Neuronal migration in the adult brain: Are we there yet?

Nature Reviews Neuroscience

Volumn 8, Issue 2, 2007, Pages 141-151

  Ghashghaei, H Troy ^a,b   Lai, Cary ^c   Anton, E S ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; BRAIN REGION; CELL FUNCTION; CELL MIGRATION; FOREBRAIN; HUMAN; LIFESPAN; MITOSIS; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMISSION; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STATISTICAL SIGNIFICANCE;

ANIMALS; BRAIN; CELL MOVEMENT; NEURONS;

EID: 33846524307     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn2074     Document Type: Review

References (170)

1. Sidman, R. L. & Rakic, P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 62, 1-35 (1973).
2. Mochida, G. H. & Walsh, C. A. Genetic basis of developmental malformations of the cerebral cortex. Arch. Neurol. 61, 637-640 (2004).
3. Nadarajah, B. & Parnavelas, J. G. Modes of neuronal migration in the developing cerebral cortex. Nature Rev. Neurosci. 3, 423-432 (2002).
4. Nadarajah, B., Alifragis, P., Wong, R. O. & Parnavelas, J. G. Ventricle-directed migration in the developing cerebral cortex. Nature Neurosci. 5, 218-224 (2002).
5. Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R. O. & Pearlman, A. L. Two modes of radial migration in early development of the cerebral cortex. Nature Neurosci. 4, 143-150 (2001).
6. Nadarajah, B. Radial glia and somal translocation of radial neurons in the developing cerebral cortex. Glia 43, 33-36 (2003).
7. O'Rourke, N. A., Dailey, M. E., Smith, S. J. & McConnell, S. K. Diverse migratory pathways in the developing cerebral cortex. Science 258, 299-302 (1992).
8. De Carlos, J. A., Lopez-Mascaraque, L. & Valverde, F. Dynamics of cell migration from the lateral ganglionic eminence in the rat. J. Neurosci. 16, 6146-6156 (1996).
9. Marin, O. & Rubenstein, J. L. Cell migration in the forebrain. Annu. Rev. Neurosci. 26, 441-483 (2003). Together with references 1-6, this provides a thorough review of neuronal migration during embryonic development.
10. Anderson, S. A., Eisenstat, D. D., Shi, L. & Rubenstein, J. L. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474-476 (1997). Revealed evidence supporting the idea that GABA-containing interneurons migrate tangentially from the subpallium to the pallidum and the dependence of this process on Dlx transcription factors.
11. Bystron, I., Rakic, P., Molnar, Z. & Blakemore, C. The first neurons of the human cerebral cortex. Nature Neurosci. 9, 880-886 (2006).
12. Meyer, G., Soria, J. M., Martinez-Galan, J. R., Martin-Clemente, B. & Fairen, A. Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J. Comp. Neurol. 397, 493-518 (1998).
13. Polleux, F., Whitford, K. L., Dijkhuizen, P. A., Vitalis, T. & Ghosh, A. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 129, 3147-3160 (2002).
14. Komuro, H. & Rakic, P. Dynamics of granule cell migration: a confocal microscopic study in acute cerebellar slice preparations. J. Neurosci. 15, 1110-1120 (1995).
15. Gray, G. E., Leber, S. M. & Sanes, J. R. Migratory patterns of clonally related cells in the developing central nervous system. Experientia 46, 929-940 (1990).
16. Ramón y Cajal, S. Degeneration and Regeneration of the Nervous System (Oxford Univ. Press/Humphrey Milford, London, 1928).
17. Bhardwaj, R. D. et al. Neocortical neurogenesis in humans is restricted to development. Proc. Natl Acad. Sci. USA 103, 12564-12568 (2006). Establishes that no newborn neurons are present in the adult human neocortex.
18. Mizrahi, A. & Katz, L. C. Dendritic stability in the adult olfactory bulb. Nature Neurosci. 6, 1201-1207 (2003).
19. Kornack, D. R. & Rakic, P. Cell proliferation without neurogenesis in adult primate neocortex. Science 294, 2127-2130 (2001).
