Offer and demand: Proliferation and survival of neurons in the dentate gyrus

European Journal of Neuroscience

Volumn 21, Issue 12, 2005, Pages 3205-3216

  Lehmann, Konrad ^a   Butz, Markus ^a   Teuchert Noodt, Gertraud ^a  

^a BIELEFELD UNIVERSITY   (Germany)

Author keywords

Artificial neuronal network; Cell survival; Hippocampus; Neuronal homeostasis

Indexed keywords

APOPTOSIS; CELL PROLIFERATION; CELL SURVIVAL; DENTATE GYRUS; HIPPOCAMPUS; NERVE CELL; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; BLOOD CIRCULATION; CELL PROLIFERATION; CELL SURVIVAL; DENTATE GYRUS; GROWTH SUBSTANCES; HORMONES; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; NEUROTRANSMITTER AGENTS;

EID: 21844442859     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04156.x     Document Type: Review

References (199)

1. Aberg, M.A., Aberg, N.D., Hedbacker, H., Oscarsson, J. & Eriksson, P.S. (2000) Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J. Neurosci., 20, 2896-2903.
2. Aberg, M.A., Aberg, N.D., Palmer, T.D., Alborn, A.M., Carlsson-Skwirut, C., Bang, P., Rosengren, L.E., Olsson, T., Gage, F.H. & Eriksson, P.S. (2003) IGF-I has a direct proliferative effect in adult hippocampal progenitor cells. Mol. Cel. Neurosci., 24, 23-40.
3. Altman, J. & Das, G.D. (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol., 124, 319-335.
4. Azmitia, E. (2001) Modern views on an ancient chemical: serotonin effects on cell proliferation, maturation, and apoptosis. Brain Res. Bull., 56, 413-424.
5. Bai, F., Bergeron, M. & Nelson, D.L. (2003) Chronic AMPA receptor potentiator (LY451646) treatment increases cell proliferation in adult rat hippocampus. Neuropharmacol., 44, 1013-1021.
6. Bengzon, J., Kokaia, Z., Elmer, E., Nanobashvili, A., Kokaia, M. & Lindvall, O. (1997) Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Natl Acad. Sci. USA, 94, 10432-10437.
7. Ben-Yaakov, G. & Golan, H. (2003) Cell proliferation in response to GABA in postnatal hippocampal slice culture. Int. J. Dev. Neurosci., 21, 153-157.
8. Bernabeu, R. & Sharp, F.R. (2000) NMDA and AMPA/kainate glutamate receptors modulate dentate neurogenesis and CA3 synapsin-I in normal and ischemic hippocampus. J. Cereb. Blood Flow Metab., 20, 1669-1680.
9. Biebl, M., Cooper, C.M., Winkler, J. & Kuhn, H.G. (2000) Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci. Lett., 291, 17-20.
10. Blümcke, I., Schewe, J.C., Normann, S., Brüstle, O., Schramm, J., Elger, C.E. & Wiestier, 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, 311-321.
11. Bode-Greuel, K.M., Klisch, J., Horvath, E., Glaser, T. & Traber, J. (1990) Effects of 5-hydroxytryptamine1A-receptor agonists on hippocampal damage after transient forebrain ischemia in the Mongolian gerbil. Stroke, 21 (12 Suppl.), IV164-166.
12. Bredy, T.M., Grant, R.J., Champagne, D.L. & Meaney, M.J. (2003) Maternal care influences neuronal survival in the hippocampus of the rat. Eur. J. Neurosci., 18, 2903-2909.
13. Bremner, J.D. & Vermetten, E. (2004) Neuroanatomical changes associated with pharmacotherapy in posttraumatic stress disorder. Ann. NY Acad. Sci., 1032, 154-157.
14. Brezun, J.M. & Daszuta, A. (1999) Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience, 89, 999-1002.
15. Brezun, J.M. & Daszuta, A. (2000a) Serotonergic reinnervation reverses lesion-induced decreases in PSA-NCAM labeling and proliferation of hippocampal cells in adult rats. Hippocampus, 10, 37-46.
16. Brezun, J.M. & Daszuta, A. (2000b) Serotonin may stimulate granule cell proliferation in the adult hippocampus, as observed in rats grafted with foetal raphe neurons. Eur. J. Neurosci., 12, 391-396.
17. Brown, J., Cooper-Kuhn, C.M., Kempermann, G., van Praag, H., Winkler, J., Gage, F.H. & Kuhn, H.G. (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci., 17, 2042-2046.
18. Bruel-Jungerman, E., Laroche, S. & Rampon, C. (2005) New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur. J. Neurosci., 21, 513-521.
19. Busche, A., Bagorda, A., Lehmann, K., Neddens, J. & Teuchert-Noodt, G. (2005) The maturation of the acetylcholine system in the dentate gyrus of gerbils (Meriones unguiculatus) is affected by epigenetic factors. J. Neural Transm., in press.
20. Busche, A., Neddens, J., Dinter, C., Dawirs, R.R. & Teuchert-Noodt, G. (2002) Differential influence of rearing conditions and methamphetamine on serotonin fibre maturation in the dentate gyrus of gerbils (Meriones unguiculatus). Dev. Neurosci., 24, 512-521.
