Abstract
New neurons are generated from neural stem cells through the neuronal progenitor cell stage at the dentate gyrus of the hippocampal formation throughout life, and contribute to higher cognitive function, such as learning and memory. Physiological conditions, such as voluntary exercise or enriched environment, or pathophysiological conditions, such as stroke or epilepsy, upregulate the generation of new neurons, but the mechanism for governing the promotion of adult neurogenesis has not been fully clarified. It has been widely accepted that the neural activities of the hippocampal circuitry regulate the generation of hippocampal new neurons. Actually, a number of neurotransmitter systems – serotoninergic, GABAergic, cholinergic, purinergic, and glutamatergic systems – are involved in the regulation of adult hippocampal neurogenesis process. In this chapter, we propose a possible involvement of activity-dependent regulation of the fate of neural stem/progenitor cells in enhanced hippocampal neurogenesis. In a series of studies, we and others have reported how hippocampal activity affects the generation of new neurons, even at the early phase of adult hippocampal neurogenesis. These findings may also contribute to the pharmaceutical enhancement of adult neurogenesis for treating neurodegenerative and psychological disorders.
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References
Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85:523–569
Airan RD, Meltzer LA, Roy M et al (2007) High-speed imaging reveals neurophysiological links to behavior in an animal model of depression. Science 317:819–823
Aizawa K, Ageyama N, Terao K, Hisatsune T (2011) Primate-specific alterations in neural stem/progenitor cells in the aged hippocampus. Neurobiol Aging, doi: 10.1016/j.neurobiolaging.32:140–150 (2011).12.011, online
Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335
Altman J, Das GD (1967) Postnatal neurogenesis in the guinea-pig. Nature 214:1098–1101
Amaral D, Lavenex P (2007) Hippocampal neuroanatomy. In: Anderson P, Morris R, Amaral D, Bliss T, O’Keefe J (eds) The hippocampus book. Oxford University Press, New York, p 37–114
Bland BH (1986) The physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26:1–54
Bordey A, Sontheimer H (2000) Ion channel expression by astrocytes in situ: comparison of different CNS regions. Glia 30:27–38
Bruel-Jungerman E, Davis S, Rampon C et al (2006) Long-term potentiation enhances neurogenesis in the adult dentate gyrus. J Neurosci 26:5888–5893
Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325–340
Buzsáki G (2006) Rhythms of the brain. Oxford University Press, New York
Cameron HA, McEwen BS, Gould E (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 15:4687–4692
Chun SK, Sun W, Park, JJ et al (2006) Enhanced proliferation of progenitor cells following long-term potentiation induction in the rat dentate gyrus. Neurobiol Learn Mem 86:322–329
Cornwell BR, Johnson LL, Holroyd T et al (2008) Human hippocampal and parahippocampal theta during goal-directed spatial navigation predicts performance on a virtual Morris water maze. J Neurosci 28:5983–5990
Deisseroth K, Singla S, Toda H et al (2004) Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535–552
Döbrössy MD, Drapeau E, Aurousseau C et al (2003) Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol Psychiatry 8:974–982
Dupret D, Fabre A, Döbrössy MD et al (2007) Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol 5:e214
Dupret D, Revest JM, Koehl M et al (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 3:e1959
Eriksson PS, Perfilieva E, Bjork-Eriksson T et al (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317
Esposito MS, Piatti VC, Laplagne DA et al (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25:10074–10086
Fabel K, Tam B, Kaufer D et al (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18:2803–2812
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 23:373–382
Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470
Fukuda S, Kato F, Tozuka Y et al (2003) Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 23:9357–9366
Ge S, Goh EL, Sailor KA et al (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589–593
Ge S, Yang CH, Hsu KS et al (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 24:559–566
Gould E, Tanapat P, McEwen BS et al (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95:3168–3171
Gould E, Beylin A, Tanapat P et al (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260–265
Green JD, Arduini A (1954) Hippocampal electrical activity in arousal. J Neurophysiol 17:533–557
Hattiangady B, Shetty AK (2008) Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiol Aging 29:129–147
Ide Y, Fujiyama F, Okamoto-Furuta K, Tamamaki N, Kaneko T, Hisatsune T (2008) Rapid integration of young newborn dentate gyrus granule cells in the adult hippocampal circuitry. Eur J Neurosci 28:2381–2392
Itou Y, Nochi R, Kuribayashi H, Saito Y, Hisatsune T (2011) Cholinergic activation of hippocampal neural stem cells in aged dentate gyrus. Hippocampus 21:446–459
Jin K, Minami M, Lan JQ et al (2001) Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 98:4710–4715
