiol. 29, 1-17.
96. Kawasaki, T., Ito, K., and Hirata, T. (2006). Netrin 1 regulates ventral tangential migration of guidepost neurons in the lateral olfactory tract. Development 133, 845-853.
97. Kitsukawa, T., Shimizu, M., Sanbo, M., Hirata, T., Taniguchi, M., Bekku, Y., Yagi, T., and Fujisawa, H. (1997). Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19, 995-1005.
98. Knöll, B., Schmidt, H., Andrews, W., Guthrie, S., Pini, A., Sundaresan, V., and Drescher, U. (2003). On the topographic targeting of basal vomeronasal axons through Slit-mediated chemorepulsion. Development 130, 5073-5082.
99. Kullander, K., Mather, N. K., Diella, F., Dottori, M., Boyd, A. W., and Klein, R. (2001). Kinase-dependent and kinase-independent functions of EphA4 receptors in major axon tract formation in vivo. Neuron 29, 73-84.
100. Lee, W., Cheng, T. W., and Gong, Q. (2008). Olfactory sensory neuron-specific and sexually dimorphic expression of protocadherin 20. J. Comp. Neurol. 507, 1076-1086.
101. Lemasson, M., Saghatelyan, A., Olivo-Marín, J. C., and Lledó, P. M. (2005). Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J. Neurosci. 25, 6816-6825.
102. Li, H. S., Chen, J. H., Wu, W., Fagaly, T., Zhou, L., Yuan, W., Dupuis, S., Jiang, Z. H., Nash, W., Gick, C., Ornitz, D. M., Wu, J. Y., and Rao, Y. (1999). Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96, 807-818.
103. Li, M., and Ransohoff, R. M. (2008). Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog. Neurobiol. 84, 116-131.
104. 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.
105. Lipscomb, B. W., Treloar, H. B., Klenoff, J., and Greer, C. A. (2003). Cell surface carbohydrates and glomerular targeting of olfactory sensory neuron axons in the mouse. J. Comp. Neurol. 467, 22-31.
106. Lledó, P. M., Merkle, F. T., and Álvarez-Buylla, A. (2008). Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 31, 392-400.
107. Lois, C., and Álvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148.
108. López-Mascaraque, L., and de Castro, F. (2002). The olfactory bulb as an independent developmental domain. Cell Death Differ. 9, 1279-1286.
109. López-Mascaraque, L., and de Castro, F. (2004). Protocortex versus protomap: a perspective from the olfactory bulb. Rev. Neurol. 39, 146-155.
110. López-Mascaraque, L., De Carlos, J. A., and Valverde, F. (1996). Early onset of the rat olfactory bulb projections. Neuroscience 70, 255-266.
111. Luskin, M. B. (1993). Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11, 173-189.
112. Luskin, M. B., and Price, J. L. (1982). The distribution of axon collaterals from the olfactory bulb and the nucleus of the horizontal limb of the diagonal band to the olfactory cortex demonstrated by double retrograde labeling techniques. J. Comp. Neurol. 209, 249-263.
113. Luxenhofer, G., Breer, H., and Strotmann, J. (2008). Differential reaction of outgrowing olfactory neurites monitored in explant culture. J. Comp. Neurol. 509, 580-593.
114. Ma, L., and Tessier-Lavigne, M. (2007). Dual branch-promoting and branch-repelling actions of Slit/Robo signaling on peripheral and central branches of developing sensory axons. J. Neurosci. 27, 6843-6851.
115. Malnic, B., Hirono, J., Sato, T., and Buck, L. B. (1999). Combinatorial receptor codes for odors. Cell 96, 713-723.
116. Mandairon, N., Sacquet, J., Jourdan, F., and Didier, A. (2006). Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: influences of olfactory deprivation. Neuroscience 141, 443-451.
117. Mann, F., Ray, S., Harris, W., and Holt, C. (2002). Topographic mapping in dorsoventral axis of the Xenopus retinotectal system depends on signaling through ephrin-B ligands. Neuron 35, 461-473.
