Skip to main content
Log in

Life-Long Hippocampal Neurogenesis: Environmental, Pharmacological and Neurochemical Modulations

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

It is now well documented that active neurogenesis does exist throughout the life span in the brain of various species including human. Two discrete brain regions contain progenitor cells that are capable of differentiating into neurons or glia, the subventricular zone and the dentate gyrus of the hippocampal formation. Recent studies have shown that neurogenesis can be modulated by a variety of factors, including stress and neurohormones, growth factors, neurotransmitters, drugs of abuse, and also strokes and traumatic brain injuries. In particular, the hippocampal neurogenesis may play a role in neuroadaptation associated with pathologies, such as cognitive disorders and depression. The increased neurogenesis at sites of injury may represent an attempt by the central nervous system to regenerate after damage. We herein review the most significant data on hippocampal neurogenesis in brain under various pathological conditions, with a special attention to mood disorders including depression and addiction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Gage FH (2000) Mammalian neural stem cells. Science 287:1433–1438

    PubMed  CAS  Google Scholar 

  2. Temple S (2001) The development of neural stem cells. Nature 414:112–117

    PubMed  CAS  Google Scholar 

  3. Gross CG (2000) Neurogenesis in the adult brain: death of a dogma. Nat Rev Neurosci 1:67–73

    PubMed  CAS  Google Scholar 

  4. Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433–457

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  6. Altman J, Das GD (1966) Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J Comp Neurol 126:337–389

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  8. Gould E, Reeves AJ, Graziano MS et al (1999) Neurogenesis in the neocortex of adult primates. Science 286:548–552

    PubMed  CAS  Google Scholar 

  9. Eriksson PS, Perfilieva E, Bjork-Eriksson T et al (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317

    PubMed  CAS  Google Scholar 

  10. Costanzo RM (1984) Comparison of neurogenesis and cell replacement in the hamster olfactory system with and without a target (olfactory bulb). Brain Res 307:295–301

    PubMed  CAS  Google Scholar 

  11. Gould E, Gross CG (2002) Neurogenesis in adult mammals: some progress and problems. J Neurosci 22:619–623

    PubMed  CAS  Google Scholar 

  12. Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179–193

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  14. Hastings NB, Seth MI, Tanapat P et al (2002) Granule neurons generated during development extend divergent axon collaterals to hippocampal area CA3. J Comp Neurol 452:324–333

    PubMed  Google Scholar 

  15. Lie DC, Song H, Colamarino SA et al (2004) Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu Rev Pharmacol Toxicol 44:399–421

    PubMed  CAS  Google Scholar 

  16. Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250

    PubMed  CAS  Google Scholar 

  17. Hastings NB, Gould E (1999) Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413:146–154

    PubMed  CAS  Google Scholar 

  18. Darsalia V, Heldmann U, Lindvall O et al (2005) Stroke-induced neurogenesis in aged brain. Stroke 36:1790–1795

    PubMed  Google Scholar 

  19. Lichtenwalner RJ, Parent JM (2006) Adult neurogenesis and the ischemic forebrain. J Cereb Blood Flow Metab 26:1–20

    PubMed  CAS  Google Scholar 

  20. Sidman RL, Miale IL, Feder N (1959) Cell proliferation and migration in the primitive ependymal zone: an autoradiographic study of histogenesis in the nervous system. Exp Neurol 1:322–333

    PubMed  CAS  Google Scholar 

  21. Gratzner HG (1982) Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: A new reagent for detection of DNA replication. Science 218:474–475

    PubMed  CAS  Google Scholar 

  22. Nowakowski RS, Lewin SB, Miller MW (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18:311–318

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  24. 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 16:2027–2033

    PubMed  CAS  Google Scholar 

  25. Miller MW, Nowakowski RS (1988) Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res 457:44–52

    PubMed  CAS  Google Scholar 

  26. Taupin P (2007) BrdU immunohistochemistry for studying adult neurogenesis: Paradigms, pitfalls, limitations, and validation. Brain Res Brain Res Rev 53:198–214

    CAS  Google Scholar 

  27. Taupin P, Ray J, Fischer WH et al (2000) FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/paracrine cofactor. Neuron 28:385–397

    PubMed  CAS  Google Scholar 

  28. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  30. Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406–417

    PubMed  CAS  Google Scholar 

  31. McEwen BS (2004) Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann NY Acad Sci 1032:1–7

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  33. Gould E, Reeves AJ, Fallah M et al (1999) Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci USA 96:5263–5267

