From Embryonic to Adult Neurogenesis in the Dentate Gyrus

  • Tatsunori Seki


Adult neurogenesis is now a very popular phenomenon in neuroscience. It is widely accepted that neurons continue to be generated in special regions of the adult brain such as the subventricular zone (SVZ) of the forebrain and the subgranular zone (SGZ) of the dentate granule cell layer. Adult neurogenesis, however, is not a special type of neurogenesis that occurs only in the adult stage, but is a part of the persistent neurogenesis that continues from embryonic to adult stages. Here, we describe the similarities and differences in the properties of progenitors and cellular architecture of proliferative zones from embryonic to adult periods and discuss the elements required for persistent neurogenesis.


Glial Fibrillary Acidic Protein Granule Cell Dentate Gyrus Neural Stem Cell Neural Cell Adhesion Molecule 
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.



I thank Dr. Takashi Namba for careful reading of the manuscript and valuable comments.


  1. Ahn, S and Joyner, A L (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437: 894–897CrossRefGoogle Scholar
  2. Alonso, G (2001) Proliferation of progenitor cells in the adult rat brain correlates with the presence of vimentin-expressing astrocytes. Glia 34: 253–266PubMedCrossRefGoogle Scholar
  3. Altman, J and Bayer, S A (1990a) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301: 365–381PubMedCrossRefGoogle Scholar
  4. Altman, J, and Bayer, S A (1990b) Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301: 325–342PubMedCrossRefGoogle Scholar
  5. Altman, J and Bayer, S A (1990c) Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale. J Comp Neurol 301: 343–364PubMedCrossRefGoogle Scholar
  6. Altman, J and Das, G D (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319–335PubMedCrossRefGoogle Scholar
  7. Alvarez-Buylla, A and Lim, D A (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41: 683–686PubMedCrossRefGoogle Scholar
  8. Alvarez-Buylla, A and Nottebohm, F (1988) Migration of young neurons in adult avian brain. Nature 335: 353–354CrossRefGoogle Scholar
  9. Andreu-Agullo, C, Morante-Redolat, J M, Delgado, A C et al (2009) Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone. Nat Neurosci 12: 1514–1523PubMedCrossRefGoogle Scholar
  10. Angevine, J B, Jr. (1965) Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp Neurol: Suppl 2: 1–70Google Scholar
  11. Bagri, A, Gurney, T, He, X et al (2002) The chemokine SDF1 regulates migration of dentate granule cells. Development 129: 4249–4260Google Scholar
  12. Barry, G, Piper, M, Lindwall, C et al (2008) Specific glial populations regulate hippocampal morphogenesis. J Neurosci 28: 12328–12340PubMedCrossRefGoogle Scholar
  13. Bayer, S A (1980) Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol 190: 87–114PubMedCrossRefGoogle Scholar
  14. Breunig, J J, Silbereis, J, Vaccarino, F M et al (2007) Notch regulates cell fate and dendrite morphology of newborn neurons in the postnatal dentate gyrus. Proc Natl Acad Sci USA 104: 20558–20563PubMedCrossRefGoogle Scholar
  15. Breunig, J J, Sarkisian, M R, Arellano, J I et al (2008) Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc Natl Acad Sci USA 105: 13127–13132PubMedCrossRefGoogle Scholar
  16. Cameron H A, Woolley C S, McEwen B S et al (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56: 337–344PubMedCrossRefGoogle Scholar
  17. Cao, L, Jiao, X, Zuzga, D S et al (2004) VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36: 827–835PubMedCrossRefGoogle Scholar
  18. Corish, P and Tyler-Smith, C (1999) Attenuation of green fluorescent protein half-life in mammalian cells. Protein Eng 12: 1035–1040PubMedCrossRefGoogle Scholar
  19. Dashtipour, K, Yan, X X, Dinh, T T et al (2002) Quantitative and morphological analysis of dentate granule cells with recurrent basal dendrites from normal and epileptic rats. Hippocampus 12: 235–244PubMedCrossRefGoogle Scholar
