Neurogenesis in the adult brain: From bench to bedside?;Adulte neurogenese im ZNS: Vom labor zur klinik?

Fortschritte der Neurologie Psychiatrie

Volumn 76, Issue 9, 2008, Pages 517-529

  Brandt, M D ^a   Storch, Alexander ^a,b  

^a CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Adult neurogenesis; Alzheimer's disease; Cerebral ischemia; Depression; Epilepsy; Hippocampus; Neural stem cells; Parkinson's disease

Indexed keywords

ALZHEIMER DISEASE; BRAIN DEVELOPMENT; BRAIN DISEASE; BRAIN FUNCTION; BRAIN ISCHEMIA; CELL PROLIFERATION; DEPRESSION; EPILEPSY; HIPPOCAMPUS; HUMAN; LATERAL BRAIN VENTRICLE; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PARKINSON DISEASE; REVIEW; SUBVENTRICULAR ZONE;

EID: 53049098182     PISSN: 07204299     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2008-1038218     Document Type: Review

References (156)

1. Ramon y Cajal S. Degeneration and Regeneration of the Nervous System. London, 1928: Oxford Univ. Press, 1913
2. Altman J. 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 1969; 137: 433-457
3. Altman J, Das GD. Postnatal neurogenesis in the guinea-pig. Nature 1967; 214: 1098-1101
4. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965; 124: 319-335
5. Kaplan MS, Hinds JW. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 1977; 197: 1092-1094
6. Gage FH. Mammalian neural stem cells. Science 2000; 287: 1433-1438
7. Gage FH. Neurogenesis in the adult brain. J Neurosci 2002; 22: 612-613
8. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997; 386: 493-495
9. 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: 2027-2033
10. Alvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron 2004; 41: 683-686
11. Temple S, Alvarez-Buylla A. Stem cells in the adult mammalian central nervous system. Curr Opin Neurobiol 1999; 9: 135-141
12. Palmer TD, Markakis EA, Willhoite AR et al. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 1999; 19: 8487-8497
13. Hermann A, Maisel M, Wegner F et al. Multipotent neural stem cells from the adult tegmentum with dopaminergic potential develop essential properties of functional neurons. Stem Cells 2006; 24: 949-964
14. Palmer TD, Ray J, Gage FH . FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci 1995; 6: 474-486
15. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000; 425: 479-494
16. Carleton A, Petreanu LT, Lansford R. A. A-B, M. LP. Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 2003; 6: 507-518
17. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci USA 1999; 96: 11619-11624
18. Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2001; 2: 287-293
19. Biebl M, Cooper CM, Winkler J et al. Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci Lett 2000; 291: 17-20
20. Baker H, Liu N, Chun HS et al. Phenotypic differentiation during migration of dopaminergic progenitor cells to the olfactory bulb. J Neurosci 2001; 21: 8505-8513
21. Kosaka K, Hama K, Nagatsu I et al. Postnatal development of neurons containing both catecholaminergic and GABAergic traits in the rat main olfactory bulb. Brain Res 1987; 403: 355-360
22. McLean JH, Shipley MT. Postmitotic, postmigrational expression of tyrosine hydroxylase in olfactory bulb dopaminergic neurons. J Neurosci 1988; 8: 3658-3669
23. Winner B, Cooper-Kuhn CM, Aigner R et al. Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci 2002; 16: 1681-1689
24. Seri B, Garcia-Verdugo JM, McEwen BS et al. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001; 21: 7153-7160
25. Filippov V, Kronenberg G, Pivneva T 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: 373-382
26. Kempermann G, Jessberger S, Steiner B et al. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004; 27: 447-452
27. Kronenberg G, Reuter K, Steiner B et al. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 2003; 467: 455-463
28. Steiner B, Kronenberg G, Jessberger S et al. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 2004; 46: 41-52
29. Tozuka Y, Fukuda S, Namba T et al. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 2005; 47: 803-815
30. Wang LP, Kempermann G, Kettenmann H. A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 2005; 29: 181-189
31. Plumpe T, Ehninger D, Steiner B et al. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 2006; 7: 77
