Glia and hippocampal neurogenesis in the normal, aged and epileptic brain

Interaction Between Neurons and Glia in Aging and Disease

Volumn , Issue , 2007, Pages 375-390

  Gray, William P ^a   Laskowski, Alexandra ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 80051719065     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-70830-0_17     Document Type: Chapter

References (131)

1. Abrous, D.N., Koehl, M. and Le Moal, M., 2005, Adult neurogenesis: from precursors to network and physiology. Physiol. Rev. 85: 523.
2. Altman, J. and Bayer, S.A., 1990, Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J. Comp. Neurol. 301: 365.
3. Altman, J. and Das, G.D., 1965, Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124: 319.
4. Banerjee, S.B., Rajendran, R., Dias, B.G., Ladiwala, U., Tole, S. and Vaidya, V.A., 2005, Recruitment of the Sonic hedgehog signaling cascade in electroconvulsive seizure-mediated regulation of adult rat hippocampal neuro genesis. Eur. J. Neurosci. 22: 1570.
5. Battista, D., Ferrari, C.C., Gage, F.H. and Pitossi, F.J., 2006, Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur. J. Neurosci. 23: 83.
6. Bayer, S.A., Yackel, J.W. and Puri, P.S., 1982, Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216: 890.
7. Bengzon, J., Kokaia, Z., Elmer, E., Nanobashvili, A., Kokaia, M. and Lindvall, O., 1997, Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Natl Acad. Sci. USA 94: 10432.
8. Bernardino, L., Ferreira, R., Cristóvão, A.J., Sales, F. and Malva, J.O., 2005, Inflammation and neurogenesis in temporal lobe epilepsy. Curr. Drug Targets CNS Neurol. Disord. 4: 349.
9. Bizon, J.L. and Gallagher, M., 2003, Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline. Eur. J. Neurosci. 18: 215.
10. Blondel, O., Collin, C., McCarran, W.J., Zhu, S., Zamostiano, R., Gozes, I., Brenneman, D.E. and McKay, R.D., 2000, A glia-derived signal regulating neuronal differentiation. J. Neurosci. 20: 8012.
11. Blumcke, I., Schewe, J.C., Normann, S., Brustle, O., Schramm, J., Elger, C.E. and Wiestler, O.D., 2001, Increase of nestin-immunoreactive neural precursor cells in the dentate gyrus of pediatric patients with early-onset temporal lobe epilepsy. Hippocampus 11: 311.
12. Bonde, S., Ekdahl, C.T. and Lindvall, O., 2006, Long-term neuronal replacement in adult rat hippocampus after status epilepticus despite chronic inflammation. Eur. J. Neurosci. 23: 965.
13. Brezun, J.M. and Daszuta, A., 2000, Serotonin may stimulate granule cell proliferation in the adult hippocampus, as observed in rats grafted with foetal raphe neurons. Eur. J. Neurosci. 12: 391.
14. Buniatian, G., Traub, P., Albinus, M., Beckers, G., Buchmann, A., Gebhardt, R. and Osswald, H., 1998, The immunoreactivity of glial fibrillary acidic protein in mesangial cells and podocytes of the glomeruli of rat kidney in vivo and in culture. Biol. Cell 90: 53.
15. Bush, T.G., Savidge, T.C., Freeman, T.C., Cox, H.J., Campbell, E.A., Mucke, L., Johnson, M.H. and Sofroniew, M.V., 1998, Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 93: 189.
16. Butovsky, O., Talpalar, A.E., Ben-Yaakov, K. and Schwartz, M., 2005, Activation of microglia by aggregated betaamyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-gamma and IL-4 render them protective. Mol. Cell Neurosci. 29: 381.
17. Butovsky, O., Ziv, Y., Schwartz, A., Landa, G., Talpalar, A.E., Pluchino, S., Martino, G. and Schwartz, M., 2006, Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol. Cell Neurosci. 31: 149.
18. Cameron, H.A. and Gould, E., 1994, Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61: 203.
19. Cameron, H.A. and McKay, R.D., 1999, Restoring production of hippocampal neurons in old age. Nat. Neurosci. 2: 894.
20. Cameron, H.A. and McKay, R.D., 2001, Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435: 406.
21. Cameron, H.A., McEwen, B.S. and Gould, E., 1995, Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J. Neurosci. 15: 4687.
