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European Archives of Psychiatry and Clinical Neuroscience

Published in:

01-08-2007 | SPECIAL ISSUE

Adult hippocampal neurogenesis and aging

Authors: Friederike Klempin, Gerd Kempermann, MD

Published in: European Archives of Psychiatry and Clinical Neuroscience | Issue 5/2007

Abstract

The demographic changes in the foreseeable future stress the need for research on successful cognitive aging. Advancing age constitutes a primary risk factor for disease of the central nervous system most notably neurodegenerative disorders. The hippocampus is one of the brain regions that is prominently affected by neurodegeneration and functional decline even in what is still considered “normal aging”. Plasticity is the basis for how the brain adapts to changes over time. The discovery of adult hippocampal neurogenesis has added a whole new dimension to research on structural plasticity in the adult and aging hippocampus. In this article, we briefly summarize and discuss recent findings on the regulation of adult neurogenesis with relevance to aging. Aging is an important co-variable for many regulatory mechanisms affecting adult neurogenesis but so far, only few studies have specifically addressed this interaction. We hypothesize that adult neurogenesis contributes to a neural reserve, i.e. the maintained potential for structural plasticity that allows compensation in situations of functional losses with aging. As such we propose that adult neurogenesis might contribute to the structural correlates of successful aging.

Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85:523–569PubMed

Aimone JB, Wiles J, Gage FH (2006) Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 9:723–727PubMed

Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. 3. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J Comp Neurol 136:269–293PubMed

Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335PubMed

Altman J, Das GD (1965) Post-natal origin of microneurons in the rat brain. Nature 207:935–956

Banasr M, Hery M, Brezun JM, Daszuta A (2001) Serotonin mediates oestrogen 207:953–956 stimulation of cell proliferation in the adult dentate gyrus. Eur J Neurosci 14:1417–1424PubMed

Banasr M, Hery M, Printemps R, Daszuta A (2004) Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 29:450–460PubMed

Barker JM, Wojtowicz JM, Boonstra R (2005) Where’s my dinner? Adult neurogenesis in free-living food-storing rodents. Genes Brain Behav 4:89–98PubMed

Becker S (2005) A computational principle for hippocampal learning and neurogenesis. Hippocampus 15:722–738PubMed

10.

Beekman AT, Penninx BW, Deeg DJ, Ormel J, Braam AW, van Tilburg W (1997) Depression and physical health in later life: results from the Longitudinal Aging Study Amsterdam (LASA). J Affect Disord 46:219–231PubMed

11.

Bizon JL, Lee HJ, Gallagher M (2004) Neurogenesis in a rat model of age-related cognitive decline. Aging Cell 3:227–234PubMed

12.

Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, Bick-Sander A, von der Behrens W, Kempermann G (2003) Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 24:603–613PubMed

13.

Brezun JM, Daszuta A (2000) Serotonergic reinnervation reverses lesion-induced decreases in PSA-NCAM labeling and proliferation of hippocampal cells in adult rats. Hippocampus 10:37–46PubMed

14.

Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, Gage FH, Kuhn HG (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17:2042–2046PubMed

15.

Buckwalter MS, Yamane M, Coleman BS, Ormerod BK, Chin JT, Palmer T, Wyss-Coray T (2006) Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am J Pathol 169:154–164PubMed

16.

Cameron HA, Hazel TG, McKay RD (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol 36:287–306PubMed

17.

Cameron HA, McKay RD (1999) Restoring production of hippocampal neurons in old age. Nat Neurosci 2:894–897PubMed

18.

Cameron HA, Woolley CS, McEwen BS, Gould E (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337–344PubMed

19.

Caporaso GL, Lim DA, Alvarez-Buylla A, Chao MV (2003) Telomerase activity in the subventricular zone of adult mice. Mol Cell Neurosci 23:693–702PubMed

20.

Carlen M, Cassidy RM, Brismar H, Smith GA, Enquist LW, Frisen J (2002) Functional integration of adult-born neurons. Curr Biol 12:606–608PubMed

21.

Cecchi GA, Petreanu LT, Alvarez-Buylla A, Magnasco MO (2001) Unsupervised learning and adaptation in a model of adult neurogenesis. J Comput Neurosci 11:175–182PubMed

22.

Chadashvili T, Peterson DA (2006) Cytoarchitecture of fibroblast growth factor receptor 2 (FGFR-2) immunoreactivity in astrocytes of neurogenic and non-neurogenic regions of the young adult and aged rat brain. J Comp Neurol 498:1–15PubMed

23.

