Birth, Migration and Function of SVZ-derived Neurons in the Adult Brain

  • Minoree Kohwi
  • Rui Pedro Galvão
  • Arturo Alvarez-Buylla


Glial Fibrillary Acidic Protein Olfactory Bulb Neural Stem Cell Neural Cell Adhesion Molecule Ependymal Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Altman, J. (1969). Autoradiographic and Histological Studies of Postnatal Neurogenesis. IV. Cell Proliferation and Migration in The Anterior Forebrain., With Special Reference to Persisting Neurogenesis in The Olfactory Bulb. J. Comp. Neurol. 137: 433–45CrossRefPubMedGoogle Scholar
  2. Alvarez-Buylla, A., Theelen, M. and Nottebohm, F. (1990). Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division. Neuron 5: 101–109CrossRefPubMedGoogle Scholar
  3. Alvarez-Buylla, A., Garcia-Verdugo, J.M. and Tramontin, A.D. (2001). A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2(2):287–293.CrossRefPubMedGoogle Scholar
  4. Artavanis-Tsakonas S., Rand, M.D. and Lake, R.J. (1999). Notch signaling: Cell fate control and signal integration in development. Science 284: 770–776.CrossRefPubMedGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. Benraiss, A., Chmielnicki, E., Lerner, K., Roh, D. and Goldman, S.A. (2001). Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J. Neurosci. 21: 6718–6731.PubMedGoogle Scholar
  7. Bolteus, A.J. and Bordey, A. (2004). GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J. Neurosci. 24:7623–7631.CrossRefPubMedGoogle Scholar
  8. Bonfanti, L. and Theodosis, D.T. (1994). Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience 62: 291–305CrossRefPubMedGoogle Scholar
  9. Bonfanti, L., Peretto, P., Merighi, A. and Fasolo, A. (1997). Newly-generated cells from the rostral migratory stream in the accessory olfactory bulb of the adult rat. Neuroscience 81: 489–502CrossRefPubMedGoogle Scholar
  10. 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: 1273–128CrossRefPubMedGoogle Scholar
  11. Burek, M.J., Nordeen, K.W. and Nordeen, E.J. (1995). Estrogen promotes neuron addition to an avian song-control nucleus by regulating post-mitotic events. Dev. Brain Res. 85: 220–224CrossRefGoogle Scholar
  12. Campbell, K. and Gotz, M. (2002). Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci. 25: 235–238.CrossRefPubMedGoogle Scholar
  13. Capela, A. and Temple, S. (2002). LeX/ssea-1 is expressed by adult mouse CNS stem cells., identifying them as nonependymal. Neuron 35: 865–875.CrossRefPubMedGoogle Scholar
  14. Carleton, A., Petreanu, L.T., Lansford, R., Alvarez-Buylla, A. and Lledo, P.M. (2003). Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6:507–518.PubMedGoogle Scholar
  15. Cecchi, G.A., Petreanu, L.T., Alvarez-Buylla, A. and Magnasco, M.O. (2001). Unsupervised Learning and Adaptation in a Model of Adult Neurogenesis. J. Comput. Neurosci. 11: 175–182.CrossRefPubMedGoogle Scholar
  16. Chambers, C.B., Peng, Y., Nguyen, H., Gaiano, N., Fishell, G. and Nye, J.S. (2001). Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development 128: 689–702.PubMedGoogle Scholar
  17. Chazal, G., Durbec, P., Jankovski, A., Rougon, G. and Cremer, H. (2000). Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci. 20: 1446–1457PubMedGoogle Scholar
  18. Chen, W.R., Xiong, W. and Shepherd, G.M. (2000). Analysis of relations between NMDA receptors and GABA release at olfactory bulb reciprocal synapses. Neuron 25: 625–633CrossRefPubMedGoogle Scholar
  19. Chiasson, B.J., Tropepe, V., Morshead, C.M. and van der Kooy, D. (1999). Adult Mammalian Forebrain Ependymal and Subependymal Cells Demonstrate Proliferative Potential., but only Subependymal Cells Have Neural Stem Cell Characteristics. J. Neurosci. 19: 4462–447PubMedGoogle Scholar
  20. Conover, J.C., Doetsch, F., Garcia-Verdugo, J.M., Gale, N.W., Yancopoulos, G.D. and Alvarez-Buylla, A. (2000). Disruption of Eph/ephrin signaling affects migration and cell proliferation in the subventricular zone of the adult mouse brain. Nat. Neurosci. 3: 1091–109CrossRefPubMedGoogle Scholar
  21. Corotto, F.S., Henegar, J.R. and Maruniak, J.A. (1994). Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience 61: 739–744.CrossRefPubMedGoogle Scholar
  22. Craig, C.G., Tropepe, V., Morshead, C.M., Reynolds, B.A., Weiss, S. and van der Kooy, D. (1996). In vivo growth factor expansion of endogen oussu bependymal neural precursor cell population sintheadult mousebrain. J. Neurosci.16:2649–2658.PubMedGoogle Scholar