32. Rao MS, Shetty AK. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 2004; 19: 234-246
33. Brandt MD, Jessberger S, Steiner B et al. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 2003; 24: 603-613
34. Hastings NB, Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 1999; 413: 146-154
35. Zhao C, Teng EM, Summers JrRG et al. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 2006; 26: 3-11
36. Kuhn HG, Biebl M, Wilhelm D et al. Increased generation of granule cells in adult Bcl-2-overexpressing mice: a role for cell death during continued hippocampal neurogenesis. Eur J Neurosci 2005; 22: 1907-1915
37. Kempermann G, Gast D, Kronenberg G et al. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 2003; 130: 391-399
38. Eriksson PS, Perfilieva E, Bjork-Eriksson T et al. Neurogenesis in the adult human hippocampus. Nat Med 1998; 4: 1313-1317
39. Curtis MA, Kam M, Nannmark U et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007; 315: 1243-1249
40. Sanai N, Tramontin AD, Quinones-Hinojosa A et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004; 427: 740-744
41. Bêdard A, Parent A. Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 2004; 151: 159-168
42. Liu Z, Martin LJ. Olfactory bulb core is a rich source of neural progenitor and stem cells in adult rodent and human. J Comp Neurol 2003; 459: 368-391
43. Sanai N, Berger MS, Garcia-Verdugo JM et al. Comment on "Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension". Science 2007; 318: 393; author reply 393
44. Kukekov VG, Laywell ED, Suslov O et al. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 1999; 156: 333-344
45. Roy NS, Benraiss A, Wang S et al. Promoter-targeted selection and isolation of neural progenitor cells from the adult human ventricular zone. J Neurosci Res 2000; 59: 321-331
46. Roy NS, Wang S, Jiang L et al. In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nat Med 2000; 6: 271-277
47. Hermann A, Maisel M, Liebau S et al. Mesodermal cell types induce neurogenesis from adult human hippocampal progenitor cells. J Neurochem 2006; 98: 629-640
48. Maisel M, Herr A, Milosevic J et al. Transcription profiling of adult and fetal human neuroprogenitors identifies divergent paths to maintain the neuroprogenitor cell state. Stem Cells 2007; 25: 1231-1240
49. Praag H van, Christie BR, Sejnowski TJ et al. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 1999; 96: 13427-13431
50. Brown J, Cooper-Kuhn CM, Kempermann G et al. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 2003; 17: 2042-2046
51. Rochefort C, Gheusi G, Vincent JD et al. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 2002; 22: 2679-2689
52. Praag H van, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999; 2: 266-270
53. Carro E, Nunez A, Busiguina S et al. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 2000; 20: 2926-2933
54. Fabel K, Tam B, Kaufer D et al. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 2003; 18: 2803-2812
55. Cameron HA, Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994; 61: 203-209
56. Gould E. The effects of adrenal steroids and excitatory input on neuronal birth and survival. Ann N Y Acad Sci 1994; 743: 73-92
57. Gould E, McEwen BS, Tanapat P et al. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997; 17: 2492-2498
58. Cameron HA, McKay RD. Restoring production of hippocampal neurons in old age. Nat Neurosci 1999; 2: 894-897
59. Kempermann G, Kuhn HG, Gage FH. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 1998; 18: 3206-3212
60. 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: 2027-2033
61. Kempermann G, Gast D, Gage FH. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 2002; 52: 135-143
62. Kempermann G, Gage FH. Experience-dependent regulation of adult hippocampal neurogenesis: effects of long-term stimulation and stimulus withdrawal. Hippocampus 1999; 9: 321-332
63. Jessberger S, Kempermann G. Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci 2003; 18: 2707-2712
64. Magavi SS, Mitchell BD, Szentirmai O et al. Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J Neurosci 2005; 25: 10729-10739
65. Praag H van, Schinder AF, Christie BR et al. Functional neurogenesis in the adult hippocampus. Nature 2002; 415: 1030-1034
66. Abraham WC, Mason SE, Demmer J et al. Correlations between immediate early gene induction and the persistence of long-term potentiation. Neuroscience 1993; 56: 717-727