Chambers RA, Potenza MN, Hoffman RE, Miranker W (2004) Simulated apoptosis/neurogenesis regulates learning and memory capabilities of adaptive neural networks. Neuropsychopharmacology 29:747–758PubMed

24.

Colcombe SJ, Kramer AF, Erickson KI, Scalf P, McAuley E, Cohen NJ, Webb A, Jerome GJ, Marquez DX, Elavsky S (2004) Cardiovascular fitness, cortical plasticity, and aging. Proc Natl Acad Sci USA 101:3316–3321PubMed

25.

Corotto FS, Henegar JA, Maruniak JA (1993) Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci Lett 149:111–114PubMed

26.

Darnaudery M, Perez-Martin M, Belizaire G, Maccari S, Garcia-Segura LM (2006) Insulin-like growth factor 1 reduces age-related disorders induced by prenatal stress in female rats. Neurobiol Aging 27:119–127PubMed

27.

Darsalia V, Heldmann U, Lindvall O, Kokaia Z (2005) Stroke-induced neurogenesis in aged brain. Stroke 36:1790–1795PubMed

28.

Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC (2004) Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535–552PubMed

29.

Dietrich J, Kempermann G (2006) Role of endogenous neural stem cells in neurological disease and brain repair. Adv Exp Med Biol 557:191–220PubMedCrossRef

30.

Dobrossy MD, Drapeau E, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2003) Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol Psychiatry 8:974–982PubMed

31.

Doetsch F, Hen R (2005) Young and excitable: the function of new neurons in the adult mammalian brain. Curr Opin Neurobiol 15:121–128PubMed

32.

Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2003) Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci USA 100:14385–14390PubMed

33.

Driscoll I, Howard SR, Stone JC, Monfils MH, Tomanek B, Brooks WM, Sutherland RJ (2006) The aging hippocampus: a multi-level analysis in the rat. Neuroscience 139:1173–1185PubMed

34.

Driscoll I, Sutherland RJ (2005) The aging hippocampus: navigating between rat and human experiments. Rev Neurosci 16:87–121PubMed

35.

D′Sa C, Duman RS (2002) Antidepressants and neuroplasticity. Bipolar Disord 4:183–194PubMed

36.

Dugar A, Keck BJ, Maines LW, Miller S, Njai R, Lakoski JM (2001) Compensatory responses in the aging hippocampal serotonergic system following neurodegenerative injury with 5,7-dihydroxytryptamine. Synapse 39:109–121PubMed

37.

Duman RS (2004) Depression: a case of neuronal life and death? Biol Psychiatry 56:140–145PubMed

38.

Duman RS, Malberg J, Nakagawa S, D’Sa C (2000) Neuronal plasticity and survival in mood disorders. Biol Psychiatry 48:732–739PubMed

39.

Duman RS, Malberg J, Thome J (1999) Neural plasticity to stress and antidepressant treatment. Biol Psychiatry 46:1181–1191PubMed

40.

Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116–1127PubMed

41.

Duman RS, Nakagawa S, Malberg J (2001) Regulation of adult neurogenesis by antidepressant treatment. Neuropsychopharmacology 25:836–844PubMed

42.

Ehninger D, Kempermann G (2006) Paradoxical effects of learning the Morris water maze on adult hippocampal neurogenesis in mice may be explained by a combination of stress and physical activity. Genes Brain Behav 5:29–39PubMed

43.

Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 24:8354–8365PubMed

44.

Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317PubMed

45.

Fabel K, Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo CJ, Palmer TD (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18:2803–2812PubMed

46.

Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang LP, Yamaguchi M, Kettenmann H, Kempermann G (2003) Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 23:373–382PubMed

47.

Galea LA, Spritzer MD, Barker JM, Pawluski JL (2006) Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 16:225–232PubMed

48.

Garcia A, Steiner B, Kronenberg G, Bick-Sander A, Kempermann G (2004) Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 3:363–371PubMed

49.

Garcia-Segura LM, Cardona-Gomez GP, Chowen JA, Azcoitia I (2000) Insulin-like growth factor-I receptors and estrogen receptors interact in the promotion of neuronal survival and neuroprotection. J Neurocytol 29:425–437PubMed

50.

Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492–2498PubMed

51.

Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, Fuchs E (1999) Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci USA 96:5263–5267PubMed

52.

Gould E, Tanapat P (1999) Stress and hippocampal neurogenesis. Biol Psychiatry 46:1472–1479PubMed

53.

Harris AH, Cronkite R, Moos R (2006) Physical activity, exercise coping, and depression in a 10-year cohort study of depressed patients. J Affect Disord 93:79–85PubMed

54.