  20. Davis, E E, Brueckner, M and Katsanis, N (2006) The emerging complexity of the vertebrate cilium: new functional roles for an ancient organelle. Dev Cell 11: 9–19PubMedCrossRefGoogle Scholar
  21. Doetsch, F, Caille, I, Lim, D A et al (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703–716PubMedCrossRefGoogle Scholar
  22. Duan, X, Chang, J H, Ge, S et al (2007) Disrupted-in-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130: 1146–1158PubMedCrossRefGoogle Scholar
  23. Eckenhoff, M F and Rakic, P (1984) Radial organization of the hippocampal dentate gyrus: a Golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey. J Comp Neurol 223: 1–21PubMedCrossRefGoogle Scholar
  24. Enikolopov, G and Overstreet-Wadiche, L (2008) The use of reporter mouse lines to study adult neurogenesis. In: Gage, F. H. et al. (eds.), Adult neurogenesis. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  25. Enomoto, A, Asai, N, Namba, T et al (2009) Roles of disrupted-in-schizophrenia 1-interacting protein girdin in postnatal development of the dentate gyrus. Neuron 63: 774–787PubMedCrossRefGoogle Scholar
  26. Esposito, M S, Piatti, V C, Laplagne, D A et al (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25: 10074–10086PubMedCrossRefGoogle Scholar
  27. Ever, L and Gaiano, N (2005) Radial ‘glial’ progenitors: neurogenesis and signaling. Curr Opin Neurobiol 15: 29–33PubMedCrossRefGoogle Scholar
  28. Filippov, V, Kronenberg, G, Pivneva, T et al (2003) Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 23: 373–382PubMedCrossRefGoogle Scholar
  29. Forster, E, Tielsch, A, Saum, B et al (2002) Reelin, disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc Natl Acad Sci USA 99: 13178–13183PubMedCrossRefGoogle Scholar
  30. Forster, E, Jossin, Y, Zhao, S et al (2006) Recent progress in understanding the role of Reelin in radial neuronal migration, with specific emphasis on the dentate gyrus. Eur J Neurosci 23: 901–909PubMedCrossRefGoogle Scholar
  31. Fujita, S (2003) The discovery of the matrix cell, the identification of the multipotent neural stem cell and the development of the central nervous system. Cell Struct Funct 28: 205–228PubMedCrossRefGoogle Scholar
  32. Fukuda, S, Kato, F, Tozuka, Y et al (2003) Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 23: 9357–9366PubMedGoogle Scholar
  33. Gaiano, N and Fishell, G (2002) The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 25: 471–490PubMedCrossRefGoogle Scholar
  34. Galceran, J, Miyashita-Lin, E M, Devaney, E et al (2000) Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development 127: 469–482Google Scholar
  35. Galichet, C, Guillemot, F, Parras, C M (2008) Neurogenin 2 has an essential role in development of the dentate gyrus. Development 135: 2031–2041CrossRefGoogle Scholar
  36. Ganat, Y M, Silbereis, J, Cave, C et al (2006) Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J Neurosci 26: 8609–8621PubMedCrossRefGoogle Scholar
  37. Gao, Z, Ure, K, Ables, J L et al (2009) Neurod1 is essential for the survival and maturation of adult-born neurons. Nat Neurosci 12: 1090–1092PubMedCrossRefGoogle Scholar
  38. Garcia, A D, Doan, N B, Imura, T et al (2004) GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7: 1233–1241PubMedCrossRefGoogle Scholar
  39. Goldman, S A and Nottbohm, F (1983) Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA 80: 2390–2394PubMedCrossRefGoogle Scholar
  40. Gong, C, Wang, T W, Huang, H S et al (2007) Reelin regulates neuronal progenitor migration in intact and epileptic hippocampus. J Neurosci 27: 1803–1811PubMedCrossRefGoogle Scholar
  41. Gould, E and Gross, C G (2002) Neurogenesis in adult mammals: some progress and problems.J Neurosci 22: 619–623PubMedGoogle Scholar
  42. Gould, E, Cameron, H A, Daniels, D C et al (1992) Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12: 3642–3650PubMedGoogle Scholar
  43. Gross, C G (2000) Neurogenesis in the adult brain: death of a dogma. Nat Rev Neurosci 1: 67–73PubMedCrossRefGoogle Scholar