  23. Cremer, H., Lange, R., Christoph, A., Plomann, M., Vopper, G., Roes, J., Brown, R., Baldwin, S., Kraemer, P., Scheff, S., Barthels, D., Rajewsky, K. and Wille, W. (1994). Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367: 455–459.CrossRefPubMedGoogle Scholar
  24. Davis, S., Gale, N.W., Aldrich, T.H., Maisonpierre, P.C., Lhotak, V., Pawson, T., Goldfarb, M. and Yancopoulos, GD. (1994). Ligands for EPH-related receptor tyrosing kinases that require membrane attachment or clustering for activity. Science 266: 816–819.PubMedGoogle Scholar
  25. Doetsch, F. and Alvarez-Buylla, A. (1996). Network of tangential pathways for neuronal migration in adult mammalian brain. Proc. Natl. Acad. Sci. U. S. A. 93: 14895–14900.CrossRefPubMedGoogle Scholar
  26. Doetsch, F., Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (1997). Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17: 5046–5061.PubMedGoogle Scholar
  27. Doetsch, F., Caille, I., Lim, D.A., García-Verdugo, J.M. and Alvarez-Buylla, A. (1999). Subventricular Zone Astrocytes Are Neural Stem Cells in the Adult mammalian Brain Cell 97: 1–20.Google Scholar
  28. Doetsch, F., Petreanu, L., Caille, I., Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (2002). EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36: 1021–1034.CrossRefPubMedGoogle Scholar
  29. Emsley, J.G. and Hagg, T. (2003). alpha6beta1 integrin directs migration of neuronal precursors in adult mouse forebrain. Exp. Neurol. 183: 273–285.CrossRefPubMedGoogle Scholar
  30. Fallon, J., Reid, S., Kinyamu, R., Opole, I., Opole, R., Baratta, J., Korc, M., Endo, TL., Duong, A., Nguyen, G., Karkehabadhi, M., Twardzik, D. and Loughlin, S. (2000). In vivo induction of massive proliferation., directed migration., and differentiation of neural cells in the adult mammalian brain. Proc. Natl. Acad. Sci. U. S. A. 97: 14686–14691.CrossRefPubMedGoogle Scholar
  31. Ferri, AL., Cavallaro, M., Braida, D., Di Cristofano, A., Canta, A., Vezzani, A., Ottolenghi, S., Pandolfi, P.P., Sala, M., DeBiasi, S. and Nicolis, S.K. (2004). Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131: 3805–3819.CrossRefPubMedGoogle Scholar
  32. Fischer, A.J. and Reh, T.A. (2001). Muller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat. Neurosci. 4: 247–252.CrossRefPubMedGoogle Scholar
  33. Frazier-Cierpial, L. and Brunjes, P.C. (1989). Early postnatal cellular proliferation and survival in the olfactory bulb and rostral migratory stream of normal and unilaterally odor-deprived rats. J. Comp. Neurol. 289: 481–492.CrossRefPubMedGoogle Scholar
  34. Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet M-C, G., McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, Chelly J (1999) Doublecortin Is a Developmentally Regulated, Microtubule-Associated Protein Expressed in Migrating and Differentiating Neurons. Neuron 23:247–256.CrossRefPubMedGoogle Scholar
  35. Friedrich, R.W. and Laurent, G. (2001). Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 291: 889–894.CrossRefPubMedGoogle Scholar
  36. Gage, F.H. (2000). Mammalian neural stem cells. Science 287: 1433–1438.CrossRefPubMedGoogle Scholar
  37. Gage, F.H., Kempermann, G., Palmer, T., Peterson, D.A., Ray, J. (1998). Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol. 36: 249–266.CrossRefPubMedGoogle Scholar
  38. Gaiano, N., Nye, J.S., Fishell, G. (2000). Radial glial identity is promoted by notch1 signaling in the murine forebrain. Neuron 26: 395–404.CrossRefPubMedGoogle Scholar
  39. Garcia, A.D., Doan, N.B., Imura, T., Bush, T.G. and Sofroniew, M.V. (2004). GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat. Neurosci. 7: 1233–1241.CrossRefPubMedGoogle Scholar
  40. García-Verdugo, J.M., Doetsch, F., Wichterle, H., Lim, D.A. and Alvarez-Buylla, A. (1998). Architecture and cell types of the adult subventricular zone: in search of the stem cells. J. Neurobiol. 36: 234–248.CrossRefPubMedGoogle Scholar
  41. Geschwind, D.H., Ou, J., Easterday, M.C., Dougherty, J.D., Jackson, R.L., Chen, Z., Antoine, H., Terskikh, A., Weissman, I.L., Nelson, S.F. and Kornblum, H.I. (2001). A genetic analysis of neural progenitor differentiation. Neuron 29:325–339.CrossRefPubMedGoogle Scholar
  42. Gheusi, G., Cremer, H., McLean, H., Chazal, G., Vincent, J.D. and Lledo, P.M. (2000). Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl. Acad. Sci. U. S. A. 97: 1823–1828.CrossRefPubMedGoogle Scholar