118. Maresh, A., Rodríguez Gil, D., Whitman, M. C., and Greer, C. A. (2008). Principles of glomerular organization in the human olfactory bulb-implications for odor processing. PLoS ONE 3, e2640. doi: 10.1371/journal.pone.0002640.
119. Marillat, V., Cases, O., N'Guyen-Ba-Charvet, K. T., Tessier-Lavigne, M., Sotelo, C., and Chedotal, A. (2002). Spatiotemporal expression patterns of slit and robo genes in the rat brain. J. Comp. Neurol. 442, 130-155.
120. Marín, O., and Rubenstein, J. L. (2003). Cell migration in the forebrain. Annu. Rev. Neurosci. 26, 441-483.
121. Martínez-Marcos, A. (2009). On the organization of olfactory and vomeronasal cortices. Prog. Neurobiol. 87, 21-30.
122. Mombaerts, P. (1996). Targeting olfaction. Curr. Opin. Neurobiol. 6, 481-486.
123. Mombaerts, P. (2001). How smell develops. Nat. Neurosci. 4(Suppl.), 1192-1198.
124. Mombaerts, P. (2006). Axonal wiring in the mouse olfactory system. Annu. Rev. Cell Dev. Biol. 22, 713-737.
125. Mouret, A., Gheusi, G., Gabellec, M. M., de Chaumont, F., Olivo-Marin, J. C., and Lledó, P. M. (2008). Learning and survival of newly generated neurons: when time matters. J. Neurosci. 28, 11511-11516.
126. Mouret, A., Lepousez, G., Gras, J., Gabellec, M. M., and Lledó, P. M. (2009). Turnover of newborn olfactory bulb neurons optimizes olfaction. J. Neurosci. 29, 12302-12314.
127. Nacher, J., Alonso-Llosa, G., Rosell, D., and McEwen, B. (2002a). PSA-NCAM expression in the piriform cortex of the adult rat. Modulation by NMDA receptor antagonist administration. Brain Res. 927, 111-121.
128. Nacher, J., Lanuza, E., and McEwen, B. S. (2002b). Distribution of PSA-NCAM expression in the amygdale of the adult rat. Neuroscience 113, 479-484.
129. Nakashiba, T., Ikeda, T., Nishimura, S., Tashiro, K., Honjo, T., Culotti, J. G., and Itohara, S. (2000). Netrin-G1:anovel glycosyl phosphatidylinositol-linkedmammalian netrin that is functionally divergent from classical netrins. J. Neurosci. 20, 6540-6550.
130. N'Guyen-Ba-Charvet, K. T., Brose, K., Ma, L., Wang, K. H., Marillat, V., Sotelo, C., Tessier-Lavigne, M., and Chédotal A. (2001). Diversity and specificity of actions of Slit2 proteolytic fragments in axon guidance. J. Neurosci. 21, 4281-4289.
131. N'Guyen-Ba-Charvet, K. T., Brose, K., Marillat, V., Kidd, T., Goodman, C. S., Tessier-Lavigne, M., Sotelo, C., and Chédotal, A. (1999). Slit2-mediated chemorepulsion and collapse of developing forebrain axons. Neuron 22, 463-473.
132. N'Guyen-Ba-Charvet, K. T., Di Meglio, T., Fouquet, C., and Chédotal, A. (2008). Robos and slits control the pathfinding and targeting of mouse olfactory sensory axons. J. Neurosci. 28, 4244-4249.
133. N'Guyen-Ba-Charvet, K. T., Plump, A. S., Tessier-Lavigne, M., and Chedotal, A. (2002). Slit1 and slit2 proteins control the development of the lateral olfactory tract. J. Neurosci. 22, 5473-5480.
134. Nomura, T., and Osumi, N. (2004). Misrouting of mitral cell progenitors in the Pax6/small eye rat telencephalon. Development 131, 787-796.
