Differential effects of stress and glucocorticoids on adult neurogenesis

Current Topics in Behavioral Neurosciences

Volumn 15, Issue , 2013, Pages 139-164

  Schoenfeld, Timothy J ^a   Gould, Elizabeth ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

Anxiety; Dentate gyrus; Learning; Neurogenesis; Physical activity; Reward; Sexual experience; Stress

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTEROID; CYTOKINE; GLUCOCORTICOID; NEUROPEPTIDE; NEUROPEPTIDE Y; NEUROTROPHIN; OXYTOCIN; SOMATOMEDIN C; VASCULOTROPIN;

ANXIETY; ARTICLE; BRAIN FUNCTION; CELL PROLIFERATION; DENTATE GYRUS; HIPPOCAMPUS; HUMAN; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURONAL GROWTH; NEUROTRANSMITTER RELEASE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEXUAL BEHAVIOR; STIMULATION; STRESS; ANIMAL; CYTOLOGY; MAMMAL; MENTAL STRESS; METABOLISM; PHYSIOLOGY; REWARD;

ANIMALS; DENTATE GYRUS; GLUCOCORTICOIDS; MAMMALS; NEUROGENESIS; REWARD; STRESS, PSYCHOLOGICAL;

EID: 84888263543     PISSN: 18663370     EISSN: 18663389     Source Type: Book Series    
DOI: 10.1007/7854_2012_233     Document Type: Article

References (230)

1. Aberg MA, Aberg ND, Hedbacker H, Oscarsson J, Eriksson PS (2000) Peripheral infusion of IGF-1 selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 20: 2896-2903
2. Aguilera G, Rabadan-Diehl C (2000) Vasopressinergic regulation of the hypothalamic-pituitaryadrenal axis: implications for stress adaptation. Regul Pept 96: 23-29
3. Alonso R, Griebel G, Pavone G, Stemmelin J, Le Fur G, Soubrié P (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
4. Aztiria E, Capodieci G, Arancio L, Leanza G (2007) Extensive training in a maze task reduces neurogenesis in the adult rat dentate gyrus probably as a result of stress. Neurosci Lett 416: 133-137
5. Bain MJ, Dwyer SM, Rusak B (2004) Restraint stress affects hippocampal cell proliferation differently in rats and mice. Neurosci Lett 368: 7-10
6. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, Zhang WN, Pothuizen HH, Feldon J (2004) Regional dissociations within the hippocampus-memory and anxiety. Neurosci Biobehav Rev 28: 273-283
7. Barha CK, Brummelte S, Lieblich SE, Galea LA (2011) Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus 21: 1216-1227
8. Belke TW, Wagner JP (2005) The reinforcing property and the rewarding aftereffect of wheel running in rats: a combination of two paradigms. Behav Processes 68: 165-172
9. Ben Menachem-Zidon O, Goshen I, Kreisel T, Ben Menahem Y, Reinhartz E, Ben Hur T, Yirmiya R (2008) Intrahippocampal transplantation of transgenic neural precursor cells overexpressing interleukin-1 antagonist blocks chronic isolation-induced impairment in memory and neurogenesis. Neuropsychopharmacology 33: 2251-2262
10. Benaroya-Milshtein N, Hollander N, Apter A, Yaniv I, Kukulansky T, Raz N, Haberman Y, Halpert H, Pick CG, Hollander N (2004) Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur J Neurosci 20: 1341-1347
11. Bernton EW, Beach JE, Holaday JW, Smallridge RC, Fein HG (1987) Release of multiple hormones by a direct action of interleukin-1 on pituitary cells. Science 238: 519-521
12. Bessa JM, Ferreira D, Melo I, Marques F, Cerqueira JJ, Palha JA, Almeida OF, Sousa N (2009) The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol Psychiatry 14: 764-773
13. Bjornebekk A, Mathe AA, Brene S (2006) Running has differential effects on NPY, opiates, and cell proliferation in an animal model of depression and controls. Neuropsychopharmacology 31: 256-264
14. Bolteus AJ, Bordey A (2004) GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci 24: 7623-7631
15. Bonilla-Jaime H, Vázquez-Palacios G, Arteaga-Silva M, Retana-Márquez S (2006) Hormonal responses to different sexually related conditions in male rats. Horm Behav 49: 376-382
16. Bowen KK, Dempsey RJ, Vemuganti R (2011) Adult interleukin-6 knockout mice show compromised neurogenesis. NeuroReport 22: 126-130