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  35. van Praag H, Schinder AF, Christie BR et al (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030–1034

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  39. Dranovsky A, Hen R (2006) Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry 59:1136–1143

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  41. Malberg JE (2004) Implications of adult hippocampal neurogenesis in antidepressant action. J Psychiatry Neurosci 29:196–205

    PubMed  Google Scholar 

  42. Taupin P, Gage FH (2002) Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 69:745–749

    PubMed  CAS  Google Scholar 

  43. Shah PJ, Ebmeier KP, Glabus MF et al (1998) Cortical grey matter reductions associated with treatment-resistant chronic unipolar depression. Controlled magnetic resonance imaging study. Br J Psychiatry 172:527–532

    Article  PubMed  CAS  Google Scholar 

  44. Sheline YI, Sanghavi M, Mintun MA et al (1999) Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci 19:5034–5043

    PubMed  CAS  Google Scholar 

  45. Sheline YI, Wang PW, Gado MH et al (1996) Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci USA 93:3908–3913

    PubMed  CAS  Google Scholar 

  46. Sapolsky RM (2001) Depression, antidepressants, and the shrinking hippocampus. Proc Natl Acad Sci USA 98:12320–12322

    PubMed  CAS  Google Scholar 

  47. Harvey PO, Fossati P, Pochon JB et al (2005) Cognitive control and brain resources in major depression: an fMRI study using the n-back task. Neuroimage 26:860–869

    PubMed  Google Scholar 

  48. McEwen BS, Magarinos AM (2001) Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Hum Psychopharmacol 16:S7–S19

    PubMed  CAS  Google Scholar 

  49. Stockmeier CA, Mahajan GJ, Konick LC et al (2004) Cellular changes in the postmortem hippocampus in major depression. Biol Psychiatry 56:640–650

    PubMed  Google Scholar 

  50. Vermetten E, Vythilingam M, Southwick SM et al (2003) Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder. Biol Psychiatry 54:693–702

    PubMed  CAS  Google Scholar 

  51. Gould E, Cameron HA, Daniels DC et al (1992) Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12:3642–3650

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  53. Cameron HA, Gould E (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61:203–209

    PubMed  CAS  Google Scholar 

  54. Wong EY, Herbert J (2004) The corticoid environment: a determining factor for neural progenitors’ survival in the adult hippocampus. Eur J Neurosci 20:2491–2498

    PubMed  Google Scholar 

  55. McEwen BS, Sapolsky RM (1995) Stress and cognitive function. Curr Opin Neurobiol 5:205–216

    PubMed  CAS  Google Scholar 

  56. Woolley CS, Gould E, McEwen BS (1990) Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531:225–231

    PubMed  CAS  Google Scholar 

  57. Czeh B, Michaelis T, Watanabe T et al (2001) Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci USA 98:12796–12801

    PubMed  CAS  Google Scholar 

  58. Fuchs E, Flugge G, Ohl F et al (2001) Psychosocial stress, glucocorticoids, and structural alterations in the tree shrew hippocampus. Physiol Behav 73:285–291

    PubMed  CAS  Google Scholar 

  59. McKittrick CR, Magarinos AM, Blanchard DC et al (2000) Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 36:85–94

    PubMed  CAS  Google Scholar 

  60. Yap JJ, Takase LF, Kochman LJ et al (2006) Repeated brief social defeat episodes in mice: effects on cell proliferation in the dentate gyrus. Behav Brain Res 172:344–350

    PubMed  Google Scholar 

  61. Pham K, Nacher J, Hof PR et al (2003) Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 17:879–886

    PubMed  Google Scholar 

  62. Fornal CA, Stevens J, Barson JR et al (2007) Delayed suppression of hippocampal cell proliferation in rats following inescapable shocks. Brain Res 1130:48–53

    PubMed  CAS  Google Scholar 

  63. Lemaire V, Koehl M, Le Moal M et al (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032–11037

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  65. Lee KJ, Kim SJ, Kim SW et al (2006) Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp Mol Med 38:44–54

    PubMed  CAS  Google Scholar 

  66. Froger N, Palazzo E, Boni C et al (2004) Neurochemical and behavioral alterations in glucocorticoid receptor-impaired transgenic mice after chronic mild stress. J Neurosci 24:2787–2796