20. Altman, J. & Das, G. D. Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J. Comp. Neurol. 126, 337-389 (1966).
21. Bayer, S. A. 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp. Brain Res. 50, 329-340 (1983).
22. Kaplan, M. S. & Bell, D. H. Neuronal proliferation in the 9-month-old rodent - radioautographic study of granule cells in the hippocampus. Exp. Brain Res. 52, 1-5 (1983).
23. Levison, S. W., Chuang, C., Abramson, B. J. & Goldman, J. E. The migrational patterns and developmental fates of glial precursors in the rat subventricular zone are temporally regulated. Development 119, 611-622 (1993).
24. Lois, C. & Alvarez-Buylla, A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA 90, 2074-2077 (1993).
25. Luskin, M. B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11, 173-189 (1993).
26. Taupin, P. & Gage, F. H. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J. Neurosci. Res. 69, 745-749 (2002).
27. Schmahmann, J. D. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J. Neuropsychiatry Clin. Neurosci. 16, 367-378 (2004).
28. Wang, V. Y. & Zoghbi, H. Y. Genetic regulation of cerebellar development. Nature Rev. Neurosci. 2, 484-491 (2001).
29. Friede, R. L. Dating the development of human cerebellum. Acta Neuropathol. (Berl.) 23, 48-58 (1973).
30. Solecki, D. J., Govek, E. E. & Hatten, M. E. mPar6α controls neuronal migration. J. Neurosci. 26, 10624-10625 (2006).
31. Machold, R. & Fishell, G. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48, 17-24 (2005).
32. Wang, V. Y., Rose, M. F. & Zoghbi, H. Y. Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48, 31-43 (2005).
33. Gilthorpe, J. D., Papantoniou, E. K., Chedotal, A., Lumsden, A. & Wingate, R. J. The migration of cerebellar rhombic lip derivatives. Development 129, 4719-4728 (2002).
34. Solecki, D. J., Govek, E. E., Tomoda, T. & Hatten, M. E. Neuronal polarity in CNS development. Genes Dev. 20, 2639-2647 (2006). Outlines recent advances in our understanding of neuronal polarity and its relevance to developmental events, including neuronal migration.
35. 2+ transients control CNS neuronal migration. Cell Calcium 37, 387-393 (2005).
36. Sisk, C. L. & Foster, D. L. The neural basis of puberty and adolescence. Nature Neurosci. 7, 1040-1047 (2004).
37. Schwanzel-Fukuda, M. & Pfaff, D. W. Origin of luteinizing hormone-releasing hormone neurons. Nature 338, 161-164 (1989).
38. Tobet, S. A. & Schwarting, G. A. Minireview: recent progress in gonadotropin-releasing hormone neuronal migration. Endocrinology 147, 1159-1165 (2006).
39. Wierman, M. E. et al. Molecular mechanisms of gonadotropin- releasing hormone neuronal migration. Trends Endocrinol. Metab. 15, 96-102 (2004).
40. Cariboni, A. & Maggi, R. Kallmann's syndrome, a neuronal migration defect. Cell. Mol. Life Sci. 63, 2512-2526 (2006).
41. Eichenbaum, H. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44, 109-120 (2004).
42. Stanfield, B. B. & Cowan, W. M. The development of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 185, 423-459 (1979).
43. 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc. Natl Acad. Sci. USA 99, 13178-13183 (2002).
44. Weiss, K. H. et al. Malformation of the radial glial scaffold in the dentate gyrus of reeler mice, scrambler mice, and ApoER2/VLDLR-deficient mice. J. Comp. Neurol. 460, 56-65 (2003).
45. Zhao, S., Chai, X., Forster, E. & Frotscher, M. Reelin is a positional signal for the lamination of dentate granule cells. Development 131, 5117-5125 (2004).