135. O'Leary, D. D. (1989). Do cortical areas emerge from a protocortex? Trends Neurosci. 12, 400-406.
136. Orioli, D., Henkemeyer, M., Lemke, G., Klein, R., and Pawon, T. (1996). Sek4 and Nuk receptors cooperate in guidance of commissural axons and in palate formation. EMBO J. 15, 6035-6049.
137. Pasterkamp, R. J., Peschon, J. J., Spriggs, M. K., and Kolodkin, A. L. (2003). Semaphorin 7A promotes axon outgrowth through integrins and MAPKs. Nature 424, 398-405.
138. Patel, K., Nash, J. A., Itoh, A., Liu, Z., Sundaresan, V., and Pini, A. (2001). Slit proteins are not dominant chemorepellents for olfactory tract and spinal motor axons. Development 128, 5031-5037.
139. Paxinos, G. (2004). The Rat Nervous System, 3rd edn. London, Elsevier Academic Press.
140. Petreanu, L., and Álvarez-Buylla, A. (2002). Maturation and death of adultborn olfactory bulb granule neurons: role of olfaction. J. Neurosci. 22, 6106-6113.
141. Pini A. (1993). Chemorepulsion of axons in the developing mammalian central nervous system. Science 261, 95-98.
142. Pires-Neto, M. A., and Lent, R. (1993). The prenatal development of the anterior commissure in hamsters: pioneer fibers lead the way. Brain Res. Dev. Brain Res. 72, 59-66.
143. Potter, S. M., Zheng, C., Koos, D. S., Feinstein, P., Fraser, S. E., and Mombaerts, P. (2001). Structure and emergence of specific olfactory glomeruli in the mouse. J. Neurosci. 21, 9713-9723.
144. Price, D. J., Kennedy, H., Dehay, C., Zhou, L., Mercier, M., Jossin, Y., Goffinet, A. M., Tissir, F., Blakey, D., and MolnÁr, Z. (2006). The development of cortical connections. Eur. J. Neurosci. 23, 910-920.
145. Priest, C. A., and Puche, A. C. (2004). GABAB receptor expression and function in olfactory receptor neuron axon growth. J. Neurobiol. 60, 154-165.
146. Przyborski, S. A., Knowles, B. B., and Ackerman, S. L. (1998). Embryonic phenotype of Unc5h3 mutant mice suggests chemorepulsion during the formation of the rostral cerebellar boundary. Development 125, 41-50.
147. Rakic, P. (1988). Specification of cerebral cortical areas. Science 241, 170-176.
148. Rakic, P., Ayoub, A. E., Breunig, J. J., and Domínguez, M. H. (2009). Decision by division: making cortical maps. Trends Neurosci. 32, 291-301.
149. Reed, R. R. (2004). After the holy grail: establishing a molecular basis for mammalian olfaction. Cell 116, 329-336.
150. Ren, T., Anderson, A., Shen, W. B., Huang, H., Plachez, C., Zhang, J., Mori, S., Kinsman, S. L., and Richards, L. J. (2006). Imaging, anatomical, and molecular analysis of callosal formation in the developing human fetal brain. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 288, 191-204.
151. Renzi, M. J., Wexler, T. L., and Raper, J. A. (2000). Olfactory sensory axons expressing a dominant-negative semaphorin receptor enter the CNS early and overshoot their target. Neuron 28, 437-447.
152. Rochefort, C., Gheusi, G., Vincent, J. D., and Lledó, P. M. (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679-2689.
153. Rodriguez-Gil, D. J., and Greer, C. A. (2008). Wnt/Frizzled family members mediate olfactory sensory neuron axon extension. J. Comp. Neurol. 511, 301-317.
154. Saha, B., Hari, P., Huilgol, D., and Tole, S. (2007). Dual role for LIM-homeodomain gene Lhx2 in the formation of the lateral olfactory tract. J. Neurosci. 27, 2290-2297.