  44. Han, Y G, Spassky, N, Romaguera-Ros, M et al (2008) Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci 11: 277–284PubMedCrossRefGoogle Scholar
  45. Hartmann, D, Sievers, J, Pehlemann, F W et al (1992) Destruction of meningeal cells over the medial cerebral hemisphere of newborn hamsters prevents the formation of the infrapyramidal blade of the dentate gyrus. J Comp Neurol 320: 33–61PubMedCrossRefGoogle Scholar
  46. Hatanaka, Y and Murakami, F (2002) In vitro analysis of the origin, migratory behavior, and maturation of cortical pyramidal cells. J Comp Neurol 454: 1–14PubMedCrossRefGoogle Scholar
  47. Hebert, J M and Fishell, G (2008) The genetics of early telencephalon patterning: some assembly required. Nat Rev Neurosci 9: 678–685PubMedCrossRefGoogle Scholar
  48. Hebert, J M, Mishina, Y and McConnell, S K (2002) BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron 35: 1029–1041PubMedCrossRefGoogle Scholar
  49. Hodge, R D, Kowalczyk, T D, Wolf, S A et al (2008) Intermediate progenitors in adult hippocampal neurogenesis: Tbr2 expression and coordinate regulation of neuronal output. J Neurosci 28: 3707–3717PubMedCrossRefGoogle Scholar
  50. Hong, S M, Liu, Z, Fan, Y et al (2007) Reduced hippocampal neurogenesis and skill reaching performance in adult Emx1 mutant mice. Exp Neurol 206: 24–32PubMedCrossRefGoogle Scholar
  51. 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: 2824–2832PubMedGoogle Scholar
  52. Jacobson, M (1991) Developmental neurobiology. Plenum Press, New YorkCrossRefGoogle Scholar
  53. Jessberger, S, Toni, N, Clemenson, G D, Jr. et al (2008) Directed differentiation of hippocampal stem/progenitor cells in the adult brain. Nat Neurosci 11: 888–893PubMedCrossRefGoogle Scholar
  54. Johnson, M A, Ables, J L and Eisch, A J (2009) Cell-intrinsic signals that regulate adult neurogenesis in vivo: insights from inducible approaches. BMB Rep 42: 245–259PubMedCrossRefGoogle Scholar
  55. Jones, S P, Rahimi, O, O’Boyle, M P et al (2003) Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3. Hippocampus 13: 413–427PubMedCrossRefGoogle Scholar
  56. Kaplan, M S (2001) Environment complexity stimulates visual cortex neurogenesis: death of a dogma and a research career. Trends Neurosci 24: 617–620PubMedCrossRefGoogle Scholar
  57. Kaplan, M S and Hinds, J W (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197: 1092–1094PubMedCrossRefGoogle Scholar
  58. Kempermann, G (2006) Adult neurogenesis. Oxford University Press, New YorkGoogle Scholar
  59. Kempermann, G, Jessberger, S, Steiner, B et al (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27: 447–452PubMedCrossRefGoogle Scholar
  60. Kim, E J, Leung, C T, Reed, R R et al (2007) In vivo analysis of Ascl1 defined progenitors reveals distinct developmental dynamics during adult neurogenesis and gliogenesis. J Neurosci 27: 12764–12774PubMedCrossRefGoogle Scholar
  61. Kim, E J, Battiste, J, Nakagawa, Y et al (2008) Ascl1 (Mash1) lineage cells contribute to discrete cell populations in CNS architecture. Mol Cell Neurosci 38: 595–606PubMedCrossRefGoogle Scholar
  62. Kim, J Y, Duan, X, Liu, C Y et al (2009) DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron 63: 761–773PubMedCrossRefGoogle Scholar
  63. Kolodziej, A, Schulz, S, Guyon, A et al (2008) Tonic activation of CXC chemokine receptor 4 in immature granule cells supports neurogenesis in the adult dentate gyrus. J Neurosci 28: 4488–4500PubMedCrossRefGoogle Scholar
  64. Kriegstein, A and Alvarez-Buylla, A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32: 149–184PubMedCrossRefGoogle Scholar
  65. Kriegstein, A R and Noctor, S C (2004) Patterns of neuronal migration in the embryonic cortex. Trends Neurosci 27: 392–399PubMedCrossRefGoogle Scholar
  66. 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: 2027–2033PubMedGoogle Scholar
  67. Lai, K, Kaspar, B K, Gage, F H et al (2003) Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci 6: 21–27PubMedCrossRefGoogle Scholar