  43. Gleeson, J.G., Lin, P.T., Flanagan, L. and Walsh, C. (1999). Doublecortin Is a Microtubule-Associated Protein and Is Expressed Widely by Migrating Neurons. Neuron 23: 257–271.CrossRefPubMedGoogle Scholar
  44. Gotz, M., Hartfuss, E. and Malatesta, P. (2002). Radial glial cells as neuronal precursors: a new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res. Bull. 57: 777–788.CrossRefPubMedGoogle Scholar
  45. Gregg, C.T., Chojnacki, A.K. and Weiss, S. (2002). Radial glial cells as neuronal precursors: the next generation? J. Neurosci. Res. 69: 708–713.CrossRefPubMedGoogle Scholar
  46. Guthrie, K.M., Wilson, D.A. and Leon, M. (1990). Early unilateral deprivation modifies olfactory bulb function. J. Neurosci. 10: 3402–3412.PubMedGoogle Scholar
  47. Hack, I., Bancila, M., Loulier, K., Carroll, P. and Cremer, H. (2002). Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat. Neurosci. 5: 939–945.CrossRefPubMedGoogle Scholar
  48. Hartfuss, E., Galli, R., Heins, N. and Gotz, M. (2001). Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229: 15–30.CrossRefPubMedGoogle Scholar
  49. Hack MA, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery-Padan R, Lledo PM, Gotz M (2005) Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci.Google Scholar
  50. Hedin-Pereira, C., Miyakoshi, L.M. and Mendez-Otero, R. (2001). Ganglioside 9-O-acetyl GD3 is involved in the migration of subventricular zone neuroblasts in vitro. In: Society for Neuroscience.Google Scholar
  51. Herrera, D.G., Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (1999). Adult-derived neural precursors transplanted into multiple regions in the adult brain. Ann. Neurol. 46: 867–877.CrossRefPubMedGoogle Scholar
  52. Hidalgo, A., Barami, K., Iversen, K. and Goldman, S.A. (1995). Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J. Neurobiol. 27: 470–487.CrossRefPubMedGoogle Scholar
  53. Hitoshi, S., Alexson, T., Tropepe, V., Donoviel, D., Elia, A.J., Nye, J.S., Conlon, R.A., Mak, T.W., Bernstein, A. and van der Kooy, D. (2002). Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev. 16: 846–858.CrossRefPubMedGoogle Scholar
  54. Hoffman, S. and Edelman, G.M. (1983). Kinetics of homophilic binding by embryonic and adult forms of the neural cell-adhesion molecule. Proc. Natl. Acad. Sci. U. S. A. 80: 5762–5766.PubMedGoogle Scholar
  55. Hogan, B.L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10: 1580–1594.PubMedGoogle Scholar
  56. Hu, H. (1999). Chemorepulsion of neuronal migration by Slit2 in the developing mammalian forebrain. Neuron 23: 703–711.CrossRefPubMedGoogle Scholar
  57. Hu, H.Y. and Rutishauser, U. (1996). A septum-derived chemorepulsive factor for migrating olfactory interneuron precursors. Neuron 16: 933–940.CrossRefPubMedGoogle Scholar
  58. Hu, H.Y., Tomasiewicz, H., Magnuson, T. and Rutishauser, U. (1996). The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16: 735–743.CrossRefPubMedGoogle Scholar
  59. Imura, T., Kornblum, H.I. and Sofroniew, M.V. (2003). The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J. Neurosci. 23: 2824–2832.PubMedGoogle Scholar
  60. Isaacson, J.S. and Strowbridge, B.W. (1998). Olfactory reciprocal synapses: Dendritic signaling in the CNS. Neuron 20: 749–761.CrossRefPubMedGoogle Scholar
  61. Jacques, T.S., Relvas, J.B., Nishimura, S., Pytela, R., Edwards, G.M. and Streuli, C.H., ffrench-Constant C. (1998). Neural precursor cell chain migration and division are regulated through different B1 integrins. Development 125:3167–3177.PubMedGoogle Scholar
  62. Jankovski, A. and Sotelo, C. (1996). Subventricular zone-olfactory bulb migratory pathway in the adult mouse: Cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J. Comp. Neurol. 371: 376–396.CrossRefPubMedGoogle Scholar
  63. Jankovski, A., Garcia, C., Soriano, E. and Sotelo, C. (1998). Proliferation., migration and differentiation of neuronal progenitor cells in the adult mouse subventricular zone surgically separated from its olfactory bulb. Eur. J. Neurosci. 10: 3853–3868.CrossRefPubMedGoogle Scholar
  64. Johansson, CB., Momma, S., Clarke, DL., Risling, M., Lendahl, U. and Frisén, J. (1999). Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96: 25–34.CrossRefPubMedGoogle Scholar
  65. Johnson, C.P., Fujimoto, I., Rutishauser, U. and Leckband, D.E. (2004). Direct evidence that NCAM polysialylation increases intermembrane repulsion and abrogates adhesion. J. Biol. Chem.Google Scholar