155. Sahay, A., Molliver, M. E., Ginty, D. D., and Kolodkin, A. L. (2003). Semaphorin 3F is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events. J. Neurosci. 23, 6671-6680.
156. Santacana, M., Heredia, M., and Valverde, F. (1992). Transient pattern of exuberant projections of olfactory axons during development in the rat. Brain Res. Dev. Brain Res. 70, 213-222.
157. Sarnat, H. B. (2007). Embryology and malformations of the forebrain commissures. Handb. Clin. Neurol. 87, 67-87.
158. Sarnat, H. B., and Flores-Sarnat, L. (2001). Neuropathologic research strategies in holoprosencephaly. J. Child Neurol. 16, 918-931.
159. Sato, Y., Hirata, T., Ogawa, M., and Fujisawa, H. (1998). Requirement for early-generated neurons recognized by monoclonal antibody lot1 in the formation of lateral olfactory tract. J. Neurosci. 18, 7800-7810.
160. Schwarting, G. A., and Henion, T. R. (2008). Olfactory axon guidance: the modified rules. J. Neurosci. Res. 86, 11-17.
161. Schwarting, G. A., Kostek, C., Ahmad, N., Dibble, C., Pays, L., and Püschel, A. W. (2000). Semaphorin 3A is required for guidance of olfactory axons in mice. J. Neurosci. 20, 7691-7697.
162. Schwarting, G. A., Raitcheva, D., Bless, E. P., Ackerman, S. L., and Tobet, S. (2004). Netrin 1-mediated chemoattraction regulates the migratory pathway of LHRH neurons. Eur. J. Neurosci. 19, 11-20.
163. Schwob, J. E., and Price, J. L. (1984). The development of axonal connections in the central olfactory system of rats. J. Comp. Neurol. 223, 177-202.
164. Schwob, J. E., Szumowski, K. E., and Stasky, A. A. (1992). Olfactory sensory neurons are trophically dependent on the olfactory bulb for their prolonged survival. J. Neurosci. 12, 3896-3919.
165. Scolnick, J. A., Cui, K., Duggan, C. D., Xuan, S., Yuan, X. B., Efstratiadis, A., and Ngai, J. (2008). Role of IGF signaling in olfactory sensory map formation and axon guidance. Neuron 57, 847-857.
166. Scott, J. W., McBride, R. L., and Schneider, S. P. (1980). The organization of projections from the olfactory bulb to the piriform cortex and olfactory tubercle in the rat. J. Comp. Neurol. 194, 519-534.
167. Seki, T., and Arai, Y. (1991). Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat. Anat. Embryol. 184, 395-401.
168. Serafini, T., Colamarino, S. A., Leonardo, E. D., Wang, H., Beddington, R., Skarnes, W. C., and Tessier-Lavigne M. (1996). Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001-1014.
169. Serizawa, S., Miyamichi, K., Takeuchi, H., Yamagishi, Y., Suzuki, M., and Sakano, H. (2006). A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127, 1057-1069.
170. Shay, E. L., Greer, C. A., and Treloar, H. B. (2008). Dynamic expression patterns of ECM molecules in the developing mouse olfactory pathway. Dev. Dyn. 237, 1837-1850.
171. Shen, Y., Mani, S., Donovan, S. L., Schwob, J. E., and Meiri, K. F. (2002). Growth-associated protein-43 is required for commissural axon guidance in the developing vertebrate nervous system. J. Neurosci. 22, 239-247.
172. Shipley, M. T., and Adamek, G. D. (1984). The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res. Bull. 12, 669-688.
173. Shipley, M. T., and Ennis, M. (1996). Functional organization of olfactory system. J. Neurobiol. 30, 123-176.
174. Shipley, M. T., Ennis, M., and Puche, A. C. (2004). Olfactory system. In The Rat Nervous System, 3rd edn, G. Paxinos, ed. (London, Elsevier Academic Press), pp. 923-964.