  68. Lathia, J D, Rao, M S, Mattson, M P et al (2007) The microenvironment of the embryonic neural stem cell: lessons from adult niches? Dev Dyn 236: 3267–3282PubMedCrossRefGoogle Scholar
  69. Laywell, E D, Rakic, P, Kukekov, V G et al (2000) Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA 97: 13883–13888PubMedCrossRefGoogle Scholar
  70. Lee, S M, Tole, S, Grove, E et al (2000) A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127: 457–467Google Scholar
  71. Li, G and Pleasure, S J (2005) Morphogenesis of the dentate gyrus: what we are learning from mouse mutants. Dev Neurosci 27: 93–99PubMedCrossRefGoogle Scholar
  72. Li, G and Pleasure, S J (2007) Genetic regulation of dentate gyrus morphogenesis. Prog Brain Res 163: 143–152PubMedCrossRefGoogle Scholar
  73. Li, G, Kataoka, H, Coughlin, S R et al (2009) Identification of a transient subpial neurogenic zone in the developing dentate gyrus and its regulation by Cxcl12 and reelin signaling. Development 136: 327–335CrossRefGoogle Scholar
  74. Lie, D C, Colamarino, S A, Song, H J et al (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437: 1370–1375CrossRefGoogle Scholar
  75. Liu, M, Pleasure, S J, Collins, A E et al (2000) Loss of BETA2/NeuroD leads to malformation of the dentate gyrus and epilepsy. Proc Natl Acad Sci USA 97: 865–870PubMedCrossRefGoogle Scholar
  76. Liu, Y, Namba, T, Liu, J et al (2010) Glial fibrillary acidic protein-expressing neural progenitors give rise to immature neurons via early intermediate progenitors expressing both glial fibrillary acidic protein and neuronal markers in the adult hippocampus. Neuroscience 166: 241–251PubMedCrossRefGoogle Scholar
  77. Lu, M, Grove, E A and Miller, R J (2002) Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc Natl Acad Sci USA 99: 7090–7095PubMedCrossRefGoogle Scholar
  78. Machold, R, Hayashi, S, Rutlin, M et al (2003) Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39: 937–950PubMedCrossRefGoogle Scholar
  79. Machon, O, van den Bout, C J, Backman, M et al (2003) Role of beta-catenin in the developing cortical and hippocampal neuroepithelium. Neuroscience 122: 129–143PubMedCrossRefGoogle Scholar
  80. Machon, O, Backman, M, Machonova, O et al (2007) A dynamic gradient of Wnt signaling controls initiation of neurogenesis in the mammalian cortex and cellular specification in the hippocampus. Dev Biol 311: 223–237PubMedCrossRefGoogle Scholar
  81. Madsen, T M, Newton, S S, Eaton, M E et al (2003) Chronic electroconvulsive seizure up-regulates beta-catenin expression in rat hippocampus: role in adult neurogenesis. Biol Psychiatry 54: 1006–1014PubMedCrossRefGoogle Scholar
  82. Malatesta, P, Hartfuss, E and Gotz, M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127: 5253–5263Google Scholar
  83. Mangale, V S, Hirokawa, K E, Satyaki, P R et al (2008) Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science 319: 304–309PubMedCrossRefGoogle Scholar
  84. Marin-Padilla, M (1998) Cajal-Retzius cells and the development of the neocortex. Trends Neurosci 21: 64–71PubMedCrossRefGoogle Scholar
  85. Martin, L A, Tan, S S and Goldowitz, D (2002) Clonal architecture of the mouse hippocampus. J Neurosci 22: 3520–3530PubMedGoogle Scholar
  86. Meyer, K D and Morris, J A (2009) Disc1 regulates granule cell migration in the developing hippocampus. Hum Mol Genet 18: 3286–3297PubMedCrossRefGoogle Scholar
  87. Miller, F D and Gauthier-Fisher, A (2009) Home at last: neural stem cell niches defined. Cell Stem Cell 4: 507–510PubMedCrossRefGoogle Scholar
  88. Miller, M W and Nowakowski, R S (1988) Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res 457: 44–52PubMedCrossRefGoogle Scholar
  89. Miyata, T, Maeda, T and Lee, J E (1999) NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev 13: 1647–1652PubMedCrossRefGoogle Scholar
  90. Miyata, T, Kawaguchi, A, Okano, H et al (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31: 727–741PubMedCrossRefGoogle Scholar