  66. Johnson CP, Fujimoto I, Rutishauser U, Leckband DE (2005) Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J Biol Chem 280:137–145.PubMedGoogle Scholar
  67. Kaplan, M.S., McNelly, N.A. and Hinds, J.W. (1985). Population dynamics of adult-formed granule neurons of the rat olfactory bulb. J. Comp. Neurol. 239:117–125.CrossRefPubMedGoogle Scholar
  68. Kempermann, G. (2002). Why new neurons? Possible functions for adult hippocampal neurogenesis. J. Neurosci. 22: 635–638.PubMedGoogle Scholar
  69. Kendrick, K.M., Lévy, F. and Keverne, E.B. (1992). Changes in the sensory processing of olfactory signals induced by birth in sheep. Science 256: 833–836.PubMedGoogle Scholar
  70. Kirschenbaum, B., Doetsch, F., Lois, C., Alvarez-Buylla, A. (1999). Adult Subventricular Zone Neuronal Precursors Continue to Proliferate and Migrate in the Absence of the Olfactory Bulb. J. Neurosci. 19: 2171–2180.PubMedGoogle Scholar
  71. Kishi, K. (1987). Golgi studies on the development of granule cells of the rat olfactory bulb with reference to migration in the subependymal layer. J. Comp. Neurol. 258: 112–124.CrossRefPubMedGoogle Scholar
  72. Kishi, K., Peng, J.Y., Kakuta, S., Murakami, K., Kuroda, M., Yokota, S., Hayakawa, S., Kuge, T. and Asayama, T. (1990). Migration of Bipolar Subependymal Cells., Precursors of the granule cells of the rat olfactory bulb., with reference to the arrangement of the radial glial fibers. Arch. Histol. Cytol. 53(2): 219–226.PubMedGoogle Scholar
  73. Kohwi M, Osumi N, Rubenstein JL, Alvarez-Buylla A (2005) Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci 25:6997–7003.CrossRefPubMedGoogle Scholar
  74. Kornack, D.R. and Rakic, P. (2001). The generation., migration., and differentiation of olfactory neurons in the adult primate brain. Proc. Natl. Acad. Sci. U. S. A. 98:4752–4757.CrossRefPubMedGoogle Scholar
  75. Kuhn, H.G., Winkler, J., Kempermann, G., Thal, L.J. and Gage, F.H. (1997). Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17: 5820–5829.PubMedGoogle Scholar
  76. Lai, K., Kaspar, B.K., Gage, F.H. and Schaffer, D.V. (2003). Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat. Neurosci. 6: 21–27.CrossRefPubMedGoogle Scholar
  77. Lambert de Rouvroit, C. and Goffinet, A.M. (2001). Neuronal migration. Mech. Dev. 105: 47–56.CrossRefPubMedGoogle Scholar
  78. Laurent, G., Stopfer, M., Friedrich, R.W., Rabinovich, M.I., Volkovskii, A. and Abarbanel H.D. (2001). Odor encoding as an active., dynamical process: experiments., computation., and theory. Annu. Rev. Neurosci. 24: 263–297.CrossRefPubMedGoogle Scholar
  79. Law, A.K., Pencea, V., Buck, C.R. and Luskin, M.B. (1999). Neurogenesis and neuronal migration in the neonatal rat forebrain anterior subventricular zone do not require GFAP-positive astrocytes. Dev. Biol. 216: 622–634.CrossRefPubMedGoogle Scholar
  80. Laywell, E.D., Rakic, P., Kukekov, V.G., Holland, E.C. and Steindler, D.A. (2000). Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc. Natl. Acad. Sci. U. S. A. 97: 13883–13888.CrossRefPubMedGoogle Scholar
  81. Levi-Montalcini, R. (1987). The nerve growth factor 35 years later. Science 237:1154–1162.PubMedGoogle Scholar
  82. 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.CrossRefPubMedGoogle Scholar
  83. Lim, D.A. and Alvarez-Buylla, A. (1999). Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 96: 7526–7531.CrossRefPubMedGoogle Scholar
  84. Lim D.A., D. TA., Trevejo, J.M., Herrera, D.G., García-Verdugo, J.M. and Alvarez-Buylla, A. (2000). Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28: 713–726.CrossRefPubMedGoogle Scholar
  85. Liu G. and Rao Y. (2003). Neuronal migration from the forebrain to the olfactory bulb requires a new attractant persistent in the olfactory bulb. J. Neurosci. 23:6651–6659.PubMedGoogle Scholar
  86. Liu, S.Y., Zhang, Z.Y., Song, Y.C., Qiu, K.J., Zhang, K.C., An, N., Zhou, Z., Cai, W.Q. and Yang, H. (2004). SVZa neural stem cells differentiate into distinct lineages in response to BMP4. Exp. Neurol. 190: 109–121.CrossRefPubMedGoogle Scholar
  87. Lois, C. and Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145–1148.PubMedGoogle Scholar
  88. Lois, C., Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (1996). Chain migration of neuronal precursors. Science 271: 978–981.PubMedGoogle Scholar
  89. Louissaint, A., Jr., Rao, S., Leventhal, C. and Goldman, S.A. (2002). Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34: 945–960.CrossRefPubMedGoogle Scholar