67. Ben-Ari Y. Cell death and synaptic reorganizations produced by seizures. Epilepsia 2001; 42 Suppl 3: 5-7
68. Shors TJ, Miesegaes G, Beylin A et al. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001; 410: 372-376
69. Shors TJ, Townsend DA, Zhao M et al. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002; 12: 578-584
70. Snyder JS, Hong NS, McDonald RJ et al. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005; 130: 843-852
71. Kempermann G. Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 2002; 22: 635-638
72. Kempermann G. The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for? Trends Neurosci 2008; 31: 163-169
73. Donovan MH, Yazdani U, Norris RD et al. Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J Comp Neurol 2006; 495: 70-83
74. Haughey NJ, Nath A, Chan SL et al. Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J Neurochem 2002; 83: 1509-1524
75. Jin K, Peel AL, Mao XO et al. Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci U S A 2004; 101: 343-347
76. Jin K, Galvan V, Xie L et al. Enhanced neurogenesis in Alzheimer 2004s disease transgenic (PDGF-APPSw,Ind) mice. Proc Natl Acad Sci U S A 2004; 101: 13363-13367
77. Zhang YW, Xu H. Molecular and cellular mechanisms for Alzheimer's disease: understanding APP metabolism. Curr Mol Med 2007; 7: 687-696
78. Chen G, Chen KS, Knox J et al. A learning deficit related to age and beta-amyloid plaques in a mouse model of Alzheimer's disease. Nature 2000; 408: 975-979
79. Nagy Z, Esiri MM, Smith AD. The cell division cycle and the pathophysiology of Alzheimer's disease. Neuroscience 1998; 87: 731-739
80. Becker M, Lavie V, Solomon B. Stimulation of endogenous neurogenesis by anti-EFRH immunization in a transgenic mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 2007; 104: 1691-1696
81. Rockenstein E, Mante M, Adame A et al. Effects of Cerebrolysin on neurogenesis in an APP transgenic model of Alzheimer's disease. Acta Neuropathol 2007; 113: 265-275
82. Costa DA, Cracchiolo JR, Bachstetter AD et al. Enrichment improves cognition in AD mice by amyloid-related and unrelated mechanisms. Neurobiol Aging 2007; 28: 831-844
83. Lazarov O, Robinson J, Tang YP et al. Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell 2005; 120: 701-713
84. Arendash GW, Garcia MF, Costa DA et al. Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable beta-amyloid deposition. Neuroreport 2004; 15: 1751-1754
85. Wolf SA, Kronenberg G, Lehmann K et al. Cognitive and physical activity differently modulate disease progression in the amyloid precursor protein (APP)-23 model of Alzheimer's disease. Biol Psychiatry 2006; 60: 1314-1323
86. Fratiglioni L, Wang HX. Brain reserve hypothesis in dementia. J Alzheimers Dis 2007; 12: 11-22
87. Steiner B, Wolf S, Kempermann G. Adult neurogenesis and neurodegenerative disease. Regen Med 2006; 1: 15-28
88. Jin K, Xie L, Mao XO et al. Alzheimer's disease drugs promote neurogenesis. Brain Res 2006; 1085: 183-188
89. Kaneko N, Okano H, Sawamoto K. Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells 2006; 11: 1145-1159
90. Zhao M, Momma S, Delfani K et al. Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci U S A 2003; 100: 7925-7930
91. Kampen JM van, Eckman CB. Dopamine D3 receptor agonist delivery to a model of Parkinson's disease restores the nigrostriatal pathway and improves locomotor behavior. J Neurosci 2006; 26: 7272-7280
92. Frielingsdorf H, Schwarz K, Brundin P et al. No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc Natl Acad Sci U S A 2004; 101: 10177-10182
93. Lie DC, Dziewczapolski G, Willhoite AR et al. The adult substantia nigra contains progenitor cells with neurogenic potential. J Neurosci 2002; 22: 6639-6649
94. Reimers D, Herranz AS, Diaz-Gil JJ et al. Intrastriatal infusion of liver growth factor stimulates dopamine terminal sprouting and partially restores motor function in 6-hydroxydopamine-lesioned rats. J Histochem Cytochem 2006; 54: 457-465
95. Hoglinger GU, Breunig JJ, Depboylu C et al. The pRb/E2F cell-cycle pathway mediates cell death in Parkinson's disease. Proc Natl Acad Sci U S A 2007; 104: 3585-3590
96. Mohapel P, Frielingsdorf H, Haggblad J et al. Platelet-derived growth factor (PDGF-BB) and brain-derived neurotrophic factor (BDNF) induce striatal neurogenesis in adult rats with 6-hydroxydopamine lesions. Neuroscience 2005; 132: 767-776