  91. Muller, M C, Osswald, M, Tinnes, S et al (2009) Exogenous reelin prevents granule cell dispersion in experimental epilepsy. Exp Neurol 216: 390–397PubMedCrossRefGoogle Scholar
  92. Nacher, J, Crespo, C and McEwen, B S (2001) Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14: 629–644PubMedCrossRefGoogle Scholar
  93. Nakahira, E and Yuasa, S (2005) Neuronal generation, migration, and differentiation in the mouse hippocampal primoridium as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation. J Comp Neurol 483: 329–340PubMedCrossRefGoogle Scholar
  94. Namba, T, Mochizuki, H, Onodera, M et al (2005) The fate of neural progenitor cells expres-sing astrocytic and radial glial markers in the postnatal rat dentate gyrus. Eur J Neurosci 22: 1928–1941PubMedCrossRefGoogle Scholar
  95. Namba, T, Namiki, H and Seki, T (2007) Direct evidence for neuronal differentiation of astrocyte-like progenitors in the postnatal hippocampus. Neurosci Res 58 Suppl 1: S209Google Scholar
  96. Nelson, W J and Nusse, R (2004) Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303: 1483–1487PubMedCrossRefGoogle Scholar
  97. Noctor, S C, Martinez-Cerdeno, V, Ivic, L et al (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7: 136–144PubMedCrossRefGoogle Scholar
  98. Noles, S R and Chenn, A (2007) Cadherin inhibition of beta-catenin signaling regulates the proliferation and differentiation of neural precursor cells. Mol Cell Neurosci 35: 549–558PubMedCrossRefGoogle Scholar
  99. O’Leary, D D and Sahara, S (2008) Genetic regulation of arealization of the neocortex. Curr Opin Neurobiol 18: 90–100PubMedCrossRefGoogle Scholar
  100. O’Leary, D D, Chou, S J and Sahara, S (2007) Area patterning of the mammalian cortex. Neuron 56: 252–269PubMedCrossRefGoogle Scholar
  101. Oldekamp, J, Kraemer, N, Alvarez-Bolado, G et al (2004) bHLH gene expression in the Emx2-deficient dentate gyrus reveals defective granule cells and absence of migrating precursors. Cereb Cortex 14: 1045–1058PubMedCrossRefGoogle Scholar
  102. Ozen, I, Galichet, C, Watts, C et al (2007) Proliferating neuronal progenitors in the postnatal hippocampus transiently express the proneural gene Ngn2. Eur J Neurosci 25: 2591–2603PubMedCrossRefGoogle Scholar
  103. Palmer, T D, Willhoite, A R and Gage, F H (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425: 479–494PubMedCrossRefGoogle Scholar
  104. Pellegrini, M, Mansouri, A, Simeone, A et al (1996) Dentate gyrus formation requires Emx2. Development 122: 3893–3898Google Scholar
  105. Rakic, P (1971) Guidance of neurons migrating to the fetal monkey neocortex. Brain Res 33: 471–476PubMedCrossRefGoogle Scholar
  106. Rakic, P (2003) Developmental and evolutionary adaptations of cortical radial glia. Cereb Cortex 13: 541–549PubMedCrossRefGoogle Scholar
  107. Rakic, P (2007) The radial edifice of cortical architecture: from neuronal silhouettes to genetic engineering. Brain Res Rev 55: 204–219PubMedCrossRefGoogle Scholar
  108. Ribak, C E, Korn, M J, Shan, Z et al (2004) Dendritic growth cones and recurrent basal dendrites are typical features of newly generated dentate granule cells in the adult hippocampus. Brain Res 1000: 195–199PubMedCrossRefGoogle Scholar
  109. 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: 449–479PubMedCrossRefGoogle Scholar
  110. Riquelme, P A, Drapeau, E and Doetsch, F (2008) Brain micro-ecologies: neural stem cell niches in the adult mammalian brain. Philos Trans R Soc Lond B Biol Sci 363: 123–137PubMedCrossRefGoogle Scholar
  111. Roelink, H (2000) Hippocampus formation: an intriguing collaboration. Curr Biol 10: R279–R281PubMedCrossRefGoogle Scholar
  112. Rousselot, P, Lois, C and Alvarez-Buylla, A D (1995) Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J Comp Neurol 351: 51–61PubMedCrossRefGoogle Scholar
  113. Salama-Cohen, P, Arevalo, M A, Grantyn, R et al (2006) Notch and NGF/p75NTR control dendrite morphology and the balance of excitatory/inhibitory synaptic input to hippocampal neurones through Neurogenin 3. J Neurochem 97: 1269–1278PubMedCrossRefGoogle Scholar