  90. Luskin, M.B. (1993). Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11: 173–189.CrossRefPubMedGoogle Scholar
  91. Luskin, M.B. (1998). Neuroblasts of the postnatal mammalian forebrain: their phenotype and fate. J. Neurobiol. 36: 221–233.CrossRefPubMedGoogle Scholar
  92. Machold, R., Hayashi, S., Rutlin, M., Muzumdar, M.D., Nery, S., Corbin, J.G., Gritli-Linde, A., Dellovade, T., Porter, J.A., Rubin, L.L., Dudek, H., McMahon, A.P. and Fishell, G. (2003). Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39: 937–950.CrossRefPubMedGoogle Scholar
  93. MacLeod, K., Backer, A. and Laurent, G. (1998). Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395: 693–698.CrossRefPubMedGoogle Scholar
  94. Malatesta, P., Hack, M.A., Hartfuss, E., Kettenmann, H., Klinkert, W., Kirchhoff, F. and Gotz, M. (2003). Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37: 751–764.CrossRefPubMedGoogle Scholar
  95. Mason, H.A., Ito, S. and Corfas, G. (2001). Extracellular signals that regulate the tangential migration of olfactory bulb neuronal precursors: inducers., inhibitors., and repellents. J. Neurosci. 21: 7654–7663.PubMedGoogle Scholar
  96. Merkle FT, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A (2004) Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci U S A 101:17528–17532.CrossRefPubMedGoogle Scholar
  97. McMahon, AP., Ingham, P.W. and Tabin, C.J. (2003). Developmental roles and clinical significance of hedgehog signaling. Curr. Top. Dev. Biol. 53: 1–114.PubMedCrossRefGoogle Scholar
  98. Mehler, M.F., Mabie, P.C., Zhang, D. and Kessler, J.A. (1997). Bone morphogenetic proteins in the nervous system. Trends Neurosci. 20: 309–317.CrossRefPubMedGoogle Scholar
  99. Merkle, F., Tramontin, AD., Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (2004). Radial glia give rise to adult neural stem cells in the subventricular zone. Proc. Natl. Acad. Sci. U. S. A. In Press.Google Scholar
  100. Miyakoshi, L.M., Mendez-Otero, R. and Hedin-Pereira, C. (2001). The 9-O-acetyl GD3 gangliosides are expressed by migrating chains of subventricular zone neurons in vitro. Braz. J. Med. Biol. Res. 34: 669–673.CrossRefPubMedGoogle Scholar
  101. Mori, K., Nagao, H. and Yoshihara, Y. (1999). The olfactory bulb: coding and processing of odor molecule information. Science 286: 711–715.CrossRefPubMedGoogle Scholar
  102. Morshead, C.M., Reynolds, B.A., Craig, C.G., McBurney, M.W., Staines, W.A., Morassutti, D., Weiss, S. and van der Kooy, D. (1994). Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron 13: 1071–1082.CrossRefPubMedGoogle Scholar
  103. Murase, S. and Horwitz, A.F. (2002). Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J. Neurosci. 22: 3568–3579.PubMedGoogle Scholar
  104. Nacher, J., Rosell, D.R. and McEwen, B.S. (2000). Widespread expression of rat collapsin response-mediated protein 4 in the telencephalon and other areas of the adult rat central nervous system. J. Comp. Neurol. 424: 628–639.CrossRefPubMedGoogle Scholar
  105. Ng KL, Li JD, Cheng MY, Leslie FM, Lee AG, Zhou QY (2005) Dependence of olfactory bulb neurogenesis on prokineticin 2 signaling. Science 308:1923–1927.CrossRefPubMedGoogle Scholar
  106. Nguyen-Ba-Charvet, K.T., Brose, K., Marillat, V., Kidd, T., Goodman, C.S., Tessier-Lavigne, M., Sotelo, C. and Chedotal, A. (1999). Slit2-Mediated chemorepulsion and collapse of developing forebrain axons. Neuron 22: 463–473.CrossRefPubMedGoogle Scholar
  107. Nguyen-Ba-Charvet, K.T., Picard-Riera, N., Tessier-Lavigne, M., Baron-Van Evercooren, A., Sotelo, C. and Chedotal, A. (2004). Multiple roles for slits in the control of cell migration in the rostral migratory stream. J. Neurosci. 24: 1497–1506.CrossRefPubMedGoogle Scholar
  108. Nicoll, RA. (1969). Inhibitory mechanisms in the rabbit olfactory bulb: Dendrodendritic mechanisms. Brain Res. 14: 157–172.CrossRefPubMedGoogle Scholar
  109. Noctor, SC., Flint, A.C., Weissman, T.A., Dammerman, R.S. and Kriegstein, A.R. (2001). Neurons derived from radial glial cells establish radial units in neocortex. Nature 409: 714–720.CrossRefPubMedGoogle Scholar
  110. Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR (2002) Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 22:3161–3173.PubMedGoogle Scholar
  111. Nottebohm, F. (2002a). Why are some neurons replaced in adult brain? J. Neurosci. 22: 624–628.PubMedGoogle Scholar