17. 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: 37-46
18. 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: 2042-2046
19. Brummelte S, Galea LA (2010a) Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats. Neuroscience 168: 680-690
20. Brummelte S, Galea LA (2010b) Chronic corticosterone during pregnancy and postpartum affects maternal care, cell proliferation and depressive-like behavior in the dam. Horm Behav 58: 769-779
21. Buynitsky T, Mostofsky DI (2009) Restraint stress in biobehavioral research: recent developments. Neurosci Biobehav Rev 33: 1089-1098
22. Cameron HA, Gould E (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61: 203-209
23. Cameron HA, McKay RD (1999) Restoring production of hippocampal neurons in old age. Nat Neurosci 2: 894-897
24. 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
25. Cameron HA, Woolley CS, Gould E (1993a) Adrenal steroid receptor immunoreactivity in cells born in the adult rat dentate gyrus. Brain Res 611: 342-346
26. Cameron HA, Woolley CS, McEwen BS, Gould E (1993b) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56: 337-344
27. 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
28. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, Young D, During MJ (2004) VEGF links hippocampal activity with neurogenesis, learning, and memory. Nat Genet 36: 827-835
29. Carro E, Nunez A, Busiguina S, Torres-Aleman I (2000) Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 20: 2926-2933
30. Carvajal CC, Vercauteren F, Dumont Y, Michalkiewicz M, Quirion R (2004) Aged neuropeptide Y transgenic rats are resistant to acute stress but maintain spatial and non-spatial learning. Behav Brain Res 153: 471-480
31. Castilla-Ortega E, Pedraza C, Estivill-Torrus G, Santin LJ (2011) When is adult hippocampal neurogenesis necessary for learning? Evidence from animal research. Rev Neurosci 22: 267-283
32. Christian KM, Miracle AD, Wellman CL, Nakazawa K (2011) Chronic stress-induced hippocampal dendritic retraction requires CA3 NMDA receptors. Neuroscience 174: 26-36
33. Christie BR, Cameron HA (2006) Neurogenesis in the adult hippocampus. Hippocampus 16: 199-207
34. Clark PJ, Kohman RA, Miller DS, Bhattacharya TK, Brzezinska WJ, Rhodes JS (2011) Genetic influences on exercise-induced adult hippocampal neurogenesis across 12 divergent mouse strains. Genes Brain Behav 10: 345-353
35. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325: 210-213
36. Cohen H, Liu T, Kozlovsky N, Kaplan Z, Zohar J, Mathe AA (2012) The neuropeptide Y (NPY)-ergic system is associated with behavioral resilience to stress exposure in an animal model of post-traumatic stress disorder. Neuropsychopharmacology 37: 350-363
37. Conrad CD (2006) What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus? Behav Cogn Neurosci Rev 5: 41-60
38. Conrad CD (2010) A critical review of chronic stress effects on spatial learning and memory. Prog Neuropsychopharmacol Biol Psychiatry 34: 742-755
39. Creer DJ, Romberg C, Saksida LM, van Praag H, Bussey TJ (2010) Running enhances spatial pattern separation in mice. Proc Natl Acad Sci U S A 107: 2367-2372
40. Crews FT, Nixon K, Wilkie ME (2004) Exercise reverses ethanol inhibition of neural stem cell proliferation. Alcohol 33: 63-71
41. Czeh B, Michaelis T, Watanabe T, Frahm J, de Biurrun G, van Kampen M, Bartolomucci A, Fuchs E (2001) Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci U S A 98: 12796-12801
42. Czeh B, Welt T, Fischer AK, Erhardt A, Schmitt W, Müeller MB, Toschi N, Fuchs E, Keck ME (2002) Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol Psychiatry 52: 1057-1065
43. Czeh B, Muller-Keuker JI, Rygula R, Abumaria N, Hiemke C, Domenici E, Fuchs E (2007) Chronic social stress inhibits cell proliferation in the adult medial prefrontal cortex: hemispheric asymmetry and reversal by fluoxetine treatment. Neuropsychopharmacology 32: 1490-1503
