Glia and Hippocampal Neurogenesis in the Normal, Aged and Epileptic Brain

  • William P. Gray
  • Alexandra Laskowski

In this chapter, we review the role of glial cells in hippocampal neurogenesis under normal conditions, in aging and in the epileptic brain. Astrocytes or astrocyte-like cells are emerging as key components of the neurogenic niche in health and disease, with roles ranging from being stem cells to regulating almost all aspects of neurogenesis and synaptic integration of the newly generated neurons. It is likely that astrocytes and microglial cells are key sensors of local environmental changes, modulating neurogenesis appropriately. This is likely to be a fruitful area of research for extending our understanding of the role of stem cells in the normal and diseased brain.


Granule Cell Dentate Gyrus Neural Stem Cell Temporal Lobe Epilepsy Adult Neurogenesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

8. References

  1. Abrous, D.N., Koehl, M. and Le Moal, M., 2005, Adult neurogenesis: from precursors to network and physiology. Physiol. Rev. 85: 523.PubMedGoogle Scholar
  2. Altman, J. and Bayer, S.A., 1990, Migration and distribution of two populations of hippocampal granule cell precur-sors during the perinatal and postnatal periods. J. Comp. Neurol. 301: 365.PubMedGoogle Scholar
  3. Altman, J. and Das, G.D., 1965, Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124: 319.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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 tempo-ral lobe epilepsy. Hippocampus 11: 311.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  14. Buniatian, G., Traub, P., Albinus, M., Beckers, G., Buchmann, A., Gebhardt, R. and Osswald, H., 1998, The immu-noreactivity 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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  16. Butovsky, O., Talpalar, A.E., Ben-Yaakov, K. and Schwartz, M., 2005, Activation of microglia by aggregated beta-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-gamma and IL-4 render them protective. Mol. Cell Neurosci. 29: 381.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  18. Cameron, H.A. and Gould, E., 1994, Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuro-science 61: 203.Google Scholar
  19. Cameron, H.A. and McKay, R.D., 1999, Restoring production of hippocampal neurons in old age. Nat. Neurosci. 2: 894.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  23. Cocchia, D., 1981, Immunocytochemical localization of S-100 protein in the brain of adult rat. An ultrastructural study. Cell Tissue Res. 214: 529.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  26. D’Sa, C. and Duman, R.S., 2002, Antidepressants and neuroplasticity. Bipolar Disord. 4: 183.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  28. Doetsch, F., Caille, I., Lim, D.A., Garcia-Verdugo, J.M. and Alvarez-Buylla, A., 1999, Subventricular zone astro-cytes are neural stem cells in the adult mammalian brain. Cell 97: 703.PubMedGoogle Scholar
  29. Drapeau, E., Mayo, W., Aurousseau, C., Le Moal, M., Piazza, P.V. and Abrous, D.N., 2003, Spatial memory per-formances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl Acad. Sci. USA 100: 14385.PubMedGoogle Scholar
  30. Eichenbaum, H., 1997, Declarative memory: insights from cognitive neurobiology. Annu. Rev. Psychol. 48: 547.PubMedGoogle Scholar
  31. Ekdahl, C.T., Claasen, J.H., Bonde, S., Kokaia, Z. and Lindvall, O., 2003, Inflammation is detrimental for neuro-genesis in adult brain. Proc. Natl Acad. Sci. USA 100: 13632.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  36. Fukuda, S., Kato, F., Tozuka, Y., Yamaguchi, M., Miyamoto, Y. and Hisatsune, T., 2003, Two distinct subpopula-tions of nestin-positive cells in adult mouse dentate gyrus. J. Neurosci. 23: 9357.PubMedGoogle Scholar
  37. Gage, F.H., 2002, Neurogenesis in the adult brain. J. Neurosci. 22: 612.PubMedGoogle Scholar
  38. Gaiano, N. and Fishell, G., 2002, The role of notch in promoting glial and neural stem cell fates. Annu. Rev. Neuro-sci. 25: 471.Google Scholar
  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 hip-pocampus. Aging Cell 3: 363.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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 neuro-genesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J. Neurosci. 26: 4701.PubMedGoogle Scholar
  49. Hinterkeuser, S., Gray, W., Hager, G., Sundstrom, L. and Steinhauser, C., 1999, Characterization of astrocytic prolif-eration in rat dentate gyrus. J. Neurochem. 73: S70.Google Scholar
  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.PubMedGoogle Scholar
  51. Houser, C.R., 1990, Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res. 535: 195.PubMedGoogle Scholar