21. Buzsaki, G., Grastyan, E., Czopf, J., Kellenyi, L. & Prohaska, O. (1981) Changes in neuronal transmission in the rat hippocampus during behavior. Brain Res., 225, 235-247.
22. Calzà, L., Giuliani, A., Fernandez, M., Pirondi, S., D'Intino, G., Aloe, L. & Giardino, L. (2003) Neural stem cells and cholinergic neurons: regulation by immunolesion and treatment with mitogens, retinoic acid, and nerve growth factor. PNAS, 100, 7325-7330.
23. Cameron, H.A. & Gould, E. (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience, 66, 247-252.
24. Cameron, H.A. & Gould, E. (1996) Distinct populations of cells in the adult dentate gyrus undergo mitosis or apoptosis in response to adrenalectomy. J. Comp. Neurol., 369, 56-63.
25. Cameron, H.A., McEwen, B.S. & Gould, E. (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J. Neurosci., 15, 4687-4692.
26. Cameron, H.A., Tanapat, P. & 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, 349-354.
27. Cameron, H.A., Woolley, C.S., McEwen, B.S. & Gould, E. (1993) Differentiation of newly-born neurons and glia in the dentate gyrus of the adult rat. Neuroscience, 56, 337-344.
28. Cao, L., Jiao, X., Zuzga, D.S., Liu, Y., Fong, D.M., Young, D. & During, M.J. (2004) VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet., 36, 827-835.
29. Carlén, M., Cassidy, R.M., Brisman, H., Smith, G.A., Enquist, L.W. & Frisén, J. (2002) Functional integration of adult-born neurons. Curr. Biol., 12, 606-608.
30. Cecchi, G.A., Petreanu, L.T., Alvarez-Buylla, A. & Magnasco, M.O. (2001) Unsupervised learning and adaptation in a model of adult neurogenesis. J. Comput. Neurosci., 11, 175-182.
31. Chambers, R.A., Potenza, M.N., Hoffman, R.E. & Miranker, W. (2004) Simulated apoptosis/neurogenesis regulates learning and memory capabilities of adaptive neural networks. Neuropsychopharmacology, 29, 747-758.
32. Chen, B., Dowlatshahi, D., MacQueen, G.M., Wang, J. & Young, L.T. (2001) Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication. Biol. Psychiat., 50, 260-265.
33. Chen, G., Du Rajkowska, G.F., Seraji-Bozorgzad, N. & Manji, H.K. (2000) Enhancement of hippocampal neurogenesis by lithium. J. Neurochem., 75, 1729-1734.
34. Cheng, Y., Black, I.B. & DiCicco-Bloom, E. (2002) Hippocampal granule neuron production and population size are regulated by levels of bFGF. Eur. J. Neurosci., 15, 3-12.
35. Clarke, P.G.H. (1985) Neuronal deatch in the development of the vertebrate nervous system. Trends Neurosci., 8, 345-349.
36. Clement, H.W., Kirsch, M., Hasse, C., Opper, C., Gemsa, D. & Wesemann, W. (1998) Effect of repeated immobilization on serotonin metabolism in different rat brain areas and on serum corticosterone. J. Neural Transm., 105, 1155-1170.
37. Coe, C.L., Kramer, M., Czeh, B., Gould, E., Reeves, A.J., Kirschbaum, C. & Fuchs, E. (2003) Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol. Psychiat., 54, 1025-1034.
38. Cohen, Z., Ehret, M., Maitre, M. & Hamel, E. (1995) Ultrastructural analysis of tryptophan hydroxylase immunoreactive nerve terminals in the rat cerebral cortex and hippocampus: their association with blood vessels. Neuroscience, 66, 555-569.
39. Cooper-Kuhn, C.M., Winkler, J. & Kuhn, H.G. (2004) Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J. Neurosci. Res., 77, 155-165.
40. Cowan, W.M., Fawcett, J.W., O'Leary, D.D.M. & Stanfield, B.B. (1984) Regressive events in neurogenesis. Science, 225, 1258-1265.
41. Dames, W., Joó, F., Fehér, J., Toldi, J. & Wolff, J.R. (1985) Gamma-aminobutyric acid enables synaptogenesis in the intact superior cervical ganglion of the adult rat. Neurosci. Lett., 54, 159-164.
42. Dammasch, I.E. (1989) Structural realization of a Hebb-type learning rule. In Cotterill, R.M.J. (ed.), Models of Brain Function. CUP, Cambridge, pp. 539-552.
43. Dammasch, I.E. & Wagner, G.P. (1984) On the properties of randomly connected McCulloch-Pitts networks: differences between input-constant and input-variant networks. Cybern. Syst., 15, 91-117.
44. Dammasch, I.E., Wagner, G.P. & Wolff, J.R. (1986) Self-stabilization of neuronal networks. Biol. Cybern., 54, 211-222.
45. Dawirs, R.R., Hildebrandt, K. & Teuchert-Noodt, G. (1998) Adult treatment with haloperidol increases dentate gyrus cell proliferation in the gerbil hippocampus. J. Neural Transm., 105, 317-327.
46. Dawirs, R.R., Teuchert-Noodt, G., Hildebrandt, K. & Fei, F. (2000) Granule cell proliferation and axon terminal degradation in the dentate gyrus of gerbils (Meriones unguiculatus) during maturation, adulthood and aging. J. Neural. Transm., 107, 639-647.