  112. Nottebohm, F. (2002b). Neuronal replacement in adult brain. Brain Res. Bull. 57:737–749.CrossRefPubMedGoogle Scholar
  113. Ogawa, M., Miyata, T., Nakajima, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H. and Mikoshiba, K. (1995). The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14: 899–912.CrossRefPubMedGoogle Scholar
  114. Ono, K., Tomasiewicz, H., Magnuson, T. and Rutishauser, U. (1994). N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13: 595–609.CrossRefPubMedGoogle Scholar
  115. Ormerod, BK., Lee, T.T. and Galea, L.A. (2003). Estradiol initially enhances but subsequently suppresses. (via adrenal steroids). granule cell proliferation in the dentate gyrus of adult female rats. J. Neurobiol. 55: 247–260.CrossRefPubMedGoogle Scholar
  116. Palma V, Lim DA, Dahmane N, Sanchez P, Brionne TC, Herzberg CD, Gitton Y, Carleton A, Alvarez-Buylla A, Ruiz i Altaba A (2005) Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 132:335–344.CrossRefPubMedGoogle Scholar
  117. Parras, C.M., Galli, R., Britz, O., Soares, S., Galichet, C., Battiste, J., Johnson, JE., Nakafuku, M., Vescovi, A. and Guillemot, F. (2004). Mash1 specifies neurons and oligodendrocytes in the postnatal brain. Embo. J. 23: 4495–4505.CrossRefPubMedGoogle Scholar
  118. Pencea, V., Bingaman, K.D., Wiegand, S.J. and Luskin, M.B. (2001a). Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum., septum., thalamus., and hypothalamus. J. Neurosci. 21: 6706–6717.PubMedGoogle Scholar
  119. Pencea, V., Bingaman, K.D., Freedman, L.J. and Luskin, M.B. (2001b). Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp. Neurol. 172: 1–16.CrossRefPubMedGoogle Scholar
  120. Pennartz, S., Belvindrah, R., Tomiuk, S., Zimmer, C., Hofmann, K., Conradt, M., Bosio A. and Cremer, H. (2004). Purification of neuronal precursors from the adult mouse brain: comprehensive gene expression analysis provides new insights into the control of cell migration, differentiation, and homeostasis. Mol. Cell. Neurosci. 25: 692–706.CrossRefPubMedGoogle Scholar
  121. Peretto, P., Merighi, A., Fasolo, A., Bonfanti, L. (1997). Glial tubes in the rostral migratory stream of the adult rat. Brain Res. Bull. 42: 9–21.CrossRefPubMedGoogle Scholar
  122. Peretto, P., Dati, C., De Marchis, S., Kim, H.H., Ukhanova, M., Fasolo, A. and Margolis, F.L. (2004). Expression of the secreted factors noggin and bone morphogenetic proteins in the subependymal layer and olfactory bulb of the adult mouse brain. Neuroscience 128: 685–696.CrossRefPubMedGoogle Scholar
  123. Perez-Martin, M., Azcoitia, I., Trejo, J.L., Sierra, A. and Garcia-Segura, L.M. (2003). An antagonist of estrogen receptors blocks the induction of adult neurogenesis by insulin-like growth factor-I in the dentate gyrus of adult female rat. Eur. J. Neurosci. 18: 923–930.CrossRefPubMedGoogle Scholar
  124. Petreanu, L. and Alvarez-Buylla, A. (2002). Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci.Google Scholar
  125. Petridis, A.K., El-Maarouf, A. and Rutishauser, U. (2004). Polysialic acid regulates cell contact-dependent neuronal differentiation of progenitor cells from the subventricular zone. Dev. Dyn. 230: 675–684.CrossRefPubMedGoogle Scholar
  126. Probstmeier, R. and Pesheva, P. (1999). Tenascin-C inhibits beta1 integrin-dependent cell adhesion and neurite outgrowth on fibronectin by a disialoganglioside-mediated signaling mechanism. Glycobiology 9: 101–114.CrossRefPubMedGoogle Scholar
  127. Raisman, G. (2001). Olfactory ensheathing cells-another miracle cure for spinal cord injury? Nat. Rev. Neurosci. 2: 369–375.CrossRefPubMedGoogle Scholar
  128. Rakic, P. (1972). Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145: 61–84.CrossRefPubMedGoogle Scholar
  129. Rakic, P. (1985). Limits of neurogenesis in primates. Science 227: 1054–1056.PubMedGoogle Scholar
  130. Rakic, P. (1988). Specification of cerebral cortical areas. Science 241: 170–176.PubMedGoogle Scholar
  131. Rakic, P. (1990). Principles of neural cell migration. Experientia 46: 882–891.CrossRefPubMedGoogle Scholar
  132. Rakic, P. (1995). Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 92: 11323–11327.PubMedGoogle Scholar
  133. Rall, W. and Shepherd, G.M. (1968). Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J. Neurophysiol. 31:884–915.PubMedGoogle Scholar