  52. Howell, O.W., Scharfman, H.E., Herzog, H., Sundstrom, L.E., Beck-Sickinger, A. and Gray, W.P., 2003, Neuropep-tide Y is neuroproliferative for post-natal hippocampal precursor cells. J. Neurochem. 86: 646.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  58. Jin, K., Sun, Y., Xie, L., Batteur, S., Mao, X.O., Smelick, C., Logvinova, A. and Greenberg, D.A., 2003, Neurogene-sis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2: 175.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  62. Kempermann, G., Jessberger, S., Steiner, B. and Kronenberg, G., 2004, Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27: 447.PubMedGoogle Scholar
  63. Kipnis, J. and Schwartz, M., 2005, Controlled autoimmunity in CNS maintenance and repair: naturally occurring CD4+CD25+ regulatory T-Cells at the crossroads of health and disease. Neuromol. Med. 7: 197.Google Scholar
  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. PubMedGoogle Scholar
  65. Kuhn, H.G., Dickinson-Anson, H. and Gage, F.H., 1996, Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16: 2027.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  77. Malberg, J.E., Eisch, A.J., Nestler, E.J. and Duman, R.S., 2000, Chronic antidepressant treatment increases neuro-genesis in adult rat hippocampus. J. Neurosci. 20: 9104.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  81. McDonald, H.Y. and Wojtowicz, J.M., 2005, Dynamics of neurogenesis in the dentate gyrus of adult rats. Neurosci. Lett. 385: 70.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  83. Monje, M.L., Toda, H. and Palmer, T.D., 2003, Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  86. Nakagawa, E., Aimi, Y., Yasuhara, O., Tooyama, I., Shimada, M., McGeer, P.L. and Kimura, H., 2000, Enhance-ment of progenitor cell division in the dentate gyrus triggered by initial limbic seizures in rat models of epi-lepsy. Epilepsia 41: 10.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  90. O’Kusky, J.R., Ye, P. and D’Ercole, A.J., 2000, Insulin-like growth factor-I promotes neurogenesis and synapto-genesis in the hippocampal dentate gyrus during postnatal development. J. Neurosci. 20: 8435.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  92. Parent, J.M., 2002, The role of seizure-induced neurogenesis in epileptogenesis and brain repair. Epilepsy Res. 50: 179.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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 matura-tion. Eur. J. Neurosci. 21: 464.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  103. Sadgrove, M.P., Chad, J.E. and Gray, W.P., 2005, Kainic acid induces rapid cell death followed by transiently re-duced cell proliferation in the immature granule cell layer of rat organotypic hippocampal slice cultures. Brain Res. 1035: 111.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  105. Scharfman, H.E. and Gray, W.P., 2006, Plasticity of neuropeptide Y in the dentate gyrus after seizures, and its rele-vance to seizure-induced neurogenesis. EXS 193.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.Google Scholar
  109. Schwartz, M., Butovsky, O., Bruck, W. and Hanisch, U.K., 2006, Microglial phenotype: is the commitment reversi-ble? Trends Neurosci. 29: 68.PubMedGoogle Scholar
  110. Seki, T. and Arai, Y., 1995, Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 6: 2479.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  115. Shors, T.J., 2004, Memory traces of trace memories: neurogenesis, synaptogenesis and awareness. Trends Neurosci. 27: 250.PubMedGoogle Scholar
  116. Shors, T.J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T. and Gould, E., 2001, Neurogenesis in the adult is in-volved in the formation of trace memories. Nature 410: 372.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  119. Snyder, J.S., Kee, N. and Wojtowicz, J.M., 2001, Effects of adult neurogenesis on synaptic plasticity in the rat den-tate gyrus. J. Neurophysiol. 85: 2423.PubMedGoogle Scholar
  120. Song, H., Stevens, C.F. and Gage, F.H., 2002a, Astroglia induce neurogenesis from adult neural stem cells. Nature 417: 39.PubMedGoogle Scholar
  121. Song, H.J., Stevens, C.F. and Gage, F.H., 2002b, Neural stem cells from adult hippocampus develop essential prop-erties of functional CNS neurons. Nat. Neurosci. 5: 438.PubMedGoogle Scholar
  122. Steiner, B., Kronenberg, G., Jessberger, S., Brandt, M.D., Reuter, K. and Kempermann, G., 2004, Differential regula-tion of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46: 41.PubMedGoogle Scholar
  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. Neu-rol. 61: 510.Google Scholar
  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.PubMedGoogle Scholar
  125. Ullian, E.M., Sapperstein, S.K., Christopherson, K.S. and Barres, B.A., 2001, Control of synapse number by glia. Science 291: 657.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  131. Zucchini, S., Barbieri, M. and Simonato, M., 2005, Alterations in seizure susceptibility and in seizure-induced plas-ticity after pharmacologic and genetic manipulation of the fibroblast growth factor-2 system. Epilepsia 46 (Suppl. 5): 52.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • William P. Gray
    • 1
  • Alexandra Laskowski
    • 1
  1. 1.Division of Clinical NeurosciencesUniversity of SouthamptonBassett Crescent EastUK

Personalised recommendations