46. Morozov, Y. M., Ayoub, A. E. & Rakic, P. Translocation of synaptically connected interneurons across the dentate gyrus of the early postnatal rat hippocampus. J. Neurosci. 26, 5017-5027 (2006).
47. Nowakowski, R. S. & Rakic, P. The site of origin and route and rate of migration of neurons to the hippocampal region of the rhesus monkey. J. Comp. Neurol. 196, 129-154 (1981).
48. Luzzati, F. et al. Glia-independent chains of neuroblasts through the subcortical parenchyma of the adult rabbit brain. Proc. Natl Acad. Sci. USA 100, 13036-13041 (2003).
49. Kornack, D. R. & Rakic, P. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl Acad. Sci. USA 96, 5768-5773 (1999).
50. Sanai, N. et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427, 740-744 (2004). Demonstrates that there is no RMS indicative of organized, long-distance neuronal migration in the adult human brain. This paper, together with references 161-163, also shows the presence of neural stem cells in the adult human brain.
51. Lois, C. & Alvarez-Buylla, A. Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148 (1994). Together with reference 25, this demonstrates how long-distance migration of new neurons occurs in the adult mammalian brain.
52. Mason, H. A., Ito, S. & Corfas, G. Extracellular signals that regulate the tangential migration of olfactory bulb neuronal precursors: inducers, inhibitors, and repellents. J. Neurosci. 21, 7654-7663 (2001). Identified a novel, astroglial-derived migration inducing factor (MIA) for RMS neuroblasts.
53. Murase, S. & Horwitz, A. F. 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 (2002).
54. Liu, G. & Rao, Y. Neuronal migration from the forebrain to the olfactory bulb requires a new attractant persistent in the olfactory bulb. J. Neurosci. 23, 6651-6659 (2003).
55. Wu, W. et al. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 400, 331-336 (1999).
56. Kirschenbaum, B., Doetsch, F., Lois, C. & Alvarez-Buylla, A. Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J. Neurosci. 19, 2171-2180 (1999).
57. Jankovski, A. & Sotelo, C. 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 (1996).
58. Lois, C., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Chain migration of neuronal precursors. Science 271, 978-981 (1996).
59. Wichterle, H., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18, 779-791 (1997). Describes the migratory organization and dynamics of new neurons generated in the SVZ.
60. Lim, D. A. & Alvarez-Buylla, A. Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc. Natl Acad. Sci. USA 96, 7526-7531 (1999).
61. Menezes, J. R., Smith, C. M., Nelson, K. C. & Luskin, M. B. The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol. Cell. Neurosci. 6, 496-508 (1995).
62. Doetsch, F., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17, 5046-5061 (1997). Characterizes the complex cellular organization of the adult SVZ.
63. Doetsch, F., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl Acad. Sci. USA 96, 11619-11624 (1999).
64. Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716 (1999).
65. Capela, A. & Temple, S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35, 865-875 (2002).
66. Morshead, C. M., Garcia, A. D., Sofroniew, M. V. & van der Kooy, D. The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur. J. Neurosci. 18, 76-84 (2003).
67. Ghashghaei, H. T. et al. The role of neuregulin-ErbB4 interactions on the proliferation and organization of cells in the subventricular zone. Proc. Natl Acad. Sci. USA 103, 1930-1935 (2006).
68. Marillat, V. et al. Spatiotemporal expression patterns of slit and robo genes in the rat brain. J. Comp. Neurol. 442, 130-155 (2002).
69. Nguyen-Ba-Charvet, K. T. et al. Multiple roles for Slits in the control of cell migration in the rostral migratory stream. J. Neurosci. 24, 1497-1506 (2004).
70. Sawamoto, K. et al. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311, 629-632 (2006). Shows how the activity of ependymal cell cilia in the lateral ventricles may convey gradients of migration-influencing cues to newly generated neuroblasts in the SVZ.
71. Higginbotham, H., Tanaka, T., Brinkman, B. C. & Gleeson, J. G. GSK3β and PKCζ function in centrosome localization and process stabilization during Slit-mediated neuronal repolarization. Mol. Cell. Neurosci. 32, 118-132 (2006).