44. Dagyte G, Van der Zee EA, Postema F, Luiten PG, Den Boer JA, Trentani A, Meerlo P (2009) Chronic but not acute foot-shock stress leads to temporary suppression of cell proliferation in rat hippocampus. Neuroscience 162: 904-913
45. Dagyte G, Crescente I, Postema F, Seguin L, Gabriel C, Mocaer E, Boer JA, Koolhaas JM (2011) Agomelatine reverses the decrease in hippocampal cell survival induced by chronic mild stress. Behav Brain Res 218: 121-128
46. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460: 563-572
47. de Groote L, Linthorst AC (2007) Exposure to novelty and forced swimming evoke stressordependent changes in extracellular GABA in the rat hippocampus. Neuroscience 148: 794-805
48. De Kloet ER, Vreugdenhil E, Oitzl MS, Joëls M (1998) Brain corticosteroid receptor balance in health and disease. Endocr Rev 19: 269-301
49. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC (2004) Excitationneurogenesis coupling in adult neural stem/progenitor cells. Neuron 42: 535-552
50. Deng W, Aimone JB, Gage FH (2010) New Neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11: 339-350
51. Droste SK, Gesing A, Ulbricht S, Muller MB, Linthorst AC, Reul JM (2003) Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis. Endocrinology 144: 3012-3023
52. Dupret D, Fabre A, Dobrossy MD, Panatier A, Rodriguez JJ, Lamarque S, Lemaire V, Oliet SH, Piazza PV, Abrous DN (2007) Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol 5: e214
53. 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: 29-39
54. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 100: 13632-13637
55. Elizalde N, Garcia-Garcia AL, Totterdell S, Gendive N, Venzala E, Ramirez MJ, Del Rio J, Tordera RM (2010) Sustained stress-induced changes in mice as a model for chronic depression. Psychopharmacology 210: 393-406
56. Epp JR, Haack AK, Galea LA (2010) Task difficulty in the Morris water task influences the survival of new neurons in the dentate gyrus. Hippocampus 20: 866-876
57. Epp JR, Scott NA, Galea LA (2011) Strain differences in neurogenesis and activation of new neurons in the dentate gyrus in response to spatial learning. Neuroscience 172: 342-354
58. Ergorul C, Eichenbaum H (2004) The hippocampus and memory for ''what, '' ''where, '' and ''when''. Learn Mem 11: 397-405
59. Espósito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25: 10074-10086
60. Everitt BJ, Fray P, Kostarczyk E, Taylor S, Stacey P (1987) Studies of instrumental behavior with sexual reinforcement in male rats (Rattus norvegicus): I. Control by brief visual stimuli paired with a receptive female. J Comp Psychol 101: 395-406
61. 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: 2803-2812
62. Falconer EM, Galea LA (2003) Sex differences in cell proliferation, cell death, and defensive behavior following acute predator odor stress in adult rats. Brain Res 975: 22-36
63. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65: 7-19
64. Farioli-Vecchioli S, Saraulli D, Costanzi M, Pacioni S, Cina I, Aceti M, Micheli L, Bacci A, Cestari V, Tirone F (2008) The timing of differentiation of adult hippocampal neurons is crucial for spatial memory. PLoS ONE 6: e246
65. Ferragud A, Haro A, Sylvain A, Velazquez-Sanchez C, Hernandez-Rabaza V, Canales JJ (2010) Enhanced habit-based learning and decreased neurogenesis in the adult hippocampus in a murine model of chronic social stress. Behav Brain Res 210: 134-139
66. Fischer AK, von Rosenstiel P, Fuchs E, Goula D, Almeida OF, Czeh B (2002) The prototypic mineralocorticoid receptor agonist aldosterone influences neurogenesis in the dentate gyrus of the adrenalectomized rat. Brain Res 947: 290-293
67. Foy MR, Stanton ME, Levine S, Thompson RF (1987) Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav Neural Biol 48: 138-149
