Neurogenesis in the adult brain;Neurogénesis en el cerebro adulto

Revista de Neurologia

Volumn 44, Issue 9, 2007, Pages 541-550

  Arias Carrión, Óscar ^a   Olivares Banuelos T ^a   Drucker Colin R ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Astrocytes; Neurogenesis; Neuronal stem cells; Radial glial cells; Regeneration; Subventricular zone

Indexed keywords

ASTROCYTE; BRAIN DEVELOPMENT; BRAIN REGION; CELL LINEAGE; EPENDYMA CELL; GLIA CELL; HIPPOCAMPUS; HUMAN; LIFESPAN; MAMMAL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; OLIGODENDROGLIA; REVIEW; ADULT; ANIMAL; BRAIN; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; GLIA; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; HOMEOSTASIS; NERVE CELL; NERVE CELL PLASTICITY; PHYSIOLOGY; STEM CELL;

ADULT; ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; HOMEOSTASIS; HUMANS; NEUROGLIA; NEURONAL PLASTICITY; NEURONS; OLFACTORY BULB; STEM CELLS;

EID: 34948860193     PISSN: 02100010     EISSN: None     Source Type: Journal    
DOI: 10.33588/rn.4409.2006426     Document Type: Review

References (130)

1. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965; 124: 319-35.
2. Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med 1998; 4: 1313-7.
3. Gould E, Reeves AJ, Graziano MS, Gross CG. Neurogenesis in the neocortex of adult primates. Science 1999; 286: 548-52.
4. Zhao M, Momma S, Delfani K, Carlén M, Cassidy RM, Johansson CB, et al. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci U S A 2003; 100: 7925-30.
5. Morshead CM, Van der Kooy D. Postmitotic death is the fate of constitutively proliferating cells in the subependimal layer of the adult mouse brain. J Neurosci 1992; 12: 249-56.
6. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, et al. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 1994; 13: 1071-82.
7. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255: 1707-10.
8. Lois C, Álvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A 1993; 90: 2074-7.
9. Laywell ED, Kukekov VG, Steindler DA. Multipotent neurospheres can be derived from forebrain subependimal zone and spinal cord of adult mice after protracted postmortem intervals. Exp Neurol 1999; 156: 430-3.
10. Roisen FJ, Klueber KM, Lu CL, Hatcher LM, Dozier A, Shields CB, et al. Adult human olfactory stem cells. Brain Res 2001; 890: 11-22.
11. Palmer TD, Schwartz PH, Taupin P, Kaspar B, Stein SA, Gage FH. Cell culture. Progenitor cells from human brain after death. Nature 2001; 411: 42-3.
12. Gage FH. Mammalian neural stem cells. Science 2000; 287: 1433-8.
13. Price J, Williams BP. Neural stem cells. Curr Opin Neurobiol 2001; 11: 564-7.
14. Tsai RY, Kittappa R, McKay RD. Plasticity, niches, and the use of stem cells. Dev Cell 2002; 2: 707-12.
15. Vescovi A, Gritti A, Cossu G, Galli R. Neural stem cells: plasticity and their transdifferentiation potential. Cells Tissues Organs 2002; 171: 64-76.
16. Wulf GG, Jackson KA, Goodell MA. Somatic stem cell plasticity: current evidence and emerging concepts. Exp Hematol 2001; 29: 1361-70.
17. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 1999; 96: 25-34.
18. Chiasson BJ, Tropepe V, Morshead CM, Van der Kooy D. Adult mammalian forebrain ependymal and subependimal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci 1999; 19: 4462-71.
19. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Álvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999; 97: 703-16.
20. Laywell ED, Rakic P, Kukekov VG, Holland EC, Steindler DA. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci U S A 2000; 97: 13883-8.
21. Frederiksen K, McKay RD. Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 1988; 8: 1144-51.
22. Álvarez-Buylla A, García-Verdugo JM, Tramontin AD. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2001; 2: 287-93.
23. Spassky N, Merkle FT, Flames N, Tramontin AD, García-Verdugo JM, Álvarez-Buylla A. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 2005; 25: 10-8.
24. Cameron RS, Rakic P. Glial cell lineage in the cerebral cortex: a review and synthesis. Glia 1991; 4: 124-37.
25. Misson JP, Austin CP, Takahashi T, Cepko CL, Caviness VS Jr. The alignment of migrating neural cells in relation to the murine neopallial radial glial fiber system. Cereb Cortex 1991; 1: 221-9.
26. Álvarez-Buylla A, Theelen M, Nottebohm F. Proliferation 'hot spots'in adult avian ventricular zone reveal radial cell division. Neuron 1990; 5: 101-9.
27. Merkle FT, Tramontin AD, García-Verdugo JM, Álvarez-Buylla A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci U S A 2004; 101: 17528-32.