72. Marin, O. et al. Directional guidance of interneuron migration to the cerebral cortex relies on subcortical Slit1/2-independent repulsion and cortical attraction. Development 130, 1889-1901 (2003).
73. Hu, H. Chemorepulsion of neuronal migration by Slit2 in the developing mammalian forebrain. Neuron 23, 703-711 (1999).
74. Hu, H. Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nature Neurosci. 4, 695-701 (2001).
75. Juliano, R. L. Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu. Rev. Pharmacol. Toxicol. 42, 283-323 (2002).
76. Tomasiewicz, H. et al. Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11, 1163-1174 (1993).
77. Cremer, H. et al. 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 (1994).
78. Ono, K., Tomasiewicz, H., Magnuson, T. & Rutishauser, U. N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13, 595-609 (1994). Demonstrates that NCAM and polysialation of NCAM are essential for neuroblast chain migration in the RMS.
79. Hu, H. Polysialic acid regulates chain formation by migrating olfactory interneuron precursors. J. Neurosci. Res. 61, 480-492 (2000).
80. Hu, H., Tomasiewicz, H., Magnuson, T. & Rutishauser, U. The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16, 735-743 (1996).
81. Murase, S. & Horwitz, A. F. Directions in cell migration along the rostral migratory stream: the pathway for migration in the brain. Curr. Top. Dev. Biol. 61, 135-152 (2004).
82. Chazal, G., Durbec, P., Jankovski, A., Rougon, G. & Cremer, H. Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J. Neurosci. 20, 1446-1457 (2000).
83. Anton, E. S. et al. Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nature Neurosci. 7, 1319-1328 (2004). Demonstrates how neuregulin-ErbB4 signalling regulates neuroblast migration in the RMS.
84. Conover, J. C. et al. Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nature Neurosci. 3, 1091-1097 (2000).
85. Jacques, T. S. et al. Neural precursor cell chain migration and division are regulated through different β1 integrins. Development 125, 3167-3177 (1998).
86. Emsley, J. G. & Hagg, T. α6β1 integrin directs migration of neuronal precursors in adult mouse forebrain. Exp. Neurol. 183, 273-285 (2003).
87. Schmid, R. S., Jo, R., Shelton, S., Kreidberg, J. A. & Anton, E. S. Reelin, integrin and DAB1 interactions during embryonic cerebral cortical development. Cereb. Cortex 15, 1632-1636 (2005).
88. Gates, M. A. et al. Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J. Comp. Neurol. 361, 249-266 (1995).
89. Thomas, L. B., Gates, M. A. & Steindler, D. A. Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte, extracellular matrix-rich pathway. Glia 17, 1-14 (1996).
90. de Chevigny, A. et al. Delayed onset of odor detection in neonatal mice lacking tenascin-C. Mol. Cell. Neurosci. 32, 174-186 (2006).
91. Kiernan, B. W., Gotz, B., Faissner, A. & ffrench-Constant, C. Tenascin-C inhibits oligodendrocyte precursor cell migration by both adhesion-dependent and adhesion-independent mechanisms. Mol. Cell. Neurosci. 7, 322-335 (1996).
92. Saga, Y., Yagi, T., Ikawa, Y., Sakakura, T. & Aizawa, S. Mice develop normally without tenascin. Genes Dev. 6, 1821-1831 (1992).
93. Colognato, H. et al. CNS integrins switch growth factor signalling to promote target-dependent survival. Nature Cell Biol. 4, 833-841 (2002).
94. Davy, A. & Robbins, S. M. Ephrin-A5 modulates cell adhesion and morphology in an integrin-dependent manner. EMBO J. 19, 5396-5405 (2000).
95. Prevost, N. et al. Eph kinases and ephrins support thrombus growth and stability by regulating integrin outside-in signaling in platelets. Proc. Natl Acad. Sci. USA 102, 9820-9825 (2005).