68. Frechette M, Rennie K, Pappas BA (2009) Developmental forebrain cholinergic lesion and environmental enrichment: behaviour, CA1 cytoarchitecture and neurogenesis. Brain Res 1252: 172-182
69. Garcia A, Steiner B, Kronenberg G, Bick-Sandler 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: 363-371
70. Garthe A, Behr J, Kempermann G (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE 4: e5464
71. Gascon E, Dayer AG, Sauvain MO, Potter G, Jenny B, De Roo M, Zgraggen E, Demaurex N, Muller D, Kiss JZ (2006) GABA regulates dendritic growth by stabilizing lamellipodia in newly generated interneurons of the olfactory bulb. J Neurosci 26: 12956-12966
72. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439: 589-593
73. Ge S, Yang CH, Hsu KS, Ming GL, Song H (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54: 559-566
74. Golub Y, Kaltwasser SF, Mauch CP, Herman L, Schmidt U, Holsboer F, Czisch M, Wotjak CT (2011) Reduced hippocampus volume in the mouse model of posttraumatic stress disorder. J Psychiatr Res 45: 650-659
75. Goshen I, Kreisel T, Ben-Menachem-Zidon O, Licht T, Weidenfeld J, Ben-Hur T, Yirmiya R (2008) Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol Psychiatry 13: 717-728
76. Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8: 481-488
77. Gould E, Tanapat P (1997) Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 80: 427-436
78. Gould E, Woolley CS, McEwen BS (1990) Short-term glucocorticoid manipulations affect neuronal morphology and survival in the adult dentate gyrus. Neuroscience 37: 367-375
79. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS (1992) Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12: 3642-3650
80. 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: 2492-2498
81. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci U S A 95: 3168-3171
82. Gould E, Tanapat P, Hastings NB, Shors TJ (1999) Neurogenesis in adulthood: a possible role in learning. Trends Cogn Sci 3: 186-192
83. Grønli J, Fiske E, Murison R, Bjorvatn B, Sorensen E, Ursin R, Portas CM (2007) Extracellular levels of serotonin and GABA in the hippocampus after chronic mild stress in rats: a microdialysis study in an animal model of depression. Behav Brain Res 181: 42-51
84. Guo J, Yu C, Liu F, Feng R, Wang H, Meng Y, Li Z, Ju G, Wang J (2010) Impaired neural stem/progenitor cell proliferation in streptozotocin-induced and spontaneous diabetic mice. Neurosci Res 68: 329-336
85. Hastings NB, Gould E (1999) Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413: 146-154
86. 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: 1304-1314
87. Herman JP, Mueller NK (2006) Role of the ventral subiculum in stress integration. Behav Brain Res 174: 215-224
88. Herman JP, Schäfer MK, Young EA, Thompson R, Douglass J, Akil H, Watson SJ (1989) Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamopituitary-adrenocortical axis. J Neurosci 9: 3072-3082
89. Herman JP, Cullinan WE, Morano MI, Akil H, Watson SJ (1995) Contribution of the ventral subiculum to inhibitory regulation of the hypothalamo-pituitary-adrenocortical axis. Neuroendocrinol 7: 475-482
90. Hill MN, Kambo JS, Sun JC, Gorzalka BB, Galea LA (2006) Endocannabinoids modulate stressinduced suppression of hippocampal cell proliferation and activation of defensive behaviours. Eur J Neurosci 24: 1845-1849
91. Hill LE, Droste SK, Nutt DJ, Linthorst AC, Reul JM (2010) Voluntary exercise alters GABA(A) receptor subunit and glutamic acid decarboxylase-67 gene expression in the rat forebrain. J Psychopharmacol 24: 745-756
92. Hitoshi S, Maruta N, Higashi M, Kumar A, Kato N, Ikenaka K (2007) Antidepressant drugs reverse the loss of adult neural stem cells following chronic stress. J Neurosci Res 85: 3574-3585
93. Hoglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH, Caille I, Hirsch EC (2004) Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 7: 726-735