  114. 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: 149–175PubMedCrossRefGoogle Scholar
  115. Schwab, M H, Bartholomae, A, Heimrich, B et al (2000) Neuronal basic helix-loop-helix proteins (NEX and BETA2/Neuro D) regulate terminal granule cell differentiation in the hippocampus. J Neurosci 20: 3714–3724PubMedGoogle Scholar
  116. Schwartz, M L, Rakic, P and Goldman-Rakic, P S (1991) Early phenotype expression of cortical neurons: evidence that a subclass of migrating neurons have callosal axons. Proc Natl Acad Sci USA 88: 1354–1358PubMedCrossRefGoogle Scholar
  117. Seki, T (2002) Hippocampal adult neurogenesis occurs in a microenvironment provided by PSA-NCAM-expressing immature neurons. J Neurosci Res 69: 772–783PubMedCrossRefGoogle Scholar
  118. Seki, T (2003) Microenvironmental elements supporting adult hippocampal neurogenesis. Anat Sci Int 78: 69–78PubMedCrossRefGoogle Scholar
  119. Seki, T and Arai, Y (1991) The persistent expression of a highly polysialylated NCAM in the dentate gyrus of the adult rat. Neurosci Res 12: 503–513PubMedCrossRefGoogle Scholar
  120. Seki, T and Arai, Y (1993a) Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci Res 17: 265–290PubMedCrossRefGoogle Scholar
  121. Seki, T and Arai, Y (1993b) Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 13: 2351–2358PubMedGoogle Scholar
  122. Seki, T and Arai, Y (1995) Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 6: 2479–2482PubMedCrossRefGoogle Scholar
  123. 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: 503–513PubMedCrossRefGoogle Scholar
  124. Seki, T, Namba, T, Mochizuki, H et al (2007) Clustering, migration, and neurite formation of neural precursor cells in the adult rat hippocampus. J Comp Neurol 502: 275–290PubMedCrossRefGoogle Scholar
  125. Seki, T, Namba, T, Liu, Y et al (2009) How do GFAP-expressing neural progenitors divide and generate neuron-committed progeny in the postnatal hippocampus? Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience Program No. 506.14Google Scholar
  126. Seress, L and Mrzljak, L (1987) Basal dendrites of granule cells are normal features of the fetal and adult dentate gyrus of both monkey and human hippocampal formations. Brain Res 405: 169–174PubMedCrossRefGoogle Scholar
  127. Seri, B, Garcia-Verdugo, J M, McEwen, B S et al (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21: 7153–7160PubMedGoogle Scholar
  128. Seri, B, Garcia-Verdugo, J M, Collado-Morente, L et al (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478: 359–378PubMedCrossRefGoogle Scholar
  129. Shapiro, L A and Ribak, C E (2005) Integration of newly born dentate granule cells into adult brains: hypotheses based on normal and epileptic rodents. Brain Res Brain Res Rev 48: 43–56PubMedCrossRefGoogle Scholar
  130. Shapiro, L A, Korn, M J, Shan, Z et al (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: 81–91PubMedCrossRefGoogle Scholar
  131. Shihabuddin, L S, Horner, P J, Ray, J et al (2000) Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J Neurosci 20: 8727–8735PubMedGoogle Scholar
  132. Shimogori, T, VanSant, J, Paik, E et al (2004) Members of the Wnt, Fz, and Frp gene families expressed in postnatal mouse cerebral cortex. J Comp Neurol 473: 496–510PubMedCrossRefGoogle Scholar
  133. Shinozaki, K, Yoshida, M, Nakamura, M et al (2004) Emx1 and Emx2 cooperate in initial phase of archipallium development. Mech Dev 121: 475–489PubMedCrossRefGoogle Scholar
  134. Sibbe, M, Forster, E, Basak, O et al (2009) Reelin and Notch1 cooperate in the development of the dentate gyrus. J Neurosci 29: 8578–8585PubMedCrossRefGoogle Scholar
  135. Sievers, J, Hartmann, D, Pehlemann, F W et al (1992) Development of astroglial cells in the proliferative matrices, the granule cell layer, and the hippocampal fissure of the hamster dentate gyrus. J Comp Neurol 320: 1–32PubMedCrossRefGoogle Scholar