96. Koshida, S. et al. Integrinα5-dependent fibronectin accumulation for maintenance of somite boundaries in zebrafish embryos. Dev. Cell 8, 587-598 (2005).
97. de Anda, F. C. et al. Centrosome localization determines neuronal polarity. Nature 436, 704-708 (2005).
98. Tsai, L. H. & Gleeson, J. G. Nucleokinesis in neuronal migration. Neuron 46, 383-388 (2005).
99. Solecki, D. J., Model, L., Gaetz, J., Kapoor, T. M. & Hatten, M. E. Par6α signaling controls glial-guided neuronal migration. Nature Neurosci. 7, 1195-1203 (2004).
100. Koizumi, H. et al. Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nature Neurosci. 9, 779-786 (2006). Shows that doublecortin is crucial for the nuclear translocation and migratory morphology of new neurons in the adult brain.
101. Kappeler, C. et al. Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum. Mol. Genet. 15, 1387-1400 (2006).
102. Yoshihara, S., Omichi, K., Yanazawa, M., Kitamura, K. & Yoshihara, Y. Arx homeobox gene is essential for development of mouse olfactory system. Development 132, 751-762 (2005).
103. D'Arcangelo, G. et al. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374, 719-723 (1995).
104. Rakic, P. & Sidman, R. L. Sequence of developmental abnormalities leading to granule cell deficit in cerebellar cortex of weaver mutant mice. J. Comp. Neurol. 152, 103-132 (1973).
105. Hack, I., Bancila, M., Loulier, K., Carroll, P. & Cremer, H. Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nature Neurosci. 5, 939-945 (2002). Describes how reelin might function to end the migration of new neurons when they reach their target in the olfactory bulb.
106. Saghatelyan, A., de Chevigny, A., Schachner, M. & Lledo, P. M. Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nature Neurosci. 7, 347-356 (2004).
107. Powell, E. M., Mars, W. M. & Levitt, P. Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 30, 79-89 (2001).
108. Pozas, E. & Ibanez, C. F. GDNF and GFRα1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 45, 701-713 (2005).
109. Marin, O., Yaron, A., Bagri, A., Tessier-Lavigne, M. & Rubenstein, J. L. Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science 293, 872-875 (2001).
110. Andrews, W. et al. Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain. Development 133, 2243-2252 (2006).
111. Magavi, S. S., Leavitt, B. R. & Macklis, J. D. Induction of neurogenesis in the neocortex of adult mice. Nature 405, 951-955 (2000).
112. Nakatomi, H. et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110, 429-441 (2002).
113. Van Praag, H. et al. Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034 (2002).
114. Yokoi, M., Mori, K. & Nakanishi, S. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl Acad. Sci. USA 92, 3371-3375 (1995).
115. Mori, K., Nagao, H. & Yoshihara, Y. The olfactory bulb: coding and processing of odor molecule information. Science 286, 711-715 (1999).
116. Magavi, S. S., Mitchell, B. D., Szentirmai, O., Carter, B. S. & Macklis, J. D. Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J. Neurosci. 25, 10729-10739 (2005).
117. Nilsson, M., Perfilieva, E., Johansson, U., Orwar, O. & Eriksson, P. S. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J. Neurobiol. 39, 569-578 (1999).
118. Shors, T. J. et al. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410, 372-376 (2001).
119. Rochefort, C., Gheusi, G., Vincent, J. D. & Lledo, P. M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679-2689 (2002).
120. Gheusi, G. et al. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl Acad. Sci. USA 97, 1823-1828 (2000).
121. Enwere, E. et al. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J. Neurosci. 24, 8354-8365 (2004).
122. Cecchi, G. A., Petreanu, L. T., Alvarez-Buylla, A. & Magnasco, M. O. Unsupervised learning and adaptation in a model of adult neurogenesis. J. Comput. Neurosci. 11, 175-182 (2001).