47. Dawirs, R.R., Teuchert-Noodt, G. & Kacza, J. (1992) Naturally occurring degrading events in axon terminals of the dentate gyrus and stratum lucidum in the spiny mouse (Acomys cahirinus) during maturation, adulthood and aging. Dev. Neurosci., 14, 210-220.
48. Dayer, A.G., Ford, A.A., Cleaver, K.M., Yassaee, M. & Cameron, H.A. (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J. Comp. Neurol., 460, 563-572.
49. De Kloet, E.R., Kovacs, G.L., Szabo, G., Telegdy, B., Bohus, B. & Versteeg, D.H. (1982) Decreased serotonin turnover in the dorsal hippocampus of rat brain shortly after adrenalectomy: selective normalization after corticosterone substitution. Brain Res., 239, 659-663.
50. Deisseroth, K., Singla, S., Toda, H., Monje, M., Palmer, T.D. & Malenka, R.C. (2004) Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron, 42, 535-552.
51. Derrick, B.E., York, A.D. & Martinez, J.E. Jr (2000) Increased granule cell neurogenesis in the adult dentate gyrus following mossy fiber stimulation sufficient to induce long-term potentiation. Brain Res., 857, 300-307.
52. Dias Soares, D., Fernández, F., Aguerre, S., Foury, A., MormPde, P. & Chaouloff, F. (2003) Fox odour affects corticosterone release but not hippocampal serotonin reuptake and open field behaviour in rats. Brain Res., 961, 166-170.
53. Doetsch, F., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci., 17, 5046-5061.
54. Drapeau, E., Mayo, W., Aurousseau, C., Le Moal, M., Piazza, P.V. & 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, 14385-14390.
55. Dringenberg, H.C. & Vanderwolf, C.H. (1997) Neocortical activation: modulation by multiple pathways acting on central cholinergic and serotonergic systems. Exp. Brain Res., 116, 160-174.
56. Dringenberg, H.C. & Vanderwolf, C.H. (1998) Involvement of direct and indirect pathways in electrocorticographic activation. Neurosci. Biobehav. Rev., 22, 243-257.
57. Eisch, A.J., Barrot, M., Schad, C.A., Self, D.W. & Nestler, E.J. (2000) Opiates inhibit neurogenesis in the adult rat hippocampus. Proc. Natl. Acad. Sci. USA, 97, 7579-7584.
58. Fabel, K., Fabel, K., Tam, B., Kaufer, D., Baiker, A., Simmons, N., Kuo, C.J. & Palmer, T.D. (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur. J. Neurosci., 18, 2803-2812.
59. Farisse, J., Boulenguez, P., Semont, A., Hery, F., Barden, N., Faudon, M. & Hery, M. (1999) Regional serotonin metabolism under basal and restraint stress conditions in the brain of transgenic mice with impaired glucocorticoid receptor function. Neuroendocrinol., 70, 413-421.
60. Farmer, J., Zhao, X., van Praag, H., Wodtke, K., Gage, F.H. & Christie, B.R. (2004) Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience, 124, 71-79.
61. Feng, R., Rampon, C., Tang, Y.P., Shrom, D., Jin, J., Kyin, M., Sopher, B., Miller, M.W., Ware, C.B., Martin, G.M., Kim, S.H., Langdon, R.B., Sisodia, S.S. & Tsien, J.Z. (2001) Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron, 32, 911-926.
62. Ferland, R.J., Gross, R.A. & Applegate, C.D. (2002) Increased mitotic activity in the dentate gyrus of the hippocampus of adult C57BL/6J mice exposed to the flurothyl kindling model of epileptogenesis. Neuroscience, 115, 669-683.
63. Foster, T.C. & Deadwyler, S.A. (1992) Acetylcholine modulates averaged sensory evoked responses and perforant path evoked field potentials in the rat dentate gyrus. Brain Res., 587, 95-101.
64. Gage, F.H. (2002) Neurogenesis in the adult brain. J. Neurosci., 22, 612-613.
65. Galea, L.A.M., Tanapat, P. & Gould, E. (1996) Exposure to predator odor suppresses cell proliferation in the dentate gyrus of adult rats via a cholinergic mechanism. Soc. Neurosci. Abstr., 22, 1196.
66. Gasbarri, A., Sulli, A. & Packard, M.G. (1997) The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog. Neuro-Psychopharmacol. Biol. Psychiat., 21, 1-22.
67. Gibbs, R.B. (2002) Basal forebrain cholinergic neurons are necessary for estrogen to enhance acquisition of a delayed matching-to-position T-maze task. Horm. Behav., 42, 245-257.
68. Gould, E. (1999) Serotonin and hippocampal neurogenesis. Neuropsychopharmacology, 21, 46S-51S.
69. Gould, E., Cameron, H.A., Daniels, D.C., Woolley, C.S. & McEwen, B.S. (1992) Adrenal hormones suppress cell division in the adult rat dentate gyrus. J. Neurosci., 12, 3642-3650.
70. Gould, E. & Gross, C.G. (2002) Neurogenesis in adult mammals: some progress and problems. J. Neurosci., 22, 619-623.
71. Gould, E., McEwen, B.S., Tanapat, P., Galea, L.A.M. & 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, 2492-2498.