94. Holsboer F (1999) The rationale for corticotropin-releasing hormone receptor (CRH-R) antagonists to treat depression and anxiety. J Psychiatr Res 33: 181-214
95. Howell OW, Doyle K, Goodman JH, Scharfman HE, Herzog H, Pringle A, Beck-Sickinger AG, Gray WP (2005) Neuropeptide Y stimulates neuronal precursor proliferation in the post-natal and adult dentate gyrus. J Neurochem 93: 560-570
96. Howell OW, Scharfman HE, Herzog H, Sundstrom LE, Beck-Sickinger A, Gray WP (2003) Neuropeptide Y is neuroproliferative for post-natal hippocampal precursor cells. J Neurochem 86(3): 646-659
97. Howland JG, Wang YT (2008) Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog Brain Res 169: 145-158
98. Hundt AG, Premack D (1963) Running as both a positive and negative reinforcer. Science 142: 1087-1088
99. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integration of the adult forebrain. Nat Neurosci 11: 1153-1161
100. Iosif RE, Ekdahl CT, Ahlenius H, Pronk CJ, Bonde S, Kokaia Z, Jacobsen SE, Lindvall O (2006) Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci 26: 9703-9712
101. Jacobson L, Sapolsky R (1991) The role of hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endo Rev 12: 118-134
102. Jessberger S, Zhao C, Toni N, Clemenson GD, Li Y, Gage FH (2007) Seizure-associated aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J Neurosci 27: 9400-9407
103. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, Lie DC, Squire LR, Gage FH (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16: 147-154
104. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci U S A 99: 11946-11950
105. Kambo JS, Galea LA (2006) Activation levels of androgens influence risk assessment behaviour but do not influence stress-induced suppression in hippocampal cell proliferation in adult male rats. Behav Brain Res 175: 263-270
106. 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
107. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115: 97-105
108. Kee N, Teixeira CM, Wang AH, FranklandPW(2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10: 355-362
109. Kempermann G, Gage FH (2002) Genetic influence on phenotypic differentiation in adult hippocampal neurogenesis. Brain Res Dev Brain Res 134: 1-12
110. 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: 135-143
111. Kim JB, Ju JY, Kim JH, Kim TY, Yang BH, Lee YS, Son H (2004) Dexamethasone inhibits proliferation of adult hippocampal neurogenesis in vivo and in vitro. Brain Res 1027: 1-10
112. Klaus F, Hauser T, Slomianka L, Lipp HP, Amrein I (2009) A reward increases running-wheel performance without changing cell proliferation, neuronal differentiation or cell death in the dentate gyrus of C57BL/6 mice. Brain Res 204: 175-181
113. Koo JW, Duman RS (2008) IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci U S A 105: 751-756
114. Kotani S, Yamauchi T, Teramoto T, Ogura H (2006) Pharmacological evidence of cholinergic involvement in adult hippocampal neurogenesis in rats. Neuroscience 142: 505-514
115. 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
116. Lagace DC, Fischer SJ, Eisch AJ (2007) Gender and endogenous levels of estradiol do not influence adult hippocampal neurogenesis in mice. Hippocampus 17: 175-180
117. Lagace DC, Donovan MH, DeCarolis NA, Farnbauch LA, Malhotra S, Berton O, Nestler EJ, Krishnan V, Eisch AJ (2010) Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance. Proc Natl Acad Sci U S A 107: 4436-4441
118. Lau WM, Qiu G, Helmeste DM, Lee TM, Tang SW, So KF, Tang SW (2007) Corticosteroid decreases subventricular zone cell proliferation, which could be reversed by paroxetine. Restor Neurol Neurosci 25: 17-23
119. Lee KJ, Kim SJ, Kim SW, Choi SH, Shin YC, Park SH, Moon BH, Cho E, Lee MS, Choi SH, Chun BG, Shin KH (2006) Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp Mol Med 38: 44-54