  134. Rall, W., Shepherd, G.M., Reese, T.S. and Brightman, M.W. (1966). Dendrodendritic synaptic pathway for inhibitation in the olfactory bulb. Exp. Neurol. 14:44–56.CrossRefPubMedGoogle Scholar
  135. Rasika, S., Nottebohm, F. and Alvarez-Buylla, A. (1994). Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc. Natl. Acad. Sci. U. S. A. 91: 7854–7858.PubMedGoogle Scholar
  136. Rasika, S., Alvarez-Buylla, A. and Nottebohm, F. (1999). BDNF mediates the effects of testosterone on the survival of new neurons in an adult brain. Neuron 22: 53–62.CrossRefPubMedGoogle Scholar
  137. Reynolds, B. and Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707–1710.PubMedGoogle Scholar
  138. Rietze, R.L., Valcanis, H., Brooker, G.F., Thomas, T., Voss, A.K. and Bartlett, P.F. (2001). Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412: 736–739.CrossRefPubMedGoogle Scholar
  139. Rochefort, C., Gheusi, G., Vincent, J.D. and Lledo, 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.PubMedGoogle Scholar
  140. Rousselot, P., Lois, C. and Alvarez-Buylla, A. (1995). Embryonic. (PSA). N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J. Comp. Neurol. 351: 51–61.CrossRefPubMedGoogle Scholar
  141. Rowitch, DH., B SJ., Lee, S.M., Flax, J.D., Snyder, E.Y. and McMahon, A.P. (1999). Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells. J. Neurosci. 19: 8954–8965.PubMedGoogle Scholar
  142. Rutishauser, U., Watanabe, M., Silver, J., Troy, F.A. and Vimr, E.R. (1985). Specific alteration of NCAM-mediated cell adhesion by an endoneuraminidase. J. Cell Biol. 101: 1842–1849.CrossRefPubMedGoogle Scholar
  143. Sadoul, R., Hirn, M., Deagostini-Bazin, H., Rougon, G. and Goridis, C. (1983). Adult and embryonic mouse neural cell adhesion molecules have different binding properties. Nature 304: 347–349.CrossRefPubMedGoogle Scholar
  144. Saghatelyan, A., de Chevigny, A., Schachner, M. and Lledo, P.M. (2004). Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nat. Neurosci. 7: 347–356.CrossRefPubMedGoogle Scholar
  145. Schmechel, D.E. and Rakic, P. (1979). A Golgi study of radial glia cells in developing monkey telencephalon: Morphogenesis and transformation into astrocytes. Anat. Embryol. 156: 115–152.CrossRefPubMedGoogle Scholar
  146. Schmidt-Hieber, C., Jonas, P. and Bischofberger, J. (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184–187.CrossRefPubMedGoogle Scholar
  147. Schoppa, NE. and Westbrook, G.L. (1999). Regulation of synaptic timing in the olfactory bulb by an A-type potassium current. Nat. Neurosci. 2: 1106–1113.CrossRefPubMedGoogle Scholar
  148. Schuurmans, C. and Guillemot, F. (2002). Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr. Opin. Neurobiol. 12: 26–34.CrossRefPubMedGoogle Scholar
  149. Seri, B., Garcia-Verdugo, J.M., McEwen, B.S. and Alvarez-Buylla, A. (2001). Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21: 7153–7160.PubMedGoogle Scholar
  150. Seroogy, K.B., Gall, C.M., Lee, D.C. and Kornblum, H.I. (1995). Proliferative zones of postnatal rat brain express epidermal growth factor receptor mRNA. Brain Res. 670: 157–164.CrossRefPubMedGoogle Scholar
  151. Shepherd, G.M. (1972). Synaptic organization of the mammalian olfactory bulb. Physiol. Rev. 52: 864–917.PubMedGoogle Scholar
  152. Shepherd, GM. and Greer, C.A. (1998). Olfactory Bulb. In: The Synaptic Organization of the Brain, 4th edn. (Shepherd, GM., ed.), Oxford University Press, Inc., New York, pp. 159–203.Google Scholar
  153. Shingo, T., Gregg, C., Enwere, E., Fujikawa, H., Hassam, R., Geary, C., Cross, J.C. and Weiss, S. (2003). Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299: 117–120.CrossRefPubMedGoogle Scholar
  154. Smith, M.T., Pencea, V., Wang, Z., Luskin, M.B. and Insel, TR. (2001). Increased number of BrdU-labeled neurons in the rostral migratory stream of the estrous prairie vole. Horm. Behav. 39: 11–21.CrossRefPubMedGoogle Scholar
  155. Spassky N, Merkle FT, Flames N, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A (2005) Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 25:10–18.CrossRefPubMedGoogle Scholar
  156. Soria JM, Taglialatela P, Gil-Perotin S, Galli R, Gritti A, Verdugo JM, Bertuzzi S (2004) Defective postnatal neurogenesis and disorganization of the rostral migratory stream in absence of the Vax1 homeobox gene. J Neurosci 24:11171–11181.CrossRefPubMedGoogle Scholar
  157. Stopfer, M., Bhagavan, S., Smith, B.H. and Laurent, G. (1997). Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390: 70–74.CrossRefPubMedGoogle Scholar