72. Gould, E., Tanapat, P., Hastings, N.B. & Shors, T.J. (1999) Neurogenesis in adulthood: a possible role in learning. Trends Cogn. Sci., 3, 186-192.
73. Gould, E., Woolley, C.S. & McEwen, B.S. (1991) Naturally occurring cell death in the developing dentate gyrus of the rat. J. Comp. Neurol., 304, 408-418.
74. Green, E.J. & Greenough, W.T. (1986) Altered synaptic transmission in dentate gyrus of rats reared in complex environments: Evidence from hippocampal slices maintained in vitro. J. Neurophysiol., 55, 739-750.
75. Greenough, W.T., Cohen, N.J. & Juraska, J.M. (1999) New neurons in old brains: learning to survive?. Nat. Neurosci., 2, 203-205.
76. Grutzendler, J., Kasthuri, N. & Gan, W.-B. (2002) Long-term dendritic spine stability in the adult cortex. Nature, 420, 812-816.
77. Gu, Q. (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience, 111, 815-835.
78. Guidi, S., Ciani, E., Seven, S., Contestabile, A. & Bartesaghi, R. (2005) Postnatal neurogenesis in the dentate gyrus of the guinea pig. Hippocampus, 15, 285-301.
79. Guzmán-Marín, R., Suntsova, N., Stewart, D.R., Gong, H., Szymusiak, R. & McGinty, D. (2003) Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats. J. Physiol. (Lond), 549, 563-571.
80. Halim, N.D., Weickert, C.S., McClintock, B.W., Weinberger, D.R. & Lipska, B.K. (2004) Effects of chronic haloperidol and clozapine treatment on neurogenesis in the adult rat hippocampus. Neuropsychopharmacology, 29, 1063-1069.
81. Hamburger, V. & Levi-Montalcini, R. (1949) Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions. J. Exp. Zool., 111, 457-501.
82. Hamel, E. (2004) Cholinergic modulation of the cortical microvascular bed. Prog. Brain Res., 145, 171-178.
83. Harzsch, S., Miller, J., Benton, J. & Beltz, B. (1999) From embryo to adult: persistent neurogenesis and apoptotic cell death shape the developing crustacean deutocerebrum. J. Neurosci., 19, 3472-3485.
84. Hastings, N.B., Seth, M.I., Tanapat, P., Rydel, T.A. & Gould, E. (2002) Granule neurons generated during development extend divergent axon collaterals to hippocampal area CA3. J. Comp. Neurol., 452, 324-333.
85. Heikkinen, T., Puolivali, J., Liu, L., Rissanen, A. & Tanila, H. (2002) Effects of ovariectomy and estrogen treatment on learning and hippocampal neurotransmitters in mice. Horm. Behav., 41, 22-32.
86. Heine, V.M., Maslam, S., Joels, M. & Lucassen, P.J. (2004a) Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol. Aging, 25, 361-375.
87. Heine, V.M., Maslam, S., Zareno, J., Joels, M. & Lucassen, P.J. (2004b) Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur. J. Neurosci., 19, 131-144.
88. Hildebrandt, K. (1999) Zur Modulation Neuroplastischer Prozesse im Hippocampus durch Umweltparameter und Neuroaktive Substanzen: Quantitative Analysen zur Körnerzellproliferation im Gehirn der Adulten Maus. PhD Thesis, Bielefeld University, Bielefeld, Germany.
89. Hildebrandt, K., Teuchert-Noodt, G. & Dawirs, R.R. (1999) A single neonatal dose of methamphetamine suppresses dentate granule cell proliferation in adult gerbils which is restored to control values by acute doses of haloperidol. J. Neural. Transm., 106, 549-558.
90. Hodges, H., Katzung, N., Sowinski, P., Hopewell, J.W., Wilkinson, J.H., Bywaters, T. & Rezvani, M. (1998) Late behavioural and neuropathological effects of local brain irradiation in the rat. Behav. Brain Res., 91, 99-114.
91. Hoffmann, K., Bagorda, F., Stevenson, A.F.G. & Teuchert-Noodt, G. (2001) Electromagnetic field exposure effects the hippocampal dentate cell proliferation in gerbils (Meriones unguiculatus). Ind. J. Exp. Biol., 39, 1220-1226.
92. Hollyday, M. & Hamburger, V. (1976) Reduction of the naturally occurring motor neuron loss by enlargement of the periphery. J. Comp. Neurol., 170, 311-320.
93. Holmes, M.M., Galea, L.A., Mistlberger, R.E. & Kempermann, G. (2004) Adult hippocampal neuogenesis and voluntary running activity: circadian and dose-dependent effects. J. Neurosci. Res., 76, 216-222.
94. Horner, P.J. & Palmer, T.D. (2003) New roles for astrocytes: The nightlife of an 'astrocyte'. La vida loca! Trends Neurosci., 26, 597-603.
95. Isaacs, K.R., Anderson, B.J., Alcantara, A.A., Black, J.E. & Greenough, W.T (1992) Exercise and the brain: angiogenesis in the adult rat cerebellum after vigorous physical activity and motor skill learning. J. Cereb. Blood Flow Metab., 12, 110-119.