Jung R, Kornmullar A (1938) Eine methodik der ableitung lokalisierter potential schwankingen aus subcorticalen hirnyebieten. Arch Psychiat Neruenkr 109:1–30
Kahana MJ, Sekuler R, Caplan JB et al (1999) Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 24:781–784
Kaneko N, Okano H, Sawamoto K (2006) Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells 11:1145–1159
Kaplan MS, Bell DH (1984) Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J Neurosci 4:1429–1441
Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092–1094
Kee N, Teixeira CM, Wang AH et al (2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10:355–362
Kempermann G, Kuhn HG, Gage FH (1997) Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci USA 94:10409–10414
Kempermann G, Brandon EP, Gage FH (1998) Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus. Curr Biol 8:939–942
Kempermann G, Jessberger S, Steiner B et al (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447–452
Koketsu D, Furuichi Y, Maeda, M et al (2006) Increased number of new neurons in the olfactory bulb and hippocampus of adult non-human primates after focal ischemia. Exp Neurol 199:92–102
Kornack DR, Rakic P (1999) Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci USA 96:5768–5773
Kramis R, Vanderwolf CH, Bland BH (1975) Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp Neurol 49:58–85
Kressin K, Kuprijanova E, Jabs R et al (1995) Developmental regulation of Na+ and K+ conductances in glial cells of mouse hippocampal brain slices. Glia 15:173–187
Lawson VH, Bland BH (1993) The role of the septohippocampal pathway in the regulation of hippocampal field activity and behavior: analysis by the intraseptal microinfusion of carbachol, atropine, and procaine. Exp Neurol 120:132–144
Matsuyama S, Nei K, Tanaka C (1997) Regulation of GABA release via NMDA and 5-HT1A receptors in guinea pig dentate gyrus. Brain Res 761:105–112
Matthias K, Kirchhoff F, Seifert G et al (2003) Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 23:1750–1758
Mohapel P, Leanza G, Kokaia M et al (2005) Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging 26:939–946
Nacher J, Rosell DR, Alonso-Llosa G et al (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
O’Keefe (2007) Hippocampal neurophysiology in the behaving animal. In: Andersen P, Morris R, Amaral D, et al (eds) The hippocampus book. Oxford University Press, New York
Olariu A, Cleaver KM, Shore LE et al (2005) A natural form of learning can increase and decrease the survival of new neurons in the dentate gyrus. Hippocampus 15:750–762
Pereira AC, Huddleston DE, Brickman AM et al (2007) An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA 104:5638–5643
Santarelli L, Saxe M, Gross C et al (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805–809
Saxe MD, Battaglia F, Wang J et al (2006) Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA 103:17501–17506
Seri B, Garcia-Verdugo JM, McEwen BS et al (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–7160
Shors TJ, Miesegaes G, Beylin A et al (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372–376
Steiner B, Klempin F, Wang L et al (2006) Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54:805–814
Suh H, Consiglio A, Ray J et al (2007) In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2(+) neural stem cells in the adult hippocampus. Cell Stem Cell 1:515–528
Tashiro A, Sandler VM, Toni N et al (2006) NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442:929–933
Tonchev AB, Yamashima T, Zhao L et al (2003) Proliferation of neural and neuronal progenitors after global brain ischemia in young adult macaque monkeys. Mol Cell Neurosci 23:292–301
Toni N, Teng EM, Bushong EA et al (2007) Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10:727–734
Tozuka Y, Fukuda S, Namba T et al (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47:803–815
van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266–270
van Praag H, Schinder AF, Christie BR et al (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030–1034
Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407–418
Wang LP, Kempermann G, Kettenmann H (2005) A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 29:181–189
Yamaguchi M, Saito H, Suzuki M et al (2000) Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. Neuroreport 26:1991–1996
Yoshimura S, Takagi Y, Harada J et al (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci USA 98:5874–5879
Zhang CL, Zou Y, He W et al (2008) A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451:1004–1007
Zhao C, Teng EM, Summers RG Jr., et al (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3–11
Acknowledgments
We thank Drs. Satoshi Fukuda and Yusuke Tozuka for their discussion, comments, and the images.
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Hisatsune, T., Ide, Y., Nochi, R. (2011). Activity-Dependent Regulation of the Early Phase of Adult Hippocampal Neurogenesis. In: Seki, T., Sawamoto, K., Parent, J.M., Alvarez-Buylla, A. (eds) Neurogenesis in the Adult Brain I. Springer, Tokyo. https://doi.org/10.1007/978-4-431-53933-9_8
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DOI: https://doi.org/10.1007/978-4-431-53933-9_8
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