    PubMed  CAS  Google Scholar 

  67. Lanfumey L, Paizanis E, Melfort MJ et al (2005) Hypothalamic-pituitary-adrenal (HPA) axis and hippocampal neurogenesis in mice. Eur Neuropharmacol 15:S332–S333

    Google Scholar 

  68. Kempermann G, Gage FH (2002) Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 16:129–136

    PubMed  CAS  Google Scholar 

  69. Pepin MC, Pothier F, Barden N (1992) Impaired type II glucocorticoid-receptor function in mice bearing antisense RNA transgene. Nature 355:725–728

    PubMed  CAS  Google Scholar 

  70. Païzanis E, Renoir T, Hanoun N et al (2006) Potent antidepressant-like effects of agomelatine in a transgenic mouse model of depression. Neuroscience Meeting Planner. Atlanta, GA: Society for Neuroscience, 2006. Online:Program No 290.294/OO251

  71. Eisch AJ, Barrot M, Schad CA et al (2000) Opiates inhibit neurogenesis in the adult rat hippocampus. Proc Natl Acad Sci USA 97:7579–7584

    PubMed  CAS  Google Scholar 

  72. Dominguez-Escriba L, Hernandez-Rabaza V, Soriano-Navarro M et al (2006) Chronic cocaine exposure impairs progenitor proliferation but spares survival and maturation of neural precursors in adult rat dentate gyrus. Eur J Neurosci 24:586–594

    PubMed  CAS  Google Scholar 

  73. Yamaguchi M, Suzuki T, Seki T et al (2005) Decreased cell proliferation in the dentate gyrus of rats after repeated administration of cocaine. Synapse 58:63–71

    PubMed  CAS  Google Scholar 

  74. Abrous DN, Adriani W, Montaron MF et al (2002) Nicotine self-administration impairs hippocampal plasticity. J Neurosci 22:3656–3662

    PubMed  CAS  Google Scholar 

  75. Hernandez-Rabaza V, Dominguez-Escriba L, Barcia JA et al (2006) Binge administration of 3,4-methylenedioxymethamphetamine (“ecstasy”) impairs the survival of neural precursors in adult rat dentate gyrus. Neuropharmacology 51:967–973

    PubMed  CAS  Google Scholar 

  76. Renoir T, Saurini F, Hamon M et al (2006) MDMA-induced long term neurogenesis dysregulation and 5-HT1A autoreceptor supersensitivity in mice. FENS Abstr 3:A165.126

    Google Scholar 

  77. He J, Nixon K, Shetty AK et al. (2005) Chronic alcohol exposure reduces hippocampal neurogenesis and dendritic growth of newborn neurons. Eur J Neurosci 21:2711–2720

    PubMed  Google Scholar 

  78. Herrera DG, Yague AG, Johnsen-Soriano S et al (2003) Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proc Natl Acad Sci USA 100:7919–7924

    PubMed  CAS  Google Scholar 

  79. Nixon K, Crews FT (2002) Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J Neurochem 83:1087–1093

    PubMed  CAS  Google Scholar 

  80. Kochman LJ, dos Santos AA, Fornal CA et al (2006) Despite strong behavioral disruption, Delta9-tetrahydrocannabinol does not affect cell proliferation in the adult mouse dentate gyrus. Brain Res 1113:86–93

    PubMed  CAS  Google Scholar 

  81. Jiang W, Zhang Y, Xiao L et al (2005) Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J Clin Invest 115:3104–3116

    PubMed  CAS  Google Scholar 

  82. Aberg E, Hofstetter CP, Olson L et al (2005) Moderate ethanol consumption increases hippocampal cell proliferation and neurogenesis in the adult mouse. Int J Neuropsychopharmacol 8:557–567

    PubMed  Google Scholar 

  83. Kelai S, Hamon M, Lanfumey L (2005) Effects of chronic alcohol intake on cell proliferation in mouse hippocampus. Alcohol Alcohol Supp 40:i43

    Google Scholar 

  84. Santarelli L, Saxe M, Gross C et al (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805–809

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  86. Chen G, Rajkowska G, Du F et al (2000) Enhancement of hippocampal neurogenesis by lithium. J Neurochem 75:1729–1734

    PubMed  CAS  Google Scholar 

  87. Encinas JM, Vaahtokari A, Enikolopov G (2006) Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci USA 103:8233–8238

    PubMed  CAS  Google Scholar 

  88. Millan MJ (2004) The role of monoamines in the actions of established and “novel” antidepressant agents: a critical review. Eur J Pharmacol 500:371–384