96. Jacobs, B.L., Tanapat, P., Reeves, A.J. & Gould, E. (1998) Serotonin stimulates the production of new hippocampal granule neurons via the 5-HT1A receptor in the adult rat. Soc. Neurosci. Abstr., 24, 1992.
97. Jang, M.H., Shin, M.C., Jung, S.B., Lee, T.H., Bahn, G.H., Kwon, Y.K., Kim, E.H. & Kim, C.J. (2002) Alcohol and nicotine reduce cell proliferation and enhance apoptosis in dentate gyrus. Neuroreport, 13, 1509-1513.
98. Jessberger, S. & Kempermann, G. (2003) Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur. J. Neurosci., 18, 2707-2712.
99. Jin, K., Peel, A.L., Mao, X.O., Xie, L., Cottrell, B.A., Henshall, D.C. & Greenberg, D.A. (2004) Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl Acad. Sci. USA, 101, 343-347.
100. Jin, K., Sun, Y., Xie, L., Batteur, S., Mao, X.O., Smelick, C., Logvinova, A. & 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, 175-183.
101. Kao, T.Y. & Lin, M.T. (1996) Brain serotonin depletion attenuates heatstroke-induced cerebral ischemia and cell death in rats. J. Appl. Physiol., 80, 680-684.
102. Kaplan, M.S. & Bell, D.H. (1984) Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J. Neurosci., 4, 1429-1441.
103. Kaplan, M.S. & Hinds, J.W. (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science, 197, 1092-1094.
104. Karst, H. & Joels, M. (2001) Calcium currents in rat dentate granule cells are altered after adrenalectomy. Eur. J. Neurosci., 14, 503-512.
105. Katoh-Semba, R., Asano, T., Ueda, H., Morishita, R., Takeuchi, I.K., Inaguma, Y. & Kato, K. (2002) Riluzole enhances expression of brain-derived neurotrophic factor with consequent proliferation of granule precursor cells in the rat hippocampus. FASEB J., 16, 1328-1330.
106. Keller, A., Bagorda, F., Hildebrandt, K. & Teuchert-Noodt, G. (2000) Effects of enriched and of restricted rearing on both neurogenesis and synaptogenesis in the hippocampal dentate gyrus of adult gerbils (Meriones unguiculatus). Neurol. Psychiat. Brain Res., 8, 101-108.
107. Kempermann, G. (2002) Why new neurons? Possible functions for adult hippocampal neurogenesis. J. Neurosci., 22, 635-638.
108. Kempermann, G., Jessberger, S., Steiner, B. & Kronenberg, G. (2004) Milestones of neuronal devlopment in the adult hippocampus. Trends Neurosci., 27, 447-452.
109. Kempermann, G., Kuhn, H.G. & Gage, F.H. (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature, 386, 493-495.
110. Kim, M.J., Kim, H.K., Kim, B.S. & Yim, S.V. (2004) Melatonin increases cell proliferation in the dentate gyrus of maternally separated rats. J. Pineal Res., 37, 193-197.
111. Kitamura, T., Missina, M. & Sugiyama, H. (2003) Enhancement of neurogenesis by running wheel exercises is suppressed in mice lacking NMDA receptor epsilon 1 subunit. Neurosci. Res., 47, 55-63.
112. Kosorovitskiy, Y. & Gould, E. (2004) Dominance hierarchy influences adult neurogenesis in the dentate gyrus. J. Neurosci., 24, 6755-6759.
113. Kronenberg, G., Reuter, K., Steiner, B., Brandt, M.D., Jessberger, S., Yamaguchi, M. & Kempermann, G. (2003) Subpopulations of proliferating cells in the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol., 467, 455-463.
114. Kulkarni, V.A., Jha, S. & Vaidya, V.A. (2002) Depletion of norepinephrine decreases the proliferation, but does not influence the survival and differentiation, of granule cell progenitors in the adult rat hippocampus. Eur. J. Neurosci., 16, 2008-2012.
115. Larsson, E., Mandel, R.J., Klein, R.L., Muzyczka, N., Lindvall, O. & Kokaia, Z. (2002) Suppression of insult-induced neurogenesis in adult rat brain by brain-derived neurotrophic factor. Exp. Neurol., 177, 1-8.
116. Lauder, J.M. & Schambra, U.B. (1999) Morphogenetic roles of acetylcholine. Env. Health Perspect., 107 (Suppl. 1), 65-69.
117. Lee, J., Duan, W., Long, J.M., Ingram, D.K. & Mattson, M.P. (2000) Dietary restriction increases the number of newly generated neural cells, and induces BDNF expression, in the dentate gyrus of rats. J. Mol. Neurosci., 15, 99-108.
118. Leventhal, C., Rafii, S., Rafii, D., Shahar, A. & Goldman, S.A. (1999) Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol. Cel Neurosci., 13, 450-464.
119. Lichtenwalner, R.J., Forbes, M.E., Bennett, S.A., Lynch, C.D., Sonntag, W.E. & Riddle, D.R. (2001) Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience, 107, 603-613.
120. Linden, R. (1994) The survival of developing neurons: a review of afferent control. Neuroscience, 58, 671-682.
121. Liu, Y., Fowler, C.D., Young, L.J., Yan, Q., Insel, T.R. & Wang, Z. (2001) Expression and estrogen regulation of brain-derived neurotrophic factor gene and protein in the forebrain of female prairie voles. J. Comp. Neurol., 433, 499-514.