97. Cooper O, Isacson O. Intrastriatal transforming growth factor alpha delivery to a model of Parkinson's disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons. J Neurosci 2004; 24: 8924-8931
98. Diaz J, Ridray S, Mignon V et al. Selective expression of dopamine D3 receptor mRNA in proliferative zones during embryonic development of the rat brain. J Neurosci 1997; 17: 4282-4292
99. Ohtani N, Goto T, Waeber C et al. Dopamine modulates cell cycle in the lateral ganglionic eminence. J Neurosci 2003; 23: 2840-2850
100. Höglinger GU, Rizk P, Muriel MP et al. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 2004; 7: 726-735
101. Freundlieb N, François C, Tandé D et al. Dopaminergic substantia nigra neurons project topographically organized to the subventricular zone and stimulate precursor cell proliferation in aged primates. J Neurosci 2006; 26: 2321-2325
102. Borta A, Hoglinger GU. Dopamine and adult neurogenesis. J Neurochem 2007; 100: 587-595
103. Gould NF, Holmes MK, Fantie BD et al. Performance on a virtual reality spatial memory navigation task in depressed patients. Am J Psychiatry 2007; 164: 516-519
104. Campbell S, Marriott M, Nahmias C et al. Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am J Psychiatry 2004; 161: 598-607
105. Videbech P, Ravnkilde B. Hippocampal volume and depression: a meta-analysis of MRI studies. Am J Psychiatry 2004; 161: 1957-1966
106. MacQueen GM, Campbell S, McEwen BS et al. Course of illness, hippocampal function, and hippocampal volume in major depression. Proc Natl Acad Sci U S A 2003; 100: 1387-1392
107. Malberg JE, Eisch AJ, Nestler EJ et al. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 2000; 20: 9104-9110
108. Czeh B, Michaelis T, Watanabe T et al. Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci U S A 2001; 98: 12796-12801
109. Santarelli L, Saxe M, Gross C et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003; 301: 805-809
110. Duman RS, Monteggia LM. A neurotrophic model for stress-related mood disorders. Biol Psychiatry 2006; 59: 1116-1127
111. Jiang W, Zhang Y, Xiao L et al. Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J Clin Invest 2005; 115: 3104-3116
112. Henn FA, Vollmayr B. Stress models of depression: forming genetically vulnerable strains. Neurosci Biobehav Rev 2005; 29: 799-804
113. Vollmayr B, Mahlstedt MM, Henn FA. Neurogenesis and depression: what animal models tell us about the link. Eur Arch Psychiatry Clin Neurosci 2007; 257: 300-303
114. Encinas JM, Vaahtokari A, Enikolopov G. Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci U S A 2006; 103: 8233-8238
115. Nakagawa S, Kim JE, Lee R et al. Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J Neurosci 2002; 22: 9868-9876
116. Nakagawa S, Kim JE, Lee R et al. Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 2002; 22: 3673-3682
117. Perera TD, Coplan JD, Lisanby SH et al. Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J Neurosci 2007; 27: 4894-4901
118. Scott BW, Wojtowicz JM, Burnham WM. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp Neurol 2000; 165: 231-236
119. Guzman-Marin R, Bashir T, Suntsova N et al. Hippocampal neurogenesis is reduced by sleep fragmentation in the adult rat. Neuroscience 2007; 148: 325-333
120. Guzman-Marin R, Suntsova N, Methippara M et al. Sleep deprivation suppresses neurogenesis in the adult hippocampus of rats. Eur J Neurosci 2005; 22: 2111-2116
121. Grassi Zucconi G, Cipriani S, Balgkouranidou I et al. "One night" sleep deprivation stimulates hippocampal neurogenesis. Brain Res Bull 2006; 69: 375-381
122. McEwen BS. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 2005; 54: 20-23
123. Czeh B, Lucassen PJ. What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? Eur Arch Psychiatry Clin Neurosci 2007; 257: 250-260
124. Imai F, Suzuki H, Oda J et al. Neuroprotective effect of exogenous microglia in global brain ischemia. J Cereb Blood Flow Metab 2007; 27: 488-500
125. Liu J, Solway K, Messing RO et al. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 1998; 18: 7768-7778
126. Takagi Y, Nozaki K, Takahashi J et al. Proliferation of neuronal precursor cells in the dentate gyrus is accelerated after transient forebrain ischemia in mice. Brain Res 1999; 831: 283-287