22. Cameron, H.A., Tanapat, P. and Gould, E., 1998, Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 82: 349.
23. Cocchia, D., 1981, Immunocytochemical localization of S-100 protein in the brain of adult rat. An ultrastructural study. Cell Tissue Res. 214: 529.
24. Crespel, A., Rigau, V., Coubes, P., Rousset, M.C., de Bock, F., Okano, H., Baldy-Moulinier, M., Bockaert, J. and Lerner-Natoli, M., 2005, Increased number of neural progenitors in human temporal lobe epilepsy. Neurobiol. Dis. 19: 436.
25. Crespo, D., Stanfield, B.B. and Cowan, W.M., 1986, Evidence that late-generated granule cells do not simply replace earlier formed neurons in the rat dentate gyrus. Exp. Brain Res. 62: 541.
26. D'Sa, C. and Duman, R.S., 2002, Antidepressants and neuroplasticity. Bipolar Disord. 4: 183.
27. Dayer, A.G., Ford, A.A., Cleaver, K.M., Yassaee, M. and Cameron, H.A., 2003, Short-term and long-term survival of new neurons in the rat dentate gyrus. J. Comp. Neurol. 460: 563.
28. Doetsch, F., Caille, I., Lim, D.A., Garcia-Verdugo, J.M. and Alvarez-Buylla, A., 1999, Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703.
29. Drapeau, E., Mayo, W., Aurousseau, C., Le Moal, M., Piazza, P.V. and Abrous, D.N., 2003, Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl Acad. Sci. USA 100: 14385.
30. Eichenbaum, H., 1997, Declarative memory: insights from cognitive neurobiology. Annu. Rev. Psychol. 48: 547.
31. Ekdahl, C.T., Claasen, J.H., Bonde, S., Kokaia, Z. and Lindvall, O., 2003, Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl Acad. Sci. USA 100: 13632.
32. Encinas, J.M., Vaahtokari, A. and Enikolopov, G. , 2006, Fluoxetine targets early progenitor cells in the adult brain. Proc. Natl Acad. Sci. USA 103: 8233.
33. Eriksson, P.S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A.M., Nordborg, C., Peterson, D.A. and Gage, F.H., 1998, Neurogenesis in the adult human hippocampus. Nat. Med. 4: 1313.
34. Filippov, V., Kronenberg, G., Pivneva, T., Reuter, K., Steiner, B., Wang, L.P., Yamaguchi, M., Kettenmann, H. and Kempermann, G., 2003, Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci. 23: 373.
35. Francis, F., Koulakoff, A., Boucher, D., Chafey, P., Schaar, B., Vinet, M.C., Friocourt, G., McDonnell, N., Reiner, O., Kahn, A., McConnell, S.K., Berwald-Netter, Y., Denoulet, P. and Chelly, J., 1999, Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23: 247.
36. Fukuda, S., Kato, F., Tozuka, Y., Yamaguchi, M., Miyamoto, Y. and Hisatsune, T., 2003, Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J. Neurosci. 23: 9357.
37. Gage, F.H., 2002, Neurogenesis in the adult brain. J. Neurosci. 22: 612.
38. Gaiano, N. and Fishell, G., 2002, The role of notch in promoting glial and neural stem cell fates. Annu. Rev. Neurosci. 25: 471.
39. Garcia, A., Steiner, B., Kronenberg, G., Bick-Sander, A. and Kempermann, G., 2004a, Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 3: 363.
40. Garcia, A.D., Doan, N.B., Imura, T., Bush, T.G. and Sofroniew, M.V., 2004b, GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat. Neurosci. 7: 1233.
41. Gould, E., McEwen, B.S., Tanapat, P., Galea, L.A. and Fuchs, E., 1997, Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci. 17: 2492.
42. Gould, E., Beylin, A., Tanapat, P., Reeves, A. and Shors, T.J., 1999, Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2: 260.
43. Gray, W.P. and Sundstrom, L.E., 1998, Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res. 790: 52.
44. Hack, M.A., Saghatelyan, A., de Chevigny, A., Pfeifer, A., Ashery-Padan, R., Lledo, P.M. and Gotz, M., 2005, Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat. Neurosci. 8: 865.