122. Louissaint, A., Rao, S., Leventhal, C. & Goldman, S.A. (2002) Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron, 34, 945-960.
123. Lu, L., Bao, G., Chen, H., Xia, P., Fan, X., Zhang, J., Pei, G. & Ma, L. (2003) Modification of hippocampal neurogenesis and neuroplasticity by social environments. Exp. Neurol., 183, 600-609.
124. Lu, P., Jones, L.L., Snyder, E.Y. & Tuszynski, M.H. (2003) Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp. Neurol., 181, 115-129.
125. Lucassen, P.J., Fuchs, E. & Czeh, B. (2004) Antidepressant treatment with tianeptine reduces apoptosis in the hippocampal dentate gyrus and temporal cortex. Biol. Psychiat., 55, 789-796.
126. Ma, W., Marie, D., Li, B.S., Hu, Q., Andreadis, J.D., Grant, G.M., Liu, Q.-Y., Shaffer, K.M., Chang, Y.C., Zhang, L., Pancrazio, J.J., Pant, H.C., Stenger, D.A. & Barker, J.L. (2000) Acetylcholine stimulates cortical precursor cell proliferation in vitro via muscarinic receptor activation and MAP kinase phosphorylation. Eur. J. Neurosci., 12, 1227-1240.
127. Maglóczky, Z., Wittner, L., Borhegyi, Z., Halasz, P., Vajda, J., Czirjak, S. & Freund, T.F. (2000) Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience, 96, 7-25.
128. Maki, P.M., Rich, J.B. & Rosenbaum, R.S. (2002) Implicit memory varies across the menstrual cycle: estrogen effects in young women. Neuropsychologia, 40, 518-529.
129. Malberg, J.E., Eisch, A.J., Nestler, E.J. & Duman, R.S. (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci., 20, 9104-9110.
130. Marr, D. (1971) Simple memory: a theory for archicortex. Phil. Trans. Roy. Soc. Lond., 262, 23-81.
131. Marriott, L.K. & Korol, D.L. (2003) Short-term estrogen treatment in ovariectomized rats augments hippocampal acetylcholine release during place learning. Neurobiol. Learn. Mem., 80, 315-322.
132. McEwen, B.S. (1994) Corticosteroids and hippocampal plasticity. Ann. NY Acad. Sci., 746, 134-142.
133. McEwen, B.S. (1999) Stress and hippocampal plasticity. Annu. Rev. Neurosci., 22, 105-122.
134. Merrill, D.A., Karim, R., Darraq, M., Chiba, A.A. & Tuszynski, M.H. (2003) Hippocampal cell genesis does not correlate with spatial learning ability in aged rats. J. Comp. Neurol., 459, 201-207.
135. Mirescu, C., Peters, J.D. & Gould, E. (2004) Early life experience alters response of adult neurogenesis to stress. Nat. Neurosci., 7, 841-846.
136. Mitome, M., Hasegawa, T. & Shirakawa, T. (2005) Mastication influences the survival of newly generated cells in mouse dentate gyrus. Neuroreport, 16, 249-252.
137. Mohapel, P., Leanza, G. & Lindvall, O. (2002) Alterations in forebrain acetylcholine influence hippocampal neurogenesis in the adult rodent. Soc. Neurosci. Abstr. [Program No. 23.9.2002 Abstract Viewer/Itinerary Planner. Washington, DC.]
138. Monje, M.L., Mizumatsu, S., Fike, J.R. & Palmer, T.D. (2002) Irradiation induces neural precursor-cell dysfunction. Nat. Med., 8, 955-962.
139. Morcuende, S., Gadd, C.A., Peters, M., Moss, A., Harris, E.A., Sheasby, A., Fisher, A.S., De Felipe, C., Mantyh, P.W., Rupniak, N.M., Giese, K.P. & Hunt, S.P. (2003) Increased neurogenesis and brain-derived neurotrophic factor in neurokinin-1 receptor gene knockout mice. Eur. J. Neurosci., 18, 1828-1836.
140. Moreno-López, B., Romero-Grimaldi, C., Noval, J.A., Murillo-Carretero, M., Matarredona, E.R. & Estrada, C. (2004) Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J. Neurosci., 24, 85-95.
141. Nacher, J., Alonso-Llosa, G., Rosell, D.R. & McEwen, B.S. (2003) NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol. Aging, 24, 273-284.
142. Nacher, J., Rosell, D.R., Alonso-Llosa, G. & 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, 512-520.
143. Nakata, N., Suda, H., Izumi, J., Tanaka, Y., Ikeda, Y., Kato, H., Itoyama, Y. & Kogure, K. (1997) Role of hippocampal serotonergic neurons in ischemic neuronal death. Behav. Brain Res., 83, 217-220.
144. Naylor, A.S., Persson, A.I., Eriksson, P.S., Jonsdottir, I.H. & Thorlin, T. (2005) Extended voluntary running inhibits exercise induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat. J. Neurophysiol., 93, 2406-2414.
145. Neeper, S.A., Gbmez-Pinilla, F., Choi, J. & Cotman, C. (1995) Exercise and brain neurotrophins. Nature, 373, 109.
146. Nilsson, M., Perfilieva, E., Johansson, U., Orwar, O. & Eriksson, P.S. (1999) Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J. Neurobiol., 39, 569-578.