28. Bernier PJ, Parent A. Bcl-2 protein as a marker of neuronal immaturity in postnatal primate brain. J Neurosci 1998; 18: 2486-97.
29. Kornack DR, Rakic P. Cell proliferation without neurogenesis in adult primate neocortex. Science 2001; 294: 2127-30.
30. Hartfuss E, Galli R, Heins N, Gotz M. Characterization of CNS precursor subtypes and radial glia. Dev Biol 2001; 229: 15-30.
31. Miyata T, Kawaguchi A, Okano H, Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 2001; 13: 727-41.
32. Malatesta P, Hartfuss E, Gotz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 2000; 127: 5253-63.
33. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001; 409: 714-20.
34. Tramontin AD, García-Verdugo JM, Lim DA, Álvarez-Buylla A. Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb Cortex 2003; 13: 580-7.
35. Tamamaki N, Nakamura K, Okamoto K, Kaneko T. Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci Res 2001; 41: 51-60.
36. Kintner C. Neurogenesis in embryos and in adult neural stem cells. J Neurosci 2002; 22: 639-43.
37. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. 3. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J Comp Neurol 1969; 136: 269-93.
38. Corotto FS, Henegar JA, Maruniak JA. Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci Lett 1993; 149: 111-4.
39. Luskin MB. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993; 11: 173-89.
40. Lois C, Álvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994; 264: 1145-81.
41. Seaberg RM, Van der Kooy D. Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J Neurosci 2002; 22: 1784-93.
42. Song HJ, Stevens CF, Gage FH. Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 2002; 5: 438-45.
43. Kaplan MS, McNelly NA, Hinds JW. Population dynamics of adult-formed granule neurons of the rat olfactory bulb. J Comp Neurol 1985; 239: 117-25.
44. Álvarez-Buylla A, García-Verdugo JM. Neurogenesis in adult subventricular zone. J Neurosci 2002; 22: 629-34.
45. Lim DA, Álvarez-Buylla A. Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci U S A 1999; 96: 7526-31.
46. Carleton A, Petreanu LT, Lansford R, Álvarez-Buylla A, Lledo PM. Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 2003; 6: 507-18.
47. Fukushima N, Yokouchi K, Kawagishi K, Moriizumi T. Differential neurogenesis and gliogenesis by local and migrating neural stem cells in the olfactory bulb. Neurosci Res 2002; 44: 467-73.
48. Lois C, García-Verdugo JM, Álvarez-Buylla A. Chain migration of neuronal precursors. Science 1996; 271: 978-81.
49. Kishi K. Golgi studies on the development of granule cells of the rat olfactory bulb with reference to migration in the subependymal layer. J Comp Neurol 1987; 258: 112-24.
50. Wichterle H, García-Verdugo JM, Álvarez-Buylla A. Direct evidence for homotypic, glia-independent neuronal migration. Neuron 1997; 18: 779-91.
51. Mason HA, Ito S, Corfas G. Extracellular signals that regulate the tangential migration of olfactory bulb neuronal precursors: inducers, inhibitors, and repellents. J Neurosci 2001; 19: 7654-63.
52. Rakic P. Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc Natl Acad Sci U S A 1995; 92: 11323-7.
53. Rakic P, Sidman RL. Weaver mutant mouse cerebellum: defective neuronal migration secondary to abnormality of Bergmann glia. Proc Natl Acad Sci U S A 1973; 70: 240-4.
54. Bonfanti L, Theodosis DT. 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 1994; 62: 291-305.
55. Jacques TS, Relvas JB, Nishimura S, Pytela R, Edwards GM, Streuli CH, et al. Neural precursor cell chain migration and division are regulated through different beta-1 integrins. Development 1998; 125: 3167-77.
56. Rousselot P, Lois C, Álvarez-Buylla A. Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J Comp Neurol 1995; 351: 51-61.
57. Thomas LB, Gates MA, Steindler DA. Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte, extracellular matrix-rich pathway. Glia 1996; 17: 1-14.
58. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, et al. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 1994; 367: 455-9.
59. Gheusi G, Cremer H, McLean H, Chazal G, Vincent JD, Lledo PM. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci U S A 2000; 97: 1823-8.
60. Bonfanti L, Peretto P, Merighi A, Fasolo A. Newly-generated cells from the rostral migratory stream in the accessory olfactory bulb of the adult rat. Neuroscience 1997; 81: 489-502.
61. Smith MT, Pencea V, Wang Z, Luskin MB, Insel TR. Increased number of BrdU-labeled neurons in the rostral migratory stream of the estrous prairie vole. Horm Behav 2001; 39: 11-21.
62. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, et al. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 2003; 299: 117-20.