45. Hagihara, H., Hara, M., Tsunekawa, K., Nakagawa, Y., Sawada, M. and Nakano, K., 2005, Tonic-clonic seizures induce division of neuronal progenitor cells with concomitant changes in expression of neurotrophic factors in the brain of pilocarpine-treated mice. Brain Res. Mol. Brain Res. 139: 258.
46. Hastings, N.B. and Gould, E., 1999, Rapid extension of axons into the CA3 region by adult-generated granule cells. J. Comp. Neurol. 413: 146.
47. Hattiangady, B., Rao, M.S. and Shetty, A.K., 2004, Chronic temporal lobe epilepsy is associated with severely declined dentate neurogenesis in the adult hippocampus. Neurobiol. Dis. 17: 473.
48. Heinrich, C., Nitta, N., Flubacher, A., Muller, M., Fahrner, A., Kirsch, M., Freiman, T., Suzuki, F., Depaulis, A., Frotscher, M. and Haas, C.A., 2006, Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J. Neurosci. 26: 4701.
49. Hinterkeuser, S., Gray, W., Hager, G., Sundstrom, L. and Steinhauser, C., 1999, Characterization of astrocytic proliferation in rat dentate gyrus. J. Neurochem. 73: S70.
50. Holmberg, K.H. and Patterson, P.H., 2006, Leukemia inhibitory factor is a key regulator of astrocytic, microglial and neuronal responses in a low-dose pilocarpine injury model. Brain Res. 1075: 26.
51. Houser, C.R., 1990, Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res. 535: 195.
52. Howell, O.W., Scharfman, H.E., Herzog, H., Sundstrom, L.E., Beck-Sickinger, A. and Gray, W.P., 2003, Neuropeptide Y is neuroproliferative for post-natal hippocampal precursor cells. J. Neurochem. 86: 646.
53. Howell, O.W., Doyle, K., Goodman, J.H., Scharfman, H.E., Herzog, H., Pringle, A., Beck-Sickinger, A.G. and Gray, W.P., 2005, Neuropeptide Y stimulates neuronal precursor proliferation in the post-natal and adult dentate gyrus. J. Neurochem. 93: 560.
54. Huttmann, K., Sadgrove, M., Wallraff, A., Hinterkeuser, S., Kirchhoff, F., Steinhauser, C. and Gray, W.P., 2003, Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: functional and immunocytochemical analysis. Eur. J. Neurosci. 18: 2769.
55. 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.
56. Jacobs, B.L., Praag, H. and Gage, F.H., 2000, Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol. Psychiatry 5: 262.
57. Jessberger, S., Romer, B., Babu, H. and Kempermann, G., 2005, Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp. Neurol. 196: 342.
58. Jin, K., Sun, Y., Xie, L., Batteur, S., Mao, X.O., Smelick, C., Logvinova, A. and Greenberg, D.A., 2003, Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2: 175.
59. Johansson, C.B., Momma, S., Clarke, D.L., Risling, M., Lendahl, U. and Frisen, J., 1999, Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96: 25.
60. Karishma, K.K. and Herbert, J., 2002, Dehydroepiandrosterone (DHEA) stimulates neurogenesis in the hippocampus of the rat, promotes survival of newly formed neurons and prevents corticosterone-induced suppression. Eur. J. Neurosci. 16: 445.
61. Kempermann, G., Kuhn, H.G. and Gage, F.H., 1997, More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493.
62. Kempermann, G., Jessberger, S., Steiner, B. and Kronenberg, G., 2004, Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27: 447.
63. + regulatory T-Cells at the crossroads of health and disease. Neuromol. Med. 7: 197.
64. Kralic, J.E., Ledergerber, D.A. and Fritschy, J.M., 2005, Disruption of the neurogenic potential of the dentate gyrus in a mouse model of temporal lobe epilepsy with focal seizures. Eur. J. Neurosci. 22: 1916.
65. Kuhn, H.G., Dickinson-Anson, H. and Gage, F.H., 1996, Neurogenesis in the dentate gyrus of the adult rat: agerelated decrease of neuronal progenitor proliferation. J. Neurosci. 16: 2027.
66. 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. USA 97: 13883.