175. Shu, T., Valentino, K. M., Seaman, C., Cooper, H. M., and Richards, L. J. (2000). Expression of the netrin-1 receptor deleted in colorectal cancer (DCC) is largely confined to projecting neurons in the developing forebrain. J. Comp. Neurol. 416, 201-212.
176. Silver, J., Lorenz, S. E., Wahlsten, D., and Coughlin, J. (1982). Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J. Comp. Neurol. 210, 10-29.
177. Soucy, E. R., Albeanu, D. F., Fantana, A. L., Murthy, V. N., and Meister, M. (2009). Precision and diversity in an odor map on the olfactory bulb. Nat. Neurosci. 12, 210-220.
178. Soussi-Yanicostas, N., de Castro, F., Julliard, K., Perfettini, I., Chédotal, A., and Petit, C. (2002). Anosmin-1 defective in the X-linked form of Kallmann syndrome promotes axonal branch formation from olfactory bulb output neurons. Cell 109, 217-228.
179. St John, J. A., Clarris, H. J., and Key, B. (2002). Multiple axon guidance cues establish the olfactory topographic map: how do these cues interact? Int. J. Dev. Biol. 46, 639-647.
180. St John, J. A., and Key, B. (2001). Chemically and morphologically identifiable glomeruli in the rat olfactory bulb. J. Comp. Neurol. 436, 497-507.
181. Stein, E., and Tessier-Lavigne, M. (2001). Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through Robo/DCC receptor complex. Science 291, 1928-1938.
182. Stoeckli, E. T., and Landmesser, L. T. (1995). Axonin-1 Nr-CAM and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. Neuron 14, 1165-1179.
183. Stoeckli, E. T., and Landmesser, L. T. (1998). Axon guidance at choice points. Curr. Opin. Neurobiol. 8, 73-79.
184. Strotmann, J., Levai, O., Fleischer, J., Schwarzenbacher, K., and Breer, H. (2004). Olfactory receptor proteins in axonal processes of chemosensory neurons. J. Neurosci. 24, 7754-7761.
185. Sugisaki, N., Hirata, T., Naruse, I., Kawakami, A., Kitsukawa, T., and Fujisawa, H. (1996). Positional cues that are strictly localized in the telencephalon induce preferential growth of mitral cell axons. J. Neurobiol. 29, 127-137.
186. Suto, F., Ito, K., Uemura, M., Shimizu, M., Shinkawa, Y., Sanbo, M., Shinoda, T., Tsuboi, M., Takashima, S., Yagi, T., and Fujisawa, H. (2005). Plexin-a4 mediates axon-repulsive activities of both secreted and transmembrane semaphorins and plays roles in nerve fiber guidance. J. Neurosci. 25, 3628-3637.
187. Szabo-Rogers, H. L., Geetha-Loganathan, P., Whiting, C. J., Nimmagadda, S., Fu, K., and Richman, J. M. (2009). Novel skeletogenic patterning roles for the olfactory pit. Development 136, 219-229.
188. Taniguchi, M., Nagao, H., Takahashi, Y. K., Yamaguchi, M., Mitsui, S., Yagi, T., Mori, K., and Shimizu, T. (2003). Distorted odor maps in the olfactory bulb of semaphorin 3A-deficient mice. J. Neurosci. 23, 1390-1397.
189. Teillon, S. M., Yiu, G., and Walsh, C. A. (2003). Reelin is expressed in the accessory olfactory system, but is not a guidance cue for vomeronasal axons. Brain Res. Dev. Brain Res. 140, 303-307.
190. Tessier-Lavigne, M., and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
191. Tissir, F., Bar, I., Jossin, Y., De Backer, O., and Goffinet, A. M. (2005). Protocadherin Celsr3 is crucial in axonal tract development. Nat. Neurosci. 8, 451-457.