    PubMed  CAS  Google Scholar 

  89. Griebel G, Simiand J, Serradeil-Le Gal C et al (2002) Anxiolytic- and antidepressant-like effects of the non-peptide vasopressin V1b receptor antagonist, SSR149415, suggest an innovative approach for the treatment of stress-related disorders. Proc Natl Acad Sci USA 99:6370–6375

    PubMed  CAS  Google Scholar 

  90. Griebel G, Simiand J, Steinberg R et al (2002) 4-(2-Chloro-4-methoxy-5-methylphenyl)-N-[(1S)-2-cyclopropyl-1-(3-fluoro-4-methylphenyl)ethyl]5-methyl-N-(2-propynyl)-1, 3-thiazol-2-amine hydrochloride (SSR125543A), a potent and selective corticotrophin-releasing factor(1) receptor antagonist. II. Characterization in rodent models of stress-related disorders. J Pharmacol Exp Ther 301:333–345

    PubMed  CAS  Google Scholar 

  91. Alonso R, Griebel G, Pavone G et al (2004) Blockade of CRF(1) or V(1b) receptors reverses stress-induced suppression of neurogenesis in a mouse model of depression. Mol Psychiatry 9:278–286

    PubMed  CAS  Google Scholar 

  92. Rupniak NM (2002) Elucidating the antidepressant actions of substance P (NK1 receptor) antagonists. Curr Opin Investig Drugs 3:257–261

    PubMed  CAS  Google Scholar 

  93. Morcuende S, Gadd CA, Peters M et al (2003) Increased neurogenesis and brain-derived neurotrophic factor in neurokinin-1 receptor gene knockout mice. Eur J Neurosci 18:1828–1836

    PubMed  Google Scholar 

  94. Banasr M, Soumier A, Hery M et al (2006) Agomelatine, a new antidepressant, induces regional changes in hippocampal neurogenesis. Biol Psychiatry 59:1087–1096

    PubMed  CAS  Google Scholar 

  95. Morley-Fletcher S, Mairesse J, Mocaer E et al (2003) Chronic treatment with agomelatine increases hippocampal cell proliferation in prenatally stressed rats. Neurosci Abst 506.20

  96. Zhu LL, Zhao T, Li HS et al (2005) Neurogenesis in the adult rat brain after intermittent hypoxia. Brain Res 1055:1–6

    PubMed  CAS  Google Scholar 

  97. Bingham B, Liu D, Wood A et al (2005) Ischemia-stimulated neurogenesis is regulated by proliferation, migration, differentiation and caspase activation of hippocampal precursor cells. Brain Res 1058:167–177

    PubMed  CAS  Google Scholar 

  98. Kluska MM, Witte OW, Bolz J et al (2005) Neurogenesis in the adult dentate gyrus after cortical infarcts: effects of infarct location, N-methyl-d-aspartate receptor blockade and anti-inflammatory treatment. Neuroscience 135:723–735

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  100. Meshi D, Drew MR, Saxe M et al (2006) Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci 9:729–731

    PubMed  CAS  Google Scholar 

  101. Giedke H, Schwarzler F (2002) Therapeutic use of sleep deprivation in depression. Sleep Med Rev 6:361–377

    PubMed  Google Scholar 

  102. Tung A, Takase L, Fornal C et al (2005) Effects of sleep deprivation and recovery sleep upon cell proliferation in adult rat dentate gyrus. Neuroscience 134:721–723

    PubMed  CAS  Google Scholar 

  103. Guzman-Marin R, Suntsova N, Methippara M et al (2005) Sleep deprivation suppresses neurogenesis in the adult hippocampus of rats. Eur J Neurosci 22:2111–2116

    PubMed  Google Scholar 

  104. Smith MA, Makino S, Kvetnansky R et al (1995) Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 15:1768–1777

    PubMed  CAS  Google Scholar 

  105. McAllister AK, Lo DC, Katz LC (1995) Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15:791–803

    PubMed  CAS  Google Scholar 

  106. Franklin TB, Perrot-Sinal TS (2006) Sex and ovarian steroids modulate brain-derived neurotrophic factor (BDNF) protein levels in rat hippocampus under stressful and non-stressful conditions. Psychoneuroendocrinology 31:38–48

    PubMed  CAS  Google Scholar 

  107. Gronli J, Bramham C, Murison R et al (2006) Chronic mild stress inhibits BDNF protein expression and CREB activation in the dentate gyrus but not in the hippocampus proper. Pharmacol Biochem Behav 85:842–849