Hattiangady B, Rao MS, Shetty GA, Shetty AK (2005) Brain-derived neurotrophic factor, phosphorylated cyclic AMP response element binding protein and neuropeptide Y decline as early as middle age in the dentate gyrus and CA1 and CA3 subfields of the hippocampus. Exp Neurol 195:353–371PubMed

55.

Hattiangady B, Shetty AK (2006) Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiol Aging PMID: 17092610

56.

Heffelfinger AK, Newcomer JW (2001) Glucocorticoid effects on memory function over the human life span. Dev Psychopathol 13:491–513PubMed

57.

Heine VM, Maslam S, Joels M, Lucassen PJ (2004) 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 25:361–375PubMed

58.

Heine VM, Zareno J, Maslam S, Joels M, Lucassen PJ (2005) Chronic stress in the adult dentate gyrus reduces cell proliferation near the vasculature and VEGF and Flk-1 protein expression. Eur J Neurosci 21:1304–1314PubMed

59.

Henn FA, Vollmayr B (2004) Neurogenesis and depression: etiology or epiphenomenon? Biol Psychiatry 56:146–150PubMed

60.

Hogervorst E, Yaffe K, Richards M, Huppert F (2002) Hormone replacement therapy for cognitive function in postmenopausal women. Cochrane Database Syst Rev:CD003122

61.

Holmes A, Yang RJ, Lesch KP, Crawley JN, Murphy DL (2003) Mice lacking the serotonin transporter exhibit 5-HT(1A) receptor-mediated abnormalities in tests for anxiety-like behavior. Neuropsychopharmacology 28:2077–2088PubMed

62.

Husum H, Aznar S, Hoyer-Hansen S, Larsen MH, Mikkelsen JD, Moller A, Mathe AA, Wortwein G (2006) Exacerbated loss of cell survival, neuropeptide Y-immunoreactive (IR) cells, and serotonin-IR fiber lengths in the dorsal hippocampus of the aged flinders sensitive line “depressed” rat: Implications for the pathophysiology of depression? J Neurosci Res 84:1292–1302PubMed

63.

Iritani S, Tohgi M, Arai T, Ikeda K (2006) Immunohistochemical study of the serotonergic neuronal system in an animal model of the mood disorder. Exp Neurol 201:60–65PubMed

64.

Jacobs BL (2002) Adult brain neurogenesis and depression. Brain Behav Immun 16:602–609PubMed

65.

Jacobs BL, Praag H, Gage FH (2000) Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol Psychiatry 5:262–269PubMed

66.

Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, Logvinova A, Greenberg DA (2003) Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2:175–183PubMed

67.

Kakiuchi T, Tsukada H, Fukumoto D, Nishiyama S (2001) Effects of aging on serotonin transporter availability and its response to fluvoxamine in the living brain: PET study with ((11)C)(+)McN5652 and ((11)C)(−)McN5652 in conscious monkeys. Synapse 40:170–179PubMed

68.

Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092–1094PubMed

69.

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 8:939–942PubMed

70.

Kempermann G, Chesler EJ, Lu L, Williams RW, Gage FH (2006) Natural variation and genetic covariance in adult hippocampal neurogenesis. Proc Natl Acad Sci USA 103:780–785PubMed

71.

Kempermann G, Gage FH (1999) Experience-dependent regulation of adult hippocampal neurogenesis: effects of long-term stimulation and stimulus withdrawal. Hippocampus 9:321–332PubMed

72.

Kempermann G, Gast D, Gage FH (2002) Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52:135–143PubMed

73.

Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447–452PubMed

74.

Kempermann G, Kronenberg G (2003) Depressed new neurons—adult hippocampal neurogenesis and a cellular plasticity hypothesis of major depression. Biol Psychiatry 54:499–503PubMed

75.

Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493–495PubMed

76.

Kempermann G, Kuhn HG, Gage FH (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18:3206–3212PubMed

77.

Kempermann G, Wiskott L, Gage FH (2004) Functional significance of adult neurogenesis. Curr Opin Neurobiol 14:186–191PubMed

78.

Keuker JI, Keijser JN, Nyakas C, Luiten PG, Fuchs E (2005) Aging is accompanied by a subfield-specific reduction of serotonergic fibers in the tree shrew hippocampal formation. J Chem Neuroanat 30:221–229PubMed

79.

Koehl M, Darnaudery M, Dulluc J, Van Reeth O, Le Moal M, Maccari S (1999) Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J Neurobiol 40:302–315PubMed

80.