127. Tonchev AB, Yamashima T. Differential neurogenic potential of progenitor cells in dentate gyrus and CA1 sector of the postischemic adult monkey hippocampus. Exp Neurol 2006; 198: 101-113
128. Yagita Y, Kitagawa K, Ohtsuki T et al. Neurogenesis by progenitor cells in the ischemic adult rat hippocampus. Stroke 2001; 32: 1890-1896
129. Arvidsson A, Kokaia Z, Lindvall O. N-methyl-D-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur J Neurosci 2001; 14: 10-18
130. Bendel O, Bueters T, Euler M von et al. Reappearance of hippocampal CA1 neurons after ischemia is associated with recovery of learning and memory. J Cereb Blood Flow Metab 2005; 25: 1586-1595
131. Ehninger D, Kempermann G. Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cereb Cortex 2003; 13: 845-851
132. Gould E, Reeves AJ, Graziano MS et al. Neurogenesis in the neocortex of adult primates. Science 1999; 286: 548-552
133. Kornack DR, Rakic P. Cell proliferation without neurogenesis in adult primate neocortex. Science 2001; 294: 2127-2130
134. Nowakowski RS, Hayes NL. New neurons: extraordinary evidence or extraordinary conclusion? Science 2000; 288: 771
135. Arvidsson A, Collin T, Kirik D et al. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002; 8: 963-970
136. Jin K, Minami M, Lan JQ et al. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci U S A 2001; 98: 4710-4715
137. Zhang R, Zhang Z, Wang L et al. Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 2004; 24: 441-448
138. Zhang RL, LeTourneau Y, Gregg SR et al. Neuroblast division during migration toward the ischemic striatum: a study of dynamic migratory and proliferative characteristics of neuroblasts from the subventricular zone. J Neurosci 2007; 27: 3157-3162
139. Ehrenreich H, Hasselblatt M, Dembowski C et al. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 2002; 8: 495-505
140. Wang L, Zhang Z, Wang Y et al. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 2004; 35: 1732-1737
141. Schabitz WR, Steigleder T, Cooper-Kuhn CM et al. Intravenous brain-derived neurotrophic factor enhances poststroke sensorimotor recovery and stimulates neurogenesis. Stroke 2007; 38: 2165-2172
142. Bengzon J, Kokaia Z, Elmer E et al. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci U S A 1997; 94: 10432-10437
143. Parent JM, Yu TW, Leibowitz RT et al. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 1997; 17: 3727-3738
144. Madsen TM, Treschow A, Bengzon J et al. Increased neurogenesis in a model of electroconvulsive therapy. Biol Psychiatry 2000; 47: 1043-1049
145. Nakagawa E, Aimi Y, Yasuhara O et al. Enhancement of progenitor cell division in the dentate gyrus triggered by initial limbic seizures in rat models of epilepsy. Epilepsia 2000; 41: 10-18
146. Parent JM, Janumpalli S, McNamara JO et al. Increased dentate granule cell neurogenesis following amygdala kindling in the adult rat. Neurosci Lett 1998; 247: 9-12
147. Helmstaedter C. Effects of chronic epilepsy on declarative memory systems. Prog Brain Res 2002; 135: 439-453
148. Stafstrom CE, Chronopoulos A, Thurber S et al. Age-dependent cognitive and behavioral deficits after kainic acid seizures. Epilepsia 1993; 34: 420-432
149. Jessberger S, Romer B, Babu H et al. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp Neurol 2005; 196: 342-351
150. Huttmann K, Sadgrove M, Wallraff A et al. Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: functional and immunocytochemical analysis. Eur J Neurosci 2003; 18: 2769-2778
151. Houser CR. Morphological changes in the dentate gyrus in human temporal lobe epilepsy. Epilepsy Res Suppl 1992; 7: 223-234
152. Shapiro LA, Korn MJ, Ribak CE. Newly generated dentate granule cells from epileptic rats exhibit elongated hilar basal dendrites that align along GFAP-immunolabeled processes. Neuroscience 2005; 136: 823-831
153. Scharfman HE, Goodman JH, Sollas AL. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J Neurosci 2000; 20: 6144-6158
154. Jakubs K, Nanobashvili A, Bonde S et al. Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron 2006; 52: 1047-1059
155. Jessberger S, Nakashima K, Clemenson JrGD et al. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 2007; 27: 5967-5975
156. Manganas LN, Zhang X, Li Y et al. Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science 2007; 318: 980-985