120. Leuner B, Caponiti JM, Gould E (2012) Oxytocin stimulates adult neurogenesis even under conditions of stress and elevated glucocorticoids. Hippocampus 22: 861-868
121. Leuner B, Gould E (2010) Structural plasticity and hippocampal function. Annu Rev Psychol 61: 111-140
122. Leuner B, Mendolia-Loffredo S, Kozorovitskiy Y, Samburg D, Gould E, Shors TJ (2004) Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J Neurosci 24: 7477-7481
123. Leuner B, Gould E, Shors TJ (2006) Is there a link between adult neurogenesis and learning? Hippocampus 16: 216-224
124. Leuner B, Kozorovitskiy Y, Gross CG, Gould E (2007) Diminished adult neurogenesis in the marmoset brain precedes old age. Proc Natl Acad Sci U S A 104: 17169-17173
125. Leuner B, Glasper ER, Gould E (2010) Sexual experience promotes adult neurogenesis in the hippocampus despite an initial elevation in stress hormones. PLoS ONE 5: e11597
126. Lewis DA, Levitt P (2002) Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 25: 409-432
127. Liu X, Wang Q, Haydar TF, Bordey A (2005) Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat Neurosci 8: 1179-1187
128. Lledo PM, Saghatelyan A (2005) Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci 28: 248-254
129. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145-1148
130. Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11: 173-189
131. Madsen TM, Kristjansen PE, Bolwig TG, Wörtwein G (2003) Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119: 635-642
132. Maekawa M, Namba T, Suzuki E, Yuasa S, Kohsaka S, Uchino S (2009) NMDA receptor antagonist memantine promotes cell proliferation and production of mature granule neurons in the adult hippocampus. Neurosci Res 63: 259-266
133. Magariños AM, McEwen BS, Flugge G, Fuchs E (1996) Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 16: 3534-3540
134. Magavi SS, Mitchell BD, Szentirmai O, Carter BS, Macklis JD (2005) Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J Neurosci 25: 10729-10739
135. Maggio N, Segal M (2007) Striking variations in corticosteroid modulation of long-term potentiation along the septotemporal axis of the hippocampus. J Neurosci 27: 5757-5765
136. Makatsori A, Duncko R, Schwendt M, Moncek F, Johansson BB, Jezova D (2003) Voluntary wheel running modulates glutamate receptor subunit gene expression and stress hormone release in Lewis rats. Psychoneuroendocrinology 28: 702-714
137. Malberg JE, Duman RS (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28: 1562-1571
138. Martisova E, Solas M, Horrillo I, Ortega JE, Meana JJ, Tordera RM, Ramirez MJ (2012) Long lasting effects of early-life stress on glutamatergic/GABAergic circuitry in the rat hippocampus. Neuropharmacology 62: 1944-1953
139. McEwen BS (2002) The end of stress as we known it. Dana Press, Washington, DC
140. McKittrick CR, Magarinos AM, Blanchard DC, Blanchard RJ, McEwen BS, Sakai RR (2000) Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 36: 85-94
141. Mineur YS, Belzung C, Crusio WE (2007) Functional implications of decreases in neurogenesis following chronic mild stress in mice. Neuroscience 150: 251-259
142. Mirescu C, Peters JD, Gould E (2004) Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 7: 841-846
143. Mitra R, Sundlass K, Parker KJ, Schatzberg AF, Lyons DM (2006) Social stress-related behavior affects hippocampal cell proliferation in mice. Physiol Behav 89: 123-127
144. Monje ML, Toda H, Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765
145. Morimoto M, Morita N, Ozawa H, Yokoyama K, Kawata M (1996) Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci Res 26: 235-269
146. Moser E, Moser MB, Andersen P (1993) Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci 13: 3916-3925
147. Mu Y, Zhao C, Gage FH (2011) Dopaminergic modulation of cortical inputs during maturation of adult-born dentate granule cells. J Neurosci 31: 4113-4123