Kronenberg G, Bick-Sander A, Bunk E, Wolf C, Ehninger D, Kempermann G (2006) Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol Aging 27:1505–1513PubMed

81.

Kronenberg G, Reuter K, Steiner B, Brandt MD, Jessberger S, Yamaguchi M, Kempermann G (2003) Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 467:455–463PubMed

82.

Kudo K, Wati H, Qiao C, Arita J, Kanba S (2005) Age-related disturbance of memory and CREB phosphorylation in CA1 area of hippocampus of rats. Brain Res 1054:30–37PubMed

83.

Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033PubMed

84.

Kwon YK (2002) Effect of neurotrophic factors on neuronal stem cell death. J Biochem Mol Biol 35:87–93PubMed

85.

Lee HW, Blasco MA, Gottlieb GJ, Horner JW 2nd, Greider CW, DePinho RA (1998) Essential role of mouse telomerase in highly proliferative organs. Nature 392:569–574PubMed

86.

Lehmann K, Butz M, Teuchert-Noodt G (2005) Offer and demand: proliferation and survival of neurons in the dentate gyrus. Eur J Neurosci 21:3205–3216PubMed

87.

Lichtenwalner RJ, Forbes ME, Bennett SA, Lynch CD, Sonntag WE, Riddle DR (2001) Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 107:603–613PubMed

88.

Low LF, Anstey KJ (2006) Hormone replacement therapy and cognitive performance in postmenopausal women—a review by cognitive domain. Neurosci Biobehav Rev 30:66–84PubMed

89.

Lucassen PJ, Heine VM, Muller MB, van der Beek EM, Wiegant VM, De Kloet ER, Joels M, Fuchs E, Swaab DF, Czeh B (2006) Stress, depression and hippocampal apoptosis. CNS Neurol Disord Drug Targets 5:531–546PubMed

90.

Lund PK, Hoyt EC, Bizon J, Smith DR, Haberman R, Helm K, Gallagher M (2004) Transcriptional mechanisms of hippocampal aging. Exp Gerontol 39:1613–1622PubMed

91.

Luo J, Daniels SB, Lennington JB, Notti RQ, Conover JC (2006) The aging neurogenic subventricular zone. Aging Cell 5:139–152PubMed

92.

Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173–189PubMed

93.

Magri F, Cravello L, Barili L, Sarra S, Cinchetti W, Salmoiraghi F, Micale G, Ferrari E (2006) Stress and dementia: the role of the hypothalamicpituitary-adrenal axis. Aging Clin Exp Res 18:167–170PubMed

94.

Malberg JE, Duman RS (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28:1562–1571PubMed

95.

Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104–9110PubMed

96.

Malberg JE, Schechter LE (2005) Increasing hippocampal neurogenesis: a novel mechanism for antidepressant drugs. Curr Pharm Des 11:145–155PubMed

97.

Mayer JL, Klumpers L, Maslam S, de Kloet ER, Joels M, Lucassen PJ (2006) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalises the corticosterone-induced reduction of adult hippocampal neurogenesis. J Neuroendocrinol 18:629–631PubMed

98.

Mazure CM, Maciejewski PK (2003) A model of risk for major depression: effects of life stress and cognitive style vary by age. Depress Anxiety 17:26–33PubMed

99.

Mercier F, Kitasako JT, Hatton GI (2002) Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J Comp Neurol 451:170–188PubMed

100.

Mirescu C, Gould E (2006) Stress and adult neurogenesis. Hippocampus 16:233–238PubMed

101.

Molofsky AV, Slutsky SG, Joseph NM, He S, Pardal R, Krishnamurthy J, Sharpless NE, Morrison SJ (2006) Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443:448–452PubMed

102.

Montaron MF, Drapeau E, Dupret D, Kitchener P, Aurousseau C, Le Moal M, Piazza PV, Abrous DN (2006) Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiol Aging 27:645–654PubMed

103.

Naylor AS, Persson AI, Eriksson PS, Jonsdottir IH, Thorlin T (2005) Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat. J Neurophysiol 93:2406–2414PubMed

104.

Ormerod BK, Lee TT, Galea LA (2003) Estradiol initially enhances but subsequently suppresses (via adrenal steroids) granule cell proliferation in the dentate gyrus of adult female rats. J Neurobiol 55:247–260PubMed

105.

Overstreet-Wadiche LS, Bensen AL, Westbrook GL (2006) Delayed development of adult-generated granule cells in dentate gyrus. J Neurosci 26:2326–2334PubMed

106.

Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479–494PubMed

107.