63. Eckenhoff MF, Rakic P. Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J Neurosci 1998; 8: 2729-47.
64. Stanfield BB, Trice JE. Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp Brain Res 1988; 72: 399-406.
65. Hastings NB, Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 1999; 413: 146-54.
66. Markakis EA, Gage FH. Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol 1999; 406: 449-60.
67. Cameron HA, McKay RD. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 2001; 435: 406-17.
68. Seri B, García-Verdugo JM, Collado-Morente L, McEwen BS, Álvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 2004; 478: 359-78.
69. Seri B, García-Verdugo JM, McEwen BS, Álvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001; 21: 7153-60.
70. Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang LP, et al. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 2003; 23: 373-82.
71. Romero-Alemán MM, Monzón-Mayor M, Yanes C, Arbelo-Galván JF, Lang D, Renau-Piqueras J, et al. S100 immunoreactive glial cells in the forebrain and midbrain of the lizard Gallotia galloti during ontogeny. J Neurobiol 2003; 57: 54-66.
72. Vives V, Alonso G, Solal AC, Joubert D, Legraverend C. Visualization of S100B-positive neurons and glia in the central nervous system of EGFP transgenic mice. J Comp Neurol 2003; 457: 404-19.
73. Barnea A, Nottebohm F. Recruitment and replacement of hippocampal neurons in young and adult chickadees: an addition to the theory of hippocampal learning. Proc Natl Acad Sci U S A 1996; 93: 714-8.
74. Feng R, Rampon C, Tang YP, Shrom D, Jin J, Kyin M, et al. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 2001; 6: 911-26.
75. Gould E, Tanapat P, Hastings NB, Shors TJ. Neurogenesis in adulthood: a possible role in learning. Trends Cogn Sci 1999; 3: 186-92.
76. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001; 410: 372-6.
77. Kempermann G, Wiskott L, Gage FH. Functional significance of adult neurogenesis. Curr Opin Neurobiol 2004; 14: 186-91.
78. Treves A, Rolls ET. Computational analysis of the role of the hippocampus in memory. Hippocampus 1994; 4: 374-91.
79. Aimone JB, Wiles J, Gage FH. Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 2006; 9: 723-7.
80. Álvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron 2004; 4: 683-6.
81. Duman RS, Malberg J, Nakagawa S. Regulation of adult neurogenesis by psychotropic drugs and stress. J Pharmacol Exp Ther 2001; 299: 401-7.
82. Hallbergson AF, Gnatenco C, Peterson DA. Neurogenesis and brain injury: managing a renewable resource for repair. J Clin Invest 2003; 112: 1128-33.
83. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 1997; 17: 5820-9.
84. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB. 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 2001; 21: 6706-17.
85. Kuhn HG, Palmer TD, Fuchs E. Adult neurogenesis: a compensatory mechanism for neuronal damage. Eur Arch Psychiatry Clin Neurosci 2001; 251: 152-8.
86. Aberg MA, Aberg ND, Hedbacker H, Oscarsson J, Eriksson PS. Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 2000; 15: 2896-903.
87. Zigova T, Pencea V, Wiegand SJ, Luskin MB. Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci 1998; 11: 234-45.
88. Lee J, Duan W, Mattson MP. Evidence that brainderived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem 2002; 82: 1367-75.
89. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996; 16: 2027-33.
90. Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, Van der Koog D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 1996; 16: 2649-58.
91. Jin K, Mao XO, Sun Y, Xie L, Jin L, Nishi E, et al. Heparin-binding epidermal growth factor-like growth factor: hypoxia-inducible expression in vitro and stimulation of neurogenesis in vitro and in vivo. J Neurosci 2002; 22: 5365-73.
92. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci U S A 2002; 99: 11946-50.
93. Cameron HA, McEwen BS, Gould E. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 1995; 15: 4687-92.
94. Cameron HA, Tanapat P, Gould E. Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 1998; 82: 349-54.
95. Nacher J, Rosell DR, Alonso-Llosa G, McEwen BS. NMDA receptor antagonist treatment induces a longlasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur J Neurosci 2001; 13: 512-20.
96. Bai F, Bergeron M, Nelson DL. Chronic AMPAreceptor potentiator (LY451646) treatment increases cell proliferation in adult rat hippocampus. Neuropharmacology 2003; 44: 1013-21.