192. Tiveron, M. C., and Cremer, H. (2008). CXCL12/CXCR4 signalling in neuronal cell migration. Curr. Opin. Neurobiol. 18, 237-244.
193. Toba, Y., Tiong, J. D., Ma, Q., and Wray, S. (2008). CXCR4/SDF-1 system modulates development of GnRH-1 neurons and the olfactory system. Dev. Neurobiol. 68, 487-503.
194. Tran, H., Chen, H., Walz, A., Posthumus, J. C., and Gong, Q. (2008). Influence of olfactory epithelium on mitral/tufted cell dendritic outgrowth. PLoS ONE 3, e3816. doi:10.1371/journal.pone.0003816.
195. Treloar, H. B., Feinstein, P., Mombaerts, P., and Greer, C. A. (2002). Specificity of glomerular targeting by olfactory sensory axons. J. Neurosci. 22, 2469-2477.
196. Treloar, H. B., Gabeau, D., Yoshihara, Y., Mori, K., and Greer, C. A. (2003). Inverse expression of olfactory cell adhesion molecule in a subset of olfactory axons and a subset of mitral/tufted cells in the developing rat main olfactory bulb. J. Comp. Neurol. 458, 389-403.
197. Treloar, H. B., Nurcombe, V., and Key, B. (1996). Expression of extracellular matrix molecules in the embryonic rat olfactory pathway. J. Neurobiol. 31, 41-55.
198. Treloar, H. B., Ray, A., Dinglasan, L. A., Schachner, M., and Greer, C. A. (2009). Tenascin-C is an inhibitory boundary molecule in the developing olfactory bulb. J. Neurosci. 29, 9405-9416.
199. Trinh, K., and Storm, D. R. (2003). Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat. Neurosci. 6, 519-525.
200. Valverde, F. (1965). Studies on the Piriform Lobe. Harvard, Harvard University Press.
201. Valverde, F., Santacana, M., and Heredia, M. (1992). Formation of an olfactory glomerulus: morphological aspects of development and organization. Neuroscience 49, 255-275.
202. Von Campenhausen, H., Yoshihara, Y., and Mori, K. (1997). OCAM reveals segregated mitral/tufted cell pathways in developing accessory olfactory bulb. Neuroreport 28, 2607-2612.
203. Walz, A., Mombaerts, P., Greer, C. A., and Treloar, H. B. (2006a). Disrupted compartmental organization of axons and dendrites within olfactory glomeruli of mice deficient in the olfactory cell adhesion molecule, OCAM. Mol. Cell Neurosci. 32, 1-14.
204. Walz, A., Omura, M., and Mombaerts, P. (2006b). Development and topography of the lateral olfactory tract in the mouse: imaging by genetically encoded and injected fluorescent markers. J. Neurobiol. 66, 835-846.
205. Walz, A., Rodriguez, I., and Mombaerts, P. (2002). Aberrant sensory innervation of the olfactory bulb in neuropilin-2 mutant mice. J. Neurosci. 22, 4025-4035.
206. Wang, K. H., Brose, K., Arnott, D., Kidd, T., Goodman, C. S., Henzel, W., and Tessier-Lavigne, M. (1999). Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96, 71-784.
207. Wang, Y., Thekdi, N., Smallwood, P. M., Macke, J. P., and Nathans, J. (2002). Frizzled-3 is required for the development of major fiber tracts in the rostral CNS. J. Neurosci. 22, 8563-8573.
208. Wang, Y., Zhang, J., Mori, S., and Nathans, J. (2006). Axonal growth and guidance defects in Frizzled3 knock-out mice: a comparison of diffusion tensor magnetic resonance imaging, neurofilament staining, and genetically directed cell labeling. J. Neurosci. 26, 355-364.