123. Bolteus, A. J. & Bordey, A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J. Neurosci. 24, 7623-7631 (2004).
124. Carleton, A., Petreanu, L. T., Lansford, R., Alvarez-Buylla, A. & Lledo, P. M. Becoming a new neuron in the adult olfactory bulb. Nature Neurosci. 6, 507-518 (2003). Describes the physiological properties of adultborn olfactory bulb interneurons at various stages of maturation in adult mice.
125. Tashiro, A., Sandler, V. M., Toni, N., Zhao, C. & Gage, F. H. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442, 929-933 (2006).
126. Aimone, J. B., Wiles, J. & Gage, F. H. Potential role for adult neurogenesis in the encoding of time in new memories. Nature Neurosci. 9, 723-727 (2006).
127. Gould, E., Beylin, A., Tanapat, P., Reeves, A. & Shors, T. J. Learning enhances adult neurogenesis in the hippocampal formation. Nature Neurosci. 2, 260-265 (1999).
128. Dayer, A. G., Cleaver, K. M., Abouantoun, T. & Cameron, H. A. New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J. Cell Biol. 168, 415-427 (2005).
129. Kaplan, M. S. Neurogenesis in the 3-month-old rat visual cortex. J. Comp. Neurol. 195, 323-338 (1981).
130. Koketsu, D., Mikami, A., Miyamoto, Y. & Hisatsune, T. Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J. Neurosci. 23, 937-942 (2003).
131. Spalding, K. L., Bhardwaj, R. D., Buchholz, B. A., Druid, H. & Frisen, J. Retrospective birth dating of cells in humans. Cell 122, 133-143 (2005).
132. Kokoeva, M. V., Yin, H. & Flier, J. S. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310, 679-683 (2005).
133. Luo, J., Daniels, S. B., Lennington, J. B., Notti, R. Q. & Conover, J. C. The aging neurogenic subventricular zone. Aging Cell 5, 139-152 (2006).
134. Mirich, J. M., Williams, N. C., Berlau, D. J. & Brunjes, P. C. Comparative study of aging in the mouse olfactory bulb. J. Comp. Neurol. 454, 361-372 (2002).
135. Pencea, V., Bingaman, K. D., Freedman, L. J. & Luskin, M. B. Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp. Neurol. 172, 1-16 (2001).
136. Lemasson, M., Saghatelyan, A., Olivo-Marin, J. C. & Lledo, P. M. Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J. Neurosci. 25, 6816-6825 (2005).
137. Caporaso, G. L., Lim, D. A., Alvarez-Buylla, A. & Chao, M. V. Telomerase activity in the subventricular zone of adult mice. Mol. Cell. Neurosci. 23, 693-702 (2003).
138. Lichtenwalner, R. J. & Parent, J. M. Adult neurogenesis and the ischemic forebrain. J. Cereb. Blood Flow Metab. 26, 1-20 (2006).
139. Fallon, J. et al. In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc. Natl Acad. Sci. USA 97, 14686-14691 (2000).
140. Houle, J. D. et al. Combining an autologous peripheral nervous system 'bridge' and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J. Neurosci. 26, 7405-7415 (2006).
141. Johansson, B. B. Environmental influence on recovery after brain lesions - experimental and clinical data. J. Rehabil. Med. 11-16 (2003).
142. Raisman, G. Myelin inhibitors: does NO mean GO? Nature Rev. Neurosci. 5, 157-161 (2004).
143. Kozlova, E. N. Differentiation and migration of astrocytes in the spinal cord following dorsal root injury in the adult rat. Eur. J. Neurosci. 17, 782-790 (2003).
144. Lee, S. R. et al. Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J. Neurosci. 26, 3491-3495 (2006).
145. Sundholm-Peters, N. L., Yang, H. K., Goings, G. E., Walker, A. S. & Szele, F. G. Subventricular zone neuroblasts emigrate toward cortical lesions. J. Neuropathol. Exp. Neurol. 64, 1089-1100 (2005).