  136. Solberg, N, Machon, O and Krauss, S (2008) Effect of canonical Wnt inhibition in the neurogenic cortex, hippocampus, and premigratory dentate gyrus progenitor pool. Dev Dyn 237: 1799–1811PubMedCrossRefGoogle Scholar
  137. Song, H, Stevens, C F and Gage, F H (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417: 39–44CrossRefGoogle Scholar
  138. Spigelman, I, Yan, X X, Obenaus, A et al (1998) Dentate granule cells form novel basal dendrites in a rat model of temporal lobe epilepsy. Neuroscience 86: 109–120PubMedCrossRefGoogle Scholar
  139. Steiner, B, Kronenberg, G, Jessberger, S et al (2004) Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46: 41–52PubMedCrossRefGoogle Scholar
  140. Steiner, B, Klempin, F, Wang, L et al (2006) Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54: 805–814PubMedCrossRefGoogle Scholar
  141. Stensaas, L J (1967) The development of hippocampal and dorsolateral pallial region of the cerebral hemisphere in fetal rabbits. V. Sixty millimeter stage, glial cell morphology. J Comp Neurol 131: 423–436PubMedCrossRefGoogle Scholar
  142. Subramanian, L and Tole, S (2009) Mechanisms underlying the specification, positional regulation, and function of the cortical hem. Cereb Cortex 19 Suppl 1: i90–i95PubMedCrossRefGoogle Scholar
  143. Subramanian, L, Remedios, R, Shetty, A et al (2009) Signals from the edges: the cortical hem and antihem in telencephalic development. Semin Cell Dev Biol 20: 712–718PubMedCrossRefGoogle Scholar
  144. Suh, H, Deng, W and Gage, F H (2009) Signaling in adult neurogenesis. Annu Rev Cell Dev Biol 25: 253–275PubMedCrossRefGoogle Scholar
  145. Suhonen, J O, Peterson, D A, Ray, J et al (1996) Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383: 624–627CrossRefGoogle Scholar
  146. Suzuki, R, Watanabe, J, Arata, S et al (2003) A transgenic mouse model for the detailed morphological study of astrocytes. Neurosci Res 47: 451–454PubMedCrossRefGoogle Scholar
  147. Tabata, H and Nakajima, K (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 23: 9996–10001PubMedGoogle Scholar
  148. Tamamaki, N, Nakamura, K, Okamoto, K et al (2001) Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci Res 41: 51–60PubMedCrossRefGoogle Scholar
  149. Theil, T, Aydin, S, Koch, S et al (2002) Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon. Development 129: 3045–3054Google Scholar
  150. Tozuka, Y, Fukuda, S, Namba, T et al (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47: 803–815PubMedCrossRefGoogle Scholar
  151. van Praag, H, Schinder, A F, Christie, B R et al (2002) Functional neurogenesis in the adult hippocampus. Nature 415: 1030–1034CrossRefGoogle Scholar
  152. Verkhusha, V V, Kuznetsova, I M, Stepanenko, O V et al (2003) High stability of Discosoma DsRed as compared to Aequorea EGFP. Biochemistry 42: 7879–7884PubMedCrossRefGoogle Scholar
  153. Yamaguchi, M, Saito, H, Suzuki, M et al (2000) Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice [In Process Citation]. Neuroreport 11: 1991–1996PubMedCrossRefGoogle Scholar
  154. Yoshida, M, Suda, Y, Matsuo, I et al (1997) Emx1 and Emx2 functions in development of dorsal telencephalon. Development 124: 101–111Google Scholar
  155. Yuasa, S (2001) Development of astrocytes in the mouse hippocampus as tracked by tenascin-C gene expression. Arch Histol Cytol 64: 149–158PubMedCrossRefGoogle Scholar
  156. Zhao, C (2007) Retrovirus-mediated cell labeling. In: Gage, F. H. et al. (eds.), Adult neurogenesis. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  157. Zhao, T, Kraemer, N, Oldekamp, J et al (2006) Emx2 in the developing hippocampal fissure region. Eur J Neurosci 23: 2895–2907PubMedCrossRefGoogle Scholar
  158. Zhou, C J, Zhao, C and Pleasure, S J (2004) Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding abnormalities. J Neurosci 24: 121–126PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  1. 1.Department of Histology and NeuroanatomyTokyo Medical UniversityTokyoJapan

Personalised recommendations