209. Watanabe, K., Tamamaki, N., Furuta, T., Ackerman, S. L., Ikenaka, K., and Ono, K. (2006). Dorsally derived netrin 1 provides an inhibitory cue and elaborates the 'waiting period' for primary sensory axons in the developing spinal cord. Development 133, 1379-1387.
210. Weiler, E., and Farbman, A. I. (1999). Mitral cell loss following lateral olfactory tract transection increases proliferation density in rat olfactory epithelium. Eur. J. Neurosci. 11, 3265-3275.
211. Whitesides, J. G., and LaMantia, A.-S. (1998). Differential adhesion and the initial assembly of the mammalian olfactory nerve. J. Comp. Neurol. 373, 240-254.
212. Wu, H. H., Ivkovic, S., Murray, R. C., Jaramillo, S., Lyons, K. M., Johnson, J. E., and Calof, A. L. (2003). Autoregulation of neurogenesis by GDF11. Neuron 37, 197-207.
213. Yamaguchi, M., and Mori, K. (2005). Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc. Natl. Acad. Sci. U.S.A. 102, 9697-9702.
214. Yamatani, H., Sato, Y., Fujisawa, H., and Hirata, T. (2004). Chronotopic organization of olfactory bulb axons in the lateral olfactory tract. J. Comp. Neurol. 475, 247-260.
215. Yoshihara, Y., Kawasaki, M., Tamada, A., Fujita, H., Hayashi, H., Kagamiyama, H., and Mori, K. (1997). OCAM: a new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons. J. Neurosci. 17, 5830-5842.
216. Yu, C. R., Power, J., Barnea, G., O'Donnell, S., Brown, H. E., Osborne, J., Axel, R., and Gogos, JA. (2004). Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42, 553-566.
217. Zhang, L. I., and Poo, M. M. (2001). Electrical activity and development of neural circuits. Nat. Neurosci. 4(SUPPL.), 1207-1214.
218. Zhang, X., and Firestein, S. (2002). The olfactory receptor gene superfamily of the mouse. Nat. Neurosci. 5, 124-133.
219. Zhao, H., and Reed, R. R. (2001). X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104, 651-660.
220. 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.
221. Zheng, J. Q., and Poo, M. M. (2007). Calcium signaling in neuronal motility. Annu. Rev. Cell. Dev. Biol. 23, 375-404.
222. Zhou, C., Qiu, Y., Pereira, F. A., Crair, M. C., Tsai, S. Y., and Tsai, M. J. (1999). The nuclear orphan receptor COUP-TFI is required for differentiation of subplate neurons and guidance of thalamocortical axons. Neuron 24, 847-859.
223. Zhou, L., Bar, I., Achouri, Y., Campbell, K., De Backer, O., Hebert, J. M., Jones, K., Kessaris, N., de Rouvroit, C. L., O'Leary, D., Richardson, W. D., Goffinet, A. M., and Tissir, F. (2008). Early forebrain wiring: genetic dissection using conditional Celsr3 mutant mice. Science 320, 946-949.
224. Zou, D. J., Chesler, A. T., Le Pichon, C. E., Kuznetsov, A., Pei, X., Hwang, E. L., and Firestein, S. (2007). Absence of adenylyl cyclase 3 perturbs peripheral olfactory projections in mice. J. Neurosci. 27, 6675-6683.
225. Zou, D. J., Feinstein, P., Rivers, A. L., Mathews, G. A., Kim, A., Greer, C. A., Mombaerts, P., and Firestein, S. (2004). Postnatal refinement of peripheral olfactory projections. Science 304, 1976-1979.
226. Zou, Y., Stoeckli, E., Chen, H., and Tessier-Lavigne, M. (2000). Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102, 363-375.
227. Zou, Z., Horowitz, L. F., Montmayeur, J. P., Snapper, S., and Buck, L. B. (2001). Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414, 173-179.
228. Zou, Z., Horowitz, L. F., Montmayeur, J. P., Snapper, S., and Buck, L. B. (2008). Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 452, 120.