146. Stefansson, H. et al. Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 71, 877-892 (2002).
147. Stefansson, H., Thorgeirsson, T. E., Gulcher, J. R. & Stefansson, K. Neuregulin 1 in schizophrenia: out of Iceland. Mol. Psychiatry 8, 639-640 (2003).
148. Yang, J. Z. et al. Association study of neuregulin 1 gene with schizophrenia. Mol. Psychiatry 8, 706-709 (2003).
149. Norton, N. et al. Evidence that interaction between neuregulin 1 and its receptor erbB4 increases susceptibility to schizophrenia. Am. J. Med. Genet. B Neuropsychiatr. Genet. 141, 96-101 (2006).
150. Hahn, C. G. et al. Altered neuregulin 1-erbB4 signaling contributes to NMDA receptor hypofunction in schizophrenia. Nature Med. 12, 824-828 (2006).
151. Ishizuka, K., Paek, M., Kamiya, A. & Sawa, A. A review of disrupted-in-schizophrenia-1 (DISC1): neurodevelopment, cognition, and mental conditions. Biol. Psychiatry 59, 1189-1197 (2006).
152. Eastwood, S. L. & Harrison, P. J. Cellular basis of reduced cortical reelin expression in schizophrenia. Am. J. Psychiatry 163, 540-542 (2006).
153. Fatemi, S. H. Reelin glycoprotein in autism and schizophrenia. Int. Rev. Neurobiol. 71, 179-187 (2005).
154. Tueting, P., Doueiri, M. S., Guidotti, A., Davis, J. M. & Costa, E. Reelin down-regulation in mice and psychosis endophenotypes. Neurosci. Biobehav. Rev. 30, 1065-1077 (2006).
155. Haas, C. A. et al. Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J. Neurosci. 22, 5797-5802 (2002).
156. Encinas, J. M., Vaahtokari, A. & Enikolopov, G. Fluoxetine targets early progenitor cells in the adult brain. Proc. Natl Acad. Sci. USA 103, 8233-8238 (2006).
157. Dranovsky, A. & Hen, R. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol. Psychiatry 59, 1136-1143 (2006).
158. Santarelli, L. et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809 (2003).
159. Gould, E., Tanapat, P., McEwen, B. S., Flugge, G. & Fuchs, E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl Acad. Sci. USA 95, 3168-3171 (1998).
160. Malberg, J. E., Eisch, A. J., Nestler, E. J. & Duman, R. S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20, 9104-9110 (2000).
161. Palmer, T. D. et al. Cell culture. Progenitor cells from human brain after death. Nature 411, 42-43 (2001).
162. Nunes, M. C. et al. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nature Med. 9, 439-447 (2003).
163. Eriksson, P. S. et al. Neurogenesis in the adult human hippocampus. Nature Med. 4, 1313-1317 (1998).
164. Bedard, A. & Parent, A. Evidence of newly generated neurons in the human olfactory bulb. Brain Res. Dev. Brain Res. 151, 159-168 (2004).
165. Liu, Z. & Martin, L. J. Olfactory bulb core is a rich source of neural progenitor and stem cells in adult rodent and human. J. Comp. Neurol. 459, 368-391 (2003).
166. Quinones-Hinojosa, A. et al. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J. Comp. Neurol. 494, 415-434 (2006). Describes the unique cellular organization of the human SVZ.
167. Font, E., Desfilis, E., Perez-Canellas, M. M. & Garcia-Verdugo, J. M. Neurogenesis and neuronal regeneration in the adult reptilian brain. Brain Behav. Evol. 58, 276-295 (2001).
168. Grandel, H., Kaslin, J., Ganz, J., Wenzel, I. & Brand, M. Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev. Biol. 295, 263-277 (2006).
169. Martin, J. H. Neuroanatomy: Text and Atlas 2nd edn (Appleton & Lange, Stamford, Connecticut, 1996).
170. Morales, D. & Hatten, M. E. Molecular markers of neuronal progenitors in the embryonic cerebellar anlage. J. Neurosci. 26, 12226-12236 (2006).