  158. Stump, G., Durrer, A., Klein, AL., Lutolf, S., Suter, U. and Taylor, V. (2002). Notch1 and its ligands Delta-like and Jagged are expressed and active in distinct cell populations in the postnatal mouse brain. Mech. Dev. 114: 153–159.CrossRefPubMedGoogle Scholar
  159. Svendsen, C.N., Bhattacharyya, A. and Tai, Y.T. (2001). Neurons from stem cells: preventing an identity crisis. Nat. Rev. Neurosci. 2: 831–834.CrossRefPubMedGoogle Scholar
  160. Takizawa T., Ochiai W., Nakashima, K. and Taga, T. (2003). Enhanced gene activation by Notch and BMP signaling cross-talk. Nucleic Acids Res. 31: 5723–5731.CrossRefPubMedGoogle Scholar
  161. Tanapat, P., Hastings, NB., Reeves, AJ. and Gould, E. (1999). Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19: 5792–5801.PubMedGoogle Scholar
  162. Temple, S. and Alvarez-Buylla, A. (1999). Stem cells in the adult mammalian central nervous system. Curr. Opin. Neurobiol. 9: 135–141.CrossRefPubMedGoogle Scholar
  163. Thomas, LB., Gates, M.A. and Steindler, D.A. (1996). Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte., extracellular matrix-rich pathway. Glia 17: 1–14.CrossRefPubMedGoogle Scholar
  164. Tomasiewicz, H., Ono, K., Yee, D., Thompson, C., Goridis, C., Rutishauser, U. and Magnuson, T. (1993). Genetic deletion of a neural cell adhesion molecule variant (N-CAM 180) produces distinct defects in the central nervous system. Neuron 11:1163–1174.CrossRefPubMedGoogle Scholar
  165. Tropepe, V., Craig, C.G., Morshead, C.M. and van der Kooy D. (1997). Transforming growth factor-α null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J. Neurosci. 17: 7850–7859.PubMedGoogle Scholar
  166. Tropepe, V., Sibilia, M., Ciruna, B.G., Rossant, J., Wagner, E.F. and van der Kooy D. (1999). Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev. Biol. 208: 166–188.CrossRefPubMedGoogle Scholar
  167. Tropepe, V., Coles, B.L., Chiasson, B.J., Horsford, D.J., Elia, A.J., McInnes, R.R. and van der Kooy D. (2000). Retinal stem cells in the adult mammalian eye. Science 287: 2032–2036.CrossRefPubMedGoogle Scholar
  168. Vescovi, A.L., Galli, R. and Gritti, A. (2001). The neural stem cells and their transdifferentiation capacity. Biomed. Pharmacother. 55: 201–205.CrossRefPubMedGoogle Scholar
  169. Voigt, T. (1989). Development of glial cells in the cerebral wall of ferrets: Direct tracing of their transformation from radial glia into astrocytes. J. Comp. Neurol. 289: 74–88.CrossRefPubMedGoogle Scholar
  170. Weickert, C.S., Webster, M.J., Colvin, S.M., Herman, M.M., Hyde, T.M., Weinberger, D.R. and Kleinman, J.E. (2000). Localization of epidermal growth factor receptors and putative neuroblasts in human subependymal zone. J. Comp. Neurol. 423: 359–372.CrossRefPubMedGoogle Scholar
  171. Weiss, S., Dunne, C., Hewson, J., Wohl, C., Wheatley, M., Peterson, A.C. and Reynolds, B.A. (1996). Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16: 7599–7609.PubMedGoogle Scholar
  172. Wichterle, H., Garcia-Verdugo, J.M. and Alvarez-Buylla, A. (1997). Direct evidence for homotypic., glia-independent neuronal migration. Neuron 18: 779–791.CrossRefPubMedGoogle Scholar
  173. Woolf, T.B., Shepherd, G.M. and Greer, C.A. (1991). Serial reconstructions of granule cell spines in the mammalian olfactory bulb. Synapse 7: 181–192.CrossRefPubMedGoogle Scholar
  174. Wu, W., Wong, K., Chen, J.H., Jiang, Z.H., Dupuls, S., Wu, J.Y. and Rao, Y. (1999). Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 400: 331–336.CrossRefPubMedGoogle Scholar
  175. Yokoi, M., Mori, K. and Nakanishi, S. (1995). Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl. Acad. Sci. U. S. A. 92. 92: 3371–3375.Google Scholar
  176. Yokosaki, Y., Monis, H., Chen, J. and Sheppard, D. (1996). Differential effects of the integrins alpha9beta1., alphavbeta3., and alphavbeta6 on cell proliferative responses to tenascin. Roles of the beta subunit extracellular and cytoplasmic domains. J. Biol. Chem. 271: 24144–24150.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Minoree Kohwi
    • 1
  • Rui Pedro Galvão
    • 2
  • Arturo Alvarez-Buylla
    • 3
  1. 1.Programs in NeuroscienceUniversity of California, San FranciscoSan Francisco
  2. 2.Programa Gulbenkian de BiomedicinaInstituto Gulbenkian de Ciência, PortugalPortugal
  3. 3.Department of NeurosurgeryUniversity of CaliforniaSan Francisco

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