67. Lemaire, V., Koehl, M., Le Moal, M. and Abrous, D.N., 2000, Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl Acad. Sci. USA 97: 11032.
68. Lendahl, U., Zimmerman, L.B. and McKay, R.D., 1990, CNS stem cells express a new class of intermediate filament protein. Cell 60: 585.
69. Levison, S.W. and Goldman, J.E., 1993, Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10: 201.
70. Levison, S.W., Young, G.M. and Goldman, J.E., 1999, Cycling cells in the adult rat neocortex preferentially generate oligodendroglia. J. Neurosci. Res. 57: 435.
71. Levitt, P. and Rakic, P., 1980, Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J. Comp. Neurol. 193: 815.
72. Lie, D.C., Colamarino, S.A., Song, H.J., Desire, L., Mira, H., Consiglio, A., Lein, E.S., Jessberger, S., Lansford, H., Dearie, A.R. and Gage, F.H., 2005, Wnt signaling regulates adult hippocampal neurogenesis. Nature 437: 1370.
73. Lim, D.A., Tramontin, A.D., Trevejo, J.M., Herrera, D.G., Garcia-Verdugo, J.M. and Alvarez-Buylla, A., 2000, Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28: 713.
74. Liu, X., Wang, Q., Haydar, T.F. and Bordey, A., 2005, Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat. Neurosci. 8: 1179.
75. Lois, C. and Alvarez-Buylla, A., 1993, Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA 90: 2074.
76. Ma, D.K., Ming, G.L. and Song, H., 2005, Glial influences on neural stem cell development: cellular niches for adult neurogenesis. Curr. Opin. Neurobiol. 15: 514.
77. Malberg, J.E., Eisch, A.J., Nestler, E.J. and Duman, R.S., 2000, Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20: 9104.
78. Markakis, E.A. and Gage, F.H., 1999, Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J. Comp. Neurol. 406: 449.
79. Mathern, G.W., Leiphart, J.L., De Vera, A., Adelson, P.D., Seki, T., Neder, L. and Leite, J.P., 2002, Seizures decrease postnatal neurogenesis and granule cell development in the human fascia dentata. Epilepsia 43 (suppl. 5): 68.
80. Mazarati, A., Lu, X., Kilk, K., Langel, U., Wasterlain, C. and Bartfai, T., 2004, Galanin type 2 receptors regulate neuronal survival, susceptibility to seizures and seizure-induced neurogenesis in the dentate gyrus. Eur. J. Neurosci. 19: 3235.
81. McDonald, H.Y. and Wojtowicz, J.M., 2005, Dynamics of neurogenesis in the dentate gyrus of adult rats. Neurosci. Lett. 385: 70.
82. Merrill, D.A., Karim, R., Darraq, M., Chiba, A.A. and Tuszynski, M.H., 2003, Hippocampal cell genesis does not correlate with spatial learning ability in aged rats. J. Comp. Neurol. 459: 201.
83. Monje, M.L., Toda, H. and Palmer, T.D., 2003, Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760.
84. Muotri, A.R., Chu, V.T., Marchetto, M.C., Deng, W., Moran, J.V. and Gage, F.H., 2005, Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435: 903.
85. Nacher, J., Rosell, D.R., Alonso-Llosa, G. and McEwen, B.S., 2001, NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur. J. Neurosci. 13: 512.
86. Nakagawa, E., Aimi, Y., Yasuhara, O., Tooyama, I., Shimada, M., McGeer, P.L. and Kimura, H., 2000, Enhancement of progenitor cell division in the dentate gyrus triggered by initial limbic seizures in rat models of epilepsy. Epilepsia 41: 10.
87. Namba, T., Mochizuki, H., Onodera, M., Mizuno, Y., Namiki, H. and Seki, T., 2005, The fate of neural progenitor cells expressing astrocytic and radial glial markers in the postnatal rat dentate gyrus. Eur. J. Neurosci. 22: 1928.
88. Navarro-Quiroga, I., Hernandez-Valdes, M., Lin, S.L. and Naegele, J.R., 2006, Postnatal cellular contributions of the hippocampus subventricular zone to the dentate gyrus, corpus callosum, fimbria, and cerebral cortex. J. Comp. Neurol. 497: 833.