147. Nixon, K. & Crews, F.T. (2002) Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J. Neurochem., 83, 1087-1093.
148. O'Kusky, J.R., Ye, P. & d'Ercole, J. (2000) Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J. Neurosci., 20, 8435-8442.
149. Osehobo, P., Adams, B., Sazgar, M., Xu, Y., Racine, R.J. & Fahnestock, M. (1999) Brain-derived neurotrophic factor infusion delays amygdala and perforant path kindling without affecting paired-pulse measures of neuronal inhibition in adult rats. Neuroscience, 92, 1367-1375.
150. Pakala, R. & Benedict, C.R. (1998) Effect of serotonin and thromboxane A2 on endothelial cell proliferation: effect of specific receptor antagonists. J. Lab. Clin. Med., 131, 527-537.
151. Palmer, T.D., Willhoite, A.R. & Gage, F.H. (2000) Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol., 425, 479-494.
152. Parent, J.M., Yu, T.W., Leibowitz, R.T., Geschwind, D.H., Sloviter, R.S. & 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, 3727-3738.
153. Park, C., Sohn, Y., Shin, K.S., Kim, J., Ahn, H. & Huh, Y. (2003) The chronic inhibition of nitric oxide synthase enhances cell proliferation in the adult rat hippocampus. Neurosci. Lett., 339, 9-12.
154. Pawlak, R., Skrzypiec, A., Sulkowksi, S. & Buczko, W. (2002) Ethanol-induced neurotoxicity is counterbalanced by increased cell proliferation in mouse dentate gyrus. Neurosci. Lett., 327, 83-86.
155. Persson, A.I., Thorlin, T., Bull., C., Zarnegar, P., Ekman, R., Terenius, L. & Eriksson, P.S. (2003) Mu- and delta-opioid receptor antagonists decrease proliferation and increase neurogenesis in cultures of rat adult hippocampal progenitors. Eur. J. Neurosci., 17, 1159-1172.
156. Pham, K., Nacher, J., Hof, P.R. & McEwen, B.S. (2003) Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci., 17, 879-886.
157. Plaisant, F., Dommergues, M.A., Spedding, M., Cecchelli, R., Brillault, J., Kato, G., Munoz, C. & Gressens, P. (2003) Neuroprotective properties of tianeptine: interactions with cytokines. Neuropharmacology, 44, 801-809.
158. van Praag, H., Kempermann, G. & Gage, F.H. (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci., 2, 266-270.
159. van Praag, H., Schinder, A.F., Christie, B.R., Toni, N., Palmer, T.D. & Gage, F.H. (2002) Functional neurogenesis in the adult hippocampus. Nature, 415, 1030-1034.
160. Pravosudov, V.V. & Omanska, A. (2005) Prolonged moderate elevation of corticosterone does not affect hippocampal anatomy or cell proliferation rates in mountain chickadees (Poecile gambeli). J. Neurobiol., 62, 82-91.
161. Prickaerts, J., Koopmans, G., Blokland, A. & Scheepens, A. (2004) Learning and adult neurogenesis: Survival with or without proliferation? Neurobiol. Learn. Mem., 81, 1-11.
162. Raber, J., Rola, R., LeFevour, A., Morhardt, D., Curley, J., Mizumatsu, S., VandenBerg, S.R. & Fike, J.R. (2004) Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat. Res., 162, 39-47.
163. Reagan, L.P. & McEwen, B.S. (1997) Controversies surrounding glucocorticoid-mediated cell death in the hippocampus. J. Chem. Neuroanat., 13, 149-167.
164. Reymann, K.G. & Ott, T. (1983) Footshock-induced modification of a monosynaptic evoked potential in the hippocampus. Physiol. Behav., 31, 615-617.
165. Richter-Levin, G. & Segal, M. (1990) Effects of serotonin releasers on dentate granule cell excitability in the rat. Exp. Brain Res., 82, 119-207.
166. Richter-Levin, G. & Segal, M. (1991) The effects of serotonin depletion and raphe grafts on hippocampal electrophysiology and behavior. J. Neurosci., 11, 1585-1596.
167. Rola, R., Raber, J., Rizk, A., Otsuka, S., VandenBerg, S.R., Morhardt, D.R. & Fike, J.R. (2004) Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp. Neurol., 188, 316-330.
168. Rueda, D., Navarro, B., Martínez-Serrano, A., Guzman, M. & Galve-Roperh, I. (2002) The endocannabinoid anandamide inhibits neuronal progenitor cell differentiation through attenuation of the Rap1/B-Raf/ERK pathway. J. Biol. Chem., 277, 46645-46650.
169. Sairanen, M., Lucas, G., Ernfors, P., Castren, M. & Castren, E. (2005) Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J. Neurosci., 25, 1089-1094.
170. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C. & Hen, R. (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science, 301, 805-809.
171. Schinder, A.F. & Gage, F.H. (2004) A hypothesis about the role of adult neurogenesis in hippocampal function. Physiology (Bethesda), 19, 253-261.
172. Schmidt-Hieber, C., Jonas, P. & Bischofberger, J. (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature, 429, 184-187.