148. Nacher J, Alonso-Llosa G, Rosell DR, McEwen BS (2003) NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol Aging 24: 273-284
149. O'Reilly RC, McClelland JL (1994) Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 4: 661-682
150. Oomen CA, Mayer JL, de Kloet ER, Joels M, Lucassen PJ (2007) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur J Neurosci 26: 3395-3401
151. Overstreet Wadiche L, Bromberg DA, Bensen AL, Westbrook GL (2005) GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 94: 4528-4532
152. Park JH, Enikolopov G (2010) Transient elevation of adult hippocampal neurogenesis after dopamine depletion. Exp Neurol 222: 267-276
153. Pathania M, Yan LD, Bordey AA (2010) A symphony of signals conducts early and late stages of adult neurogenesis. Neuropharmacology 58: 865-876
154. Pavlides C, Nivon LG, McEwen BS (2002) Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 12: 245-257
155. Petreanu L, Alvarez-Boylla A (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22: 6106-6113
156. Pham K, Nacher J, Hof PF, McEwen BS (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. Plane JM, Whitney JT, Schallert T, Parent JM (2008) Retinoic acid and environmental enrichment alter subventricular zone and striatal neurogenesis after stroke. Exp Neurol 214: 125-134
158. Platel JC, Dave KA, Bordey A (2008) Control of neuroblast production and migration by converging GABA and glutamate signals in the postnatal forebrain. J Physiol 586: 3739-3743
159. Qiu G, Helmeste DM, Samaranayake AN, Lau WM, Lee TM, Tang SW, So KF (2007) Modulation of the suppressive effect of corticosterone on adult rat hippocampal cell proliferation by paroxetine. Neurosci Bull 23: 131-136
160. Radley JJ, Jacobs BL (2002) 5-HT1A receptor antagonist administration decreases cell proliferation in the dentate gyrus. Brain Res 955: 264-267
161. Ramirez-Amaya V, Marrone DF, Gage FH, Worley PF, Barnes CA (2006) Integration of new neurons into functional neural networks. J Neurosci 26: 12237-12241
162. Reul JM, de Kloet ER (1985) Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117: 2505-2511
163. Ribak CE, Korn MJ, Shan Z, Obenaus A (2004) Dendritic growth cones and recurrent basal dendrites are typical features of newly generated dentate granule cells in the adult hippocampus. Brain Res 1000: 195-199
164. Rosenbrock H, Koros E, Bloching A, Podhorna J, Borsini F (2005) Effect of chronic intermittent restraint stress on hippocampal expression of marker proteins for synaptic plasticity and progenitor cell proliferation in rats. Brain Res 1040: 55-63
165. Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F, Fabbri ME, Tessarollo L, Maffei L, Berardi N, Caleo M (2006) Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 24: 1850-1856
166. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsly A, Hen R (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472: 466-470
167. 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
168. Sapolsky RM (2004) Why zebras don't get ulcers. W. H. Freeman and Company, New York
169. Saxe MD, Battaglia F, Wang JW, Malleret G, David DJ, Monckton JE, Garcia AD, Sofroniew MV, Kandel ER, Santarelli L, Hen R, Drew MR (2006) Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci U S A 103: 17501-17506
170. Schauwecker PE (2006) Genetic influence on neurogenesis in the dentate gyrus of two strains of adult mice. Brain Res 1120: 83-92
171. Seki T, Arai Y (1995) Age-related production of new granule cells in the adult dentate gyrus. NeuroReport 6: 2479-2482
172. Shors TJ, Gallegos RA, Breindl A (1997) Transient and persistent consequences of acute stress on long-term potentiation (LTP), synaptic efficacy, theta rhythms and bursts in area CA1 of the hippocampus. Synapse 26: 209-217
173. 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: 372-376
174. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy T, Gould E (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12: 578-584