89. Neubauer, K., Knittel, T., Aurisch, S., Fellmer, P. and Ramadori, G., 1996, Glial fibrillary acidic protein-a cell type specific marker for Ito cells in vivo and in vitro. J. Hepatol. 24: 719.
90. O'Kusky, J.R., Ye, P. and D'Ercole, A.J., 2000, Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J. Neurosci. 20: 8435.
91. Overstreet-Wadiche, L.S., Bromberg, D.A., Bensen, A.L. and Westbrook, G.L., 2006, Seizures accelerate functional integration of adult-generated granule cells. J. Neurosci. 26: 4095.
92. Parent, J.M., 2002, The role of seizure-induced neurogenesis in epileptogenesis and brain repair. Epilepsy Res. 50: 179.
93. Parent, J.M., Yu, T.W., Leibowitz, R.T., Geschwind, D.H., Sloviter, R.S. and Lowenstein, D.H., 1997, Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17: 3727.
94. Parent, J.M., Valentin, V.V. and Lowenstein, D.H., 2002, Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J. Neurosci. 22: 3174.
95. Parent, J.M., von dem Bussche, N. and Lowenstein, D.H., 2006, Prolonged seizures recruit caudal subventricular zone glial progenitors into the injured hippocampus. Hippocampus 16: 321.
96. Pirttila, T.J., Lukasiuk, K., Hakansson, K., Grubb, A., Abrahamson, M. and Pitkanen, A., 2005, Cystatin C modulates neurodegeneration and neurogenesis following status epilepticus in mouse. Neurobiol. Dis. 20: 241.
97. Prickaerts, J., Koopmans, G., Blokland, A. and Scheepens, A., 2004, Learning and adult neurogenesis: survival with or without proliferation? Neurobiol. Learn. Mem. 81: 1.
98. Radley, J.J. and Jacobs, B.L., 2003, Pilocarpine-induced status epilepticus increases cell proliferation in the dentate gyrus of adult rats via a 5-HT1A receptor-dependent mechanism. Brain Res. 966: 1.
99. Rao, M. and Shetty, A.K., 2004, 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. 19: 234.
100. Rao, M.S., Hattiangady, B., Abdel-Rahman, A., Stanley, D.P. and Shetty, A.K., 2005, Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur. J. Neurosci. 21: 464.
101. Rickmann, M., Amaral, D.G. and Cowan, W.M., 1987, Organization of radial glial cells during the development of the rat dentate gyrus. J. Comp. Neurol. 264: 449.
102. Rietze, R., Poulin, P. and Weiss, S., 2000, Mitotically active cells that generate neurons and astrocytes are present in multiple regions of the adult mouse hippocampus. J. Comp. Neurol. 424: 397.
103. Sadgrove, M.P., Chad, J.E. and Gray, W.P., 2005, Kainic acid induces rapid cell death followed by transiently reduced cell proliferation in the immature granule cell layer of rat organotypic hippocampal slice cultures. Brain Res. 1035: 111.
104. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C. and Hen, R., 2003, Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301: 805.
105. Scharfman, H.E. and Gray, W.P., 2006, Plasticity of neuropeptide Y in the dentate gyrus after seizures, and its relevance to seizure-induced neurogenesis. EXS 193.
106. Scharfman, H.E., Goodman, J.H. and Sollas, A.L., 2000, 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. 20: 6144.
107. Schlessinger, A.R., Cowan, W.M. and Gottlieb, D.I., 1975, An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J. Comp. Neurol. 159: 149.
108. Schmechel, D.E. and Rakic, P., 1979, A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat. Embryol. (Berl.) 156: 115.
109. Schwartz, M., Butovsky, O., Bruck, W. and Hanisch, U.K., 2006, Microglial phenotype: is the commitment reversible? Trends Neurosci. 29: 68.
110. Seki, T. and Arai, Y., 1995, Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 6: 2479.
111. Seki, T. and Arai, Y., 1999, Temporal and spacial relationships between PSA-NCAM-expressing, newly generated granule cells, and radial glia-like cells in the adult dentate gyrus. J. Comp. Neurol. 410: 503.
112. Seri, B., Garcia-Verdugo, J.M., Collado-Morente, L., McEwen, B.S. and Alvarez-Buylla, A., 2004, Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J. Comp. Neurol. 478: 359.