97. Yoshimizu T, Chaki S. Increased cell proliferation in the adult mouse hippocampus following chronic administration of group II metabotropic glutamate receptor antagonist, MGS0039. Biochem Biophys Res Commun 2004; 315: 493-6.
98. Gould E. Serotonin and hippocampal neurogenesis. Neuropsychopharmacology 1999; 21: S46-51.
99. Brezun JM, Daszuta A. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 1999; 89: 999-1002.
100. Brezun JM, Daszuta A. Serotonin may stimulate granule cell proliferation in the adult hippocampus, as observed in rats grafted with foetal raphe neurons. Eur J Neurosci 2000; 12: 391-6.
101. Jacobs B, Tanapat P, Reeves A, Gould E. Serotonin stimulates the production of new hippocampal granuleneurons via 5-HT1A receptor in the adult brain. Soc Neurosci 1998; Abstr. 24.
102. Duman RS, Heninger GR, Nestler EJ. Molecular and cellular theory of depression. Arch Gen Psychiatry 1997; 54: 597-606.
103. Kulkarni VA, Jha S, Vaidya VA. Depletion of norepinephrine decreases the proliferation, but does not influence the survival and differentiation, of granule cell progenitors in the adult rat hippocampus. Eur J Neurosci 2002; 16: 2008-12.
104. Bauer S, Moyse E, Jourdan F, Colpaert F, Martel JC, Marien M. Effects of the alpha 2-adrenoreceptor antagonist dexefaroxan on neurogenesis in the olfactory bulb of the adult rat in vivo: selective protection against neuronal death. Neuroscience 2003; 117: 281-91.
105. Hoglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH, Caille I, et al. Dopamine depletion impairs precursor cell proliferation in Parkinson's disease. Nat Neurosci 2004; 7: 726-35.
106. Banasr M, Hery M, Brezun JM, Daszuta A. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur J Neurosci 2001; 14: 1417-24.
107. Ormerod BK, Galea LA. Reproductive status influences cell proliferation and cell survival in the dentate gyrus of adult female meadow voles: a possible regulatory role for estradiol. Neuroscience 2001; 102: 369-79.
108. Tanapat P, Hastings NB, Reeves AJ, Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 1999; 19: 5792-801.
109. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC. Neural stem cell detection, characterization, and agerelated changes in the subventricular zone of mice. J Neurosci 2004; 24: 1726-33.
110. Sapolsky RM. Do glucocorticoid concentrations rise with age in the rat? Neurobiol Aging 1992; 13: 171-4.
111. Cameron HA, McKay RD. Restoring production of hippocampal neurons in old age. Nat Neurosci 1999; 2: 894-7.
112. Bizon JL, Gallagher M. Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline. Eur J Neurosci 2003; 18: 215-9.
113. Bondolfi L, Ermini F, Long JM, Ingram DK, Jucker M. Impact of age and caloric restriction on neurogenesis in the dentate gyrus of C57BL/6 mice. Neurobiol Aging 2004; 25: 333-40.
114. Kempermann G, Kronenberg G. Depressed new neurons -adult hippocampal neurogenesis and a cellular plasticity hypothesis of major depression. Biol Psychiatry 2003; 54: 499-503.
115. Peterson DA. Stem cells in brain plasticity and repair. Curr Opin Pharmacol 2002; 2: 34-42.
116. Tanapat P, Hastings NB, Gould E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J Comp Neurol 2005; 481: 252-65.
117. Gould E, Tanapat P, Rydel T, Hastings N. Regulation of hippocampal neurogenesis in adulthood. Biol Psychiatry 2000; 48: 715-20.
118. Mirescu C, Peters JD, Gould E. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 2004; 7: 841-6.
119. Van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 1999; 96: 13427-31.
120. Gould E. The effects of adrenal steroids and excitatory input on neuronal birth and survival. Ann N Y Acad Sci 1994; 743:73-93.
121. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 1992; 12: 3642-50.
122. Gould E, Cameron HA, McEwen BS. Blockade of NMDA receptors increases cell death and birth in the developing rat dentate gyrus. J Comp Neurol 1994; 340: 551-65.
123. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997; 386: 493-5.
124. Barnea A, Nottebohm F. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci U S A 1994; 11: 217-21.
125. Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 1999; 39: 569-78.
126. Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997; 17: 2492-8.
127. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci U S A 1998; 95: 3168-71.
128. Tanapat P, Hastings NB, Rydel TA, Galea LA, Gould E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 2001; 437: 496-504.
129. Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci U S A 2000; 97: 11032-7.
130. Lennington JB, Yang Z, Conove JC. Neural stem cells and the regulation of adult neurogenesis. Reprod Biol Endocrinol 2003; 1: 99.