Rando TA (2006) Stem cells, ageing and the quest for immortality. Nature 441:1080–1086PubMed

108.

Rao MS, Hattiangady B, Abdel-Rahman A, Stanley DP, Shetty AK (2005) Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur J Neurosci 21:464–476PubMed

109.

Rosenbrock H, Bloching A, Weiss C, Borsini F (2005) Partial serotonergic denervation decreases progenitor cell proliferation in the adult rat hippocampus, but has no effect on rat behavior in the forced swimming test. Pharmacol Biochem Behav 80:549–556PubMed

110.

Rosenzweig ES, Barnes CA (2003) Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69:143–179PubMed

111.

Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57–65PubMed

112.

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 301:805–809PubMed

113.

Sapolsky RM (1999) Glucocorticoids, stress, and their adverse neurological effects: relevance to aging. Exp Gerontol 34:721–732PubMed

114.

Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184–187PubMed

115.

Seki T (2003) Microenvironmental elements supporting adult hippocampal neurogenesis. Anat Sci Int 78:69–78PubMed

116.

Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–7160PubMed

117.

Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW (1996) Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci USA 93:3908–3913PubMed

118.

Shetty AK, Hattiangady B, Shetty GA (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 51:173–186PubMed

119.

Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372–376PubMed

120.

Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12:578–584PubMed

121.

Simon M, Czeh B, Fuchs E (2005) Age-dependent susceptibility of adult hippocampal cell proliferation to chronic psychosocial stress. Brain Res 1049:244–248PubMed

122.

Steiner B, Wolf SA, Kempermann G (2007) Adult neurogenesis and neurodegenerative disorders. Regen Medicine 1:15–28

123.

Sun LY, Evans MS, Hsieh J, Panici J, Bartke A (2005) Increased neurogenesis in dentate gyrus of long-lived Ames dwarf mice. Endocrinology 146:1138–1144PubMed

124.

Tanapat P, Hastings NB, Reeves AJ, 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 19:5792–5801PubMed

125.

Toth M (2003) 5-HT1A receptor knockout mouse as a genetic model of anxiety. Eur J Pharmacol 463:177–184PubMed

126.

Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47:803–815PubMed

127.

Trejo JL, 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 21:1628–1634PubMed

128.

van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427–13431PubMed

129.

van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266–270PubMed

130.

van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191–198PubMed

131.

van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030–1034PubMed

132.

van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680–8685PubMed

133.

Videbech P, Ravnkilde B (2004) Hippocampal volume and depression: a meta-analysis of MRI studies. Am J Psychiatry 161:1957–1966PubMed

134.

Wang LP, Kempermann G, Kettenmann H (2005) A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 29:181–189PubMed

135.

Wati H, Kudo K, Qiao C, Kuroki T, Kanba S (2006) A decreased survival of proliferated cells in the hippocampus is associated with a decline in spatial memory in aged rats. Neurosci Lett 399:171–174PubMed

136.

West MJ, Coleman PD, Flood DG, Troncoso JC (1994) Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer’s disease. Lancet 344:769–772PubMed

137.

Wilson RS, Mendes De Leon CF, Barnes LL, Schneider JA, Bienias JL, Evans DA, Bennett DA (2002) Participation in cognitively stimulating activities and risk of incident Alzheimer disease. Jama 287:742–748PubMed

138.

Winner B, Cooper-Kuhn CM, Aigner R, Winkler J, Kuhn HG (2002) Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur J Neurosci 16:1681–1689PubMed

139.

Wise PM (2003) Creating new neurons in old brains. Sci Aging Knowledge Environ 2003:PE13PubMed

140.

Wiskott L, Rasch MJ, Kempermann G (2006) A functional hypothesis for adult hippocampal neurogenesis: avoidance of catastrophic interference in the dentate gyrus. Hippocampus 16:329–343PubMed

141.

Yan W, Wilson CC, Haring JH (1997) 5-HT1a receptors mediate the neurotrophic effect of serotonin on developing dentate granule cells. Brain Res Dev Brain Res 98:185–190PubMed

Title: Adult hippocampal neurogenesis and aging
Authors: Friederike Klempin
Gerd Kempermann, MD
Publication date: 01-08-2007
Publisher: D. Steinkopff-Verlag
Published in: European Archives of Psychiatry and Clinical Neuroscience / Issue 5/2007
Print ISSN: 0940-1334
Electronic ISSN: 1433-8491
DOI: https://doi.org/10.1007/s00406-007-0731-5

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Adult hippocampal neurogenesis and aging

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

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