113. Shapiro, L.A., Korn, M.J., Shan, Z. and Ribak, C.E., 2005, GFAP-expressing radial glia-like cell bodies are involved in a one-to-one relationship with doublecortin-immunolabeled newborn neurons in the adult dentate gyrus. Brain Res. 1040: 81.
114. Shetty, A.K., Hattiangady, B. and Shetty, G.A., 2005, Stem/progenitor cell proliferation factors FGF-2, IGF-1, and VEGF exhibit early decline during the course of aging in the hippocampus: role of astrocytes. Glia 51: 173.
115. Shors, T.J., 2004, Memory traces of trace memories: neurogenesis, synaptogenesis and awareness. Trends Neurosci. 27: 250.
116. Shors, T.J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T. and Gould, E., 2001, Neurogenesis in the adult is involved in the formation of trace memories. Nature 410: 372.
117. Simon, M., Czeh, B. and Fuchs, E., 2005, Age-dependent susceptibility of adult hippocampal cell proliferation to chronic psychosocial stress. Brain Res. 1049: 244.
118. Smith, P.D., McLean, K.J., Murphy, M.A., Turnley, A.M. and Cook, M.J., 2005, Seizures, not hippocampal neuronal death, provoke neurogenesis in a mouse rapid electrical amygdala kindling model of seizures. Neuroscience 136: 405.
119. Snyder, J.S., Kee, N. and Wojtowicz, J.M., 2001, Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J. Neurophysiol. 85: 2423.
120. Song, H., Stevens, C.F. and Gage, F.H., 2002a, Astroglia induce neurogenesis from adult neural stem cells. Nature 417: 39.
121. Song, H.J., Stevens, C.F. and Gage, F.H., 2002b, Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat. Neurosci. 5: 438.
122. Steiner, B., Kronenberg, G., Jessberger, S., Brandt, M.D., Reuter, K. and Kempermann, G., 2004, Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46: 41.
123. Thom, M., Sisodiya, S.M., Beckett, A., Martinian, L., Lin, W.R., Harkness, W., Mitchell, T.N., Craig, J., Duncan, J. and Scaravilli, F., 2002, Cytoarchitectural abnormalities in hippocampal sclerosis. J. Neuropathol. Exp. Neurol. 61: 510.
124. Ueki, T., Tanaka, M., Yamashita, K., Mikawa, S., Qiu, Z., Maragakis, N.J., Hevner, R.F., Miura, N., Sugimura, H. and Sato, K., 2003, A novel secretory factor, Neurogenesin-1, provides neurogenic environmental cues for neural stem cells in the adult hippocampus. J. Neurosci. 23: 11732.
125. Ullian, E.M., Sapperstein, S.K., Christopherson, K.S. and Barres, B.A., 2001, Control of synapse number by glia. Science 291: 657.
126. Vallieres, L., Campbell, I.L., Gage, F.H. and Sawchenko, P.E., 2002, Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J. Neurosci. 22: 486.
127. van Praag, H., Schinder, A.F., Christie, B.R., Toni, N., Palmer, T.D. and Gage, F.H., 2002, Functional neurogenesis in the adult hippocampus. Nature 415: 1030.
128. Yoshimura, S., Takagi, Y., Harada, J., Teramoto, T., Thomas, S.S., Waeber, C., Bakowska, J.C., Breakefield, X.O. and Moskowitz, M.A., 2001, FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc. Natl Acad. Sci. USA 98: 5874.
129. Zhu, H., Dahlstrom, A. and Hansson, H.A., 2005, Characterization of cell proliferation in the adult dentate under normal conditions and after kainate induced seizures using ribonucleotide reductase and BrdU. Brain Res. 1036: 7.
130. Ziv, Y., Ron, N., Butovsky, O., Landa, G., Sudai, E., Greenberg, N., Cohen, H., Kipnis, J. and Schwartz, M., 2006, Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 9: 268.
131. Zucchini, S., Barbieri, M. and Simonato, M., 2005, Alterations in seizure susceptibility and in seizure-induced plasticity after pharmacologic and genetic manipulation of the fibroblast growth factor-2 system. Epilepsia 46 (Suppl. 5): 52