175. Silva R, Mesquita AR, Bessa J, Sousa JC, Sotiropoulos I, Leao P, Almeida OF, Sousa N (2008) Lithium blocks stress-induced changes in depressive-like behavior and hippocampal cell fate: the role of glycogen-synthase-kinase-3beta. Neuroscience 152: 656-669
176. Simon M, Czeh B, Fuchs E (2005) Age-dependent susceptibility of adult hippocampal cell proliferation to chronic psychosocial stress. Brain Res 1049: 244-248
177. Sloviter RS, Valiquette G, Abrams GM, Ronk EC, Solias AL, Paul LA, Neubort S (1989) Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science 243: 535-538
178. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130: 843-852
179. Snyder JS, Choe JS, Clifford MA, Jeurling SI, Hurley P, Brown A, Kamhi JF, Cameron HA (2009a) Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 29: 14484-14495
180. Snyder JS, Glover LR, Sanzone KM, Kamhi JF, Cameron HA (2009b) The effects of exercise and stress on the survival and maturation of adult-generated granule cells. Hippocampus 19: 898-906
181. Snyder JS, Radik R, Wojtowicz JM, Cameron HA (2009c) Anatomical gradients of adult neurogenesis and activity: young neurons in the ventral dentate gyrus are activated by water maze training. Hippocampus 19: 360-370
182. Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA (2011) Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476: 458-461
183. Snyder JS, Clifford MA, Jeurling SI, Cameron HA (2012) Complementary activation of hippocampal-cortical subregions and immature neurons following chronic training in single and multiple context versions of the water maze. Behav Brain Res 227: 330-339
184. Steiner B, Kronenberg G, Jessberger S, Brandt MD, Reuter K, Kempermann G (2004) Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46: 41-52
185. Stone SS, Teixeira CM, Devito LM, Zaslavsky K, Josselyn SA, Lozano AM, Frankland PW (2011) Stimulation of entorhinal cortex promotes adult neurogenesis and facilitates spatial memory. J Neurosci 31: 13469-13484
186. Stranahan AM, Khalil D, Gould E (2006) Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 9: 526-533
187. Sun Y, Jin K, Childs JT, Xie L, Mao XO, Greenberg DA (2006) Vascular endothelial growth factor-B (VEGFB) stimulates neurogenesis: evidence from knockout mice and growth factor administration. Dev Biol 289: 329-335
188. Sun B, Halabisky B, Zhou Y, Palop JJ, Yu G, Mucke L, Gan L (2009) Imbalance between GABAergic and glutamatergic transmission impairs adult neurogenesis in an animal model of Alzheimer's disease. Cell Stem Cell 5: 624-633
189. Surget A, Saxe M, Leman S, Ibarguen-Vargas Y, Chalon S, Griebel G, Hen R, Belzung C (2008) Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol Psychiatry 64: 293-301
190. Surget A, Tanti A, Leonardo ED, Laugeray A, Rainer Q, Touma C, Palme R, Griebel G, Ibarguen-Vargas Y, Hen R, Belzung C (2011) Antidepressants recruit new neurons to improve stress response regulation. Mol Psychiatry 16: 1177-1188
191. Takahashi T, Zhu Y, Hata T, Shimizu-Okabe C, Suzuki K, Nakahara D (2009) Intracranial selfstimulation enhances neurogenesis in hippocampus of adult mice and rats. Neuroscience 158: 402-411
192. Taliaz D, Stall N, Dar DE, Zangen A (2010) Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol Psychiatry 15: 80-92
193. 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: 5792-5801
194. Tanapat P, Hastings NB, Rydel TA, Galea LA, 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
195. Tanti A, Rainer Q, Minier F, Surget A, Belzung C (2012) Differential environmental regulation of neurogenesis along the septo-temporal axis of the hippocampus. Neuropharmacology 63: 374-384
196. Tashiro A, Makino H, Gage FH (2007) Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during the immature stage. J Neurosci 27: 3252-3259
197. Tenk CM, Wilson H, Zhang Q, Pitchers KK, Coolen LM