173. Schmitt, A., Weber, S., Jatzko, A., Braus, D.F. & Henn, F.A. (2004) Hippocampal Volume and cell proliferation after acute and chronic clozapine or haloperidol treatment. J. Neural Transm., 111, 91-100.
174. Schwegler, H., Boldyreva, M., Linke, R., Wu, J., Zilles, K. & Crusio, W.E. (1996) Genetic variation in the morphology of the septo-hippocampal cholinergic and GABAergic systems in mice. II. Morpho-behavioral correlations. Hippocampus, 6, 535-545.
175. Seki, T. & 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, 503-513.
176. Shors, T.J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T. & Gould, E. (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature, 410, 372-376.
177. Shors, T.J., Townsend, D.A., Zhao, M., Kozorovitskiy, Y. & Gould, E. (2002) Neurogenesis may relate to some but not all types of hippocampal- dependent learning. Hippocampus, 12, 578-584.
178. Snyder, J.S., Jont, N.S., McDonald, R.J. & Wojtowicz, J.M. (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience, 130, 843-852.
179. Spoerri, P.E. & Wolff, J.R. (1981) Effect of GABA-administration on murine neuroblastoma cells in culture. Cell Tissue Res., 218, 567-579.
180. Stanfield, B.B. & Trice, J.E. (1988) Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp. Brain Res., 72, 399-406.
181. Tanapat, P., Galea, L.A. & Gould, E. (1998) Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. Int. J. Dev. Neurosci., 16, 235-239.
182. Tanapat, P., Hastings, N.B., Reeves, A.J. & Gould, E. (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci., 19, 5792-5801.
183. Tanapat, P., Hastings, N.B., Rydel, T.A., Galea, L.A. & Gould, E. (2001) Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J. Comp. Neurol., 437, 496-504.
184. Teuchert-Noodt, G. (2000) Neuronal degradation and reorganization: a mutual principle in pathological and in healthy interactions of limbic and prefrontal circuits. J. Neural Transm. Suppl., 60, 315-333.
185. Teuchert-Noodt, G., Dawirs, R.R. & Hildebrandt, K. (2000) Adult treatment with methamphetamine transiently decreases dentate granule cell proliferation in the gerbil hippocampus. J. Neural Transm., 107, 133-143.
186. Tooyama, I., Bellier, J.P., Park, M., Minnasch, P., Uemura, S., Hisano, T., Iwami, M., Aimi, Y., Yasuhara, O. & Rimura, H. (2002) Morphologic study of neuronal death, glial activation, and progenitor cell division in the hippocampus of rat models of epilepsy. Epilepsia, 43 (Suppl. 9), 39-43.
187. Trachtenberg, J.T., Chen, B.E., Knott, G.W., Feng, G., Sanes, J.R., Welker, E. & Svoboda, K. (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature, 420, 788-794.
188. Trejo, J.L., Carro, E. & Torres-Aleman, I. (2001) Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J. Neurosci., 21, 1628-1634.
189. Turrigiano, G.G., Leslie, K.R., Desai, N.S., Rutherford, L.C. & Nelson, S.B. (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature, 391, 892-896.
190. Wagner, J.P., Black, LB. & DiCicco-Bloom, E. (1999) Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J. Neurosci., 19, 6006-6016.
191. Wakade, C.G., Mahadik, S.P., Waller, J.L. & Chiu, F.-C. (2002) Atypical neuroleptics stimulate neurogenesis in adult rat brain. J. Neurosci. Res., 69, 72-79.
192. West, M. & Deadwyler, S.A. (1980) Circadian modulation of granule cell response to perforant path synaptic input in the rat. Neuroscience, 5, 1597-1602.
193. Wiskott, L., Resch, M.J. & Kempermann, G. (2004) What is the functional role of adult neurogenesis in the hippocampus? Cognitive Sciences EPrint Archive (CogPrints), 4012. [http://cogprints.org/4012/]
194. Wolff, J.R. & Missler, M. (1992) Synaptic reorganization in developing and adult nervous systems. Ann. Anat., 174, 393-403.
195. Wolff, J.R. & Wagner, G.P. (1983) Self-organization in synaptogenesis: interaction between the formation of excitatory and inhibitory synapses. In Basar, E., Flohr, H., Haken, H. & Mandell, A.J. (eds), Synergetics of the Brain. Springer, Berlin, Heidelberg, New York, Tokyo, pp. 50-59.
196. Yamaguchi, M., Suzuki, T., Seki, T., Namba, T., Juan, R., Arai, H., Hori, T. & Asada, T. (2004) Repetitive cocaine administration decreases neurogenesis in adult rat hippocampus. Ann. NY Acad. Sci., 1025, 351-362.
197. Yoshida, M., Sakai, M., Kani, K., Nagatsu, I. & Tanaka, M. (1988) The dopaminergic innervation as observed by immunohistochemistry using antidopamine serum in the rat cerebral cortex. Experientia, 44, 700-702.
198. Young, D., Lawlor, P.A., Leone, P., Dragunow, M. & During, M.J. (1999) Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat. Med., 5, 448-453.
199. Yu, I.T., Lee, S.H., Lee, Y.S. & Son, H. (2004) Differential effects of corticosterone and dexamethasone on hippocampal neurogenesis in vitro. Biochem. Biophys. Res. Commun., 317, 484-490.