    PubMed  CAS  Google Scholar 

  108. Tao X, Finkbeiner S, Arnold DB et al (1998) Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709–726

    PubMed  CAS  Google Scholar 

  109. Alfonso J, Frick LR, Silberman DM et al (2006) Regulation of hippocampal gene expression is conserved in two species subjected to different stressors and antidepressant treatments. Biol Psychiatry 59:244–251

    PubMed  CAS  Google Scholar 

  110. Nibuya M, Nestler EJ, Duman RS (1996) Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J Neurosci 16:2365–2372

    PubMed  CAS  Google Scholar 

  111. Dowlatshahi D, MacQueen GM, Wang JF et al (1998) Increased temporal cortex CREB concentrations and antidepressant treatment in major depression. Lancet 352:1754–1755

    PubMed  CAS  Google Scholar 

  112. Pluzarev O, Pandey SC (2004) Modulation of CREB expression and phosphorylation in the rat nucleus accumbens during nicotine exposure and withdrawal. J Neurosci Res 77:884–891

    PubMed  CAS  Google Scholar 

  113. Nibuya M, Morinobu S, Duman RS (1995) Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 15:7539–7547

    PubMed  CAS  Google Scholar 

  114. Shirayama Y, Chen AC, Nakagawa S et al (2002) Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci 22:3251–3261

    PubMed  CAS  Google Scholar 

  115. Siuciak JA, Lewis DR, Wiegand SJ et al (1997) Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol Biochem Behav 56:131–137

    PubMed  CAS  Google Scholar 

  116. Hayley S, Poulter MO, Merali Z et al (2005) The pathogenesis of clinical depression: stressor- and cytokine-induced alterations of neuroplasticity. Neuroscience 135:659–678

    PubMed  CAS  Google Scholar 

  117. Kaneko N, Kudo K, Mabuchi T et al (2006) Suppression of cell proliferation by interferon-alpha through interleukin-1 production in adult rat dentate gyrus. Neuropsychopharmacology 31:2619–2626

    PubMed  CAS  Google Scholar 

  118. Beck RD Jr, Wasserfall C, Ha GK et al (2005) Changes in hippocampal IL-15, related cytokines, and neurogenesis in IL-2 deficient mice. Brain Res 1041:223–230

    PubMed  CAS  Google Scholar 

  119. Kim SH, Won SJ, Mao XO et al (2006) Role for neuronal nitric-oxide synthase in cannabinoid-induced neurogenesis. J Pharmacol Exp Ther 319:150–154

    PubMed  CAS  Google Scholar 

  120. Reif A, Schmitt A, Fritzen S et al (2004) Differential effect of endothelial nitric oxide synthase (NOS-III) on the regulation of adult neurogenesis and behaviour. Eur J Neurosci 20:885–895

    PubMed  Google Scholar 

  121. Snyder SH, Ferris CD (2000) Novel neurotransmitters and their neuropsychiatric relevance. Am J Psychiatry 157:1738–1751

    PubMed  CAS  Google Scholar 

  122. Bredt DS, Snyder SH (1994) Nitric oxide: a physiologic messenger molecule. Annu Rev Biochem 63:175–195

    PubMed  CAS  Google Scholar 

  123. Zhu DY, Liu SH, Sun HS et al (2003) Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus. J Neurosci 23:223–229

    PubMed  CAS  Google Scholar 

  124. Packer MA, Stasiv Y, Benraiss A et al (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci USA 100:9566–9571

    PubMed  CAS  Google Scholar 

  125. Pinnock SB, Balendra R, Chan M et al (2007) Interactions between nitric oxide and corticosterone in the regulation of progenitor cell proliferation in the dentate gyrus of the adult rat. Neuropsychopharmacology 32:493–504

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research has been supported by grants from INSERM, ATC Alcool INSERM (A02229DS), IREB (2006/11), and the European Community (QLG3-CT-2002-00809).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laurence Lanfumey.

Additional information

Special issue dedicated to Dr. Moussa Youdim.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Paizanis, E., Kelaï, S., Renoir, T. et al. Life-Long Hippocampal Neurogenesis: Environmental, Pharmacological and Neurochemical Modulations. Neurochem Res 32, 1762–1771 (2007). https://doi.org/10.1007/s11064-007-9330-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-007-9330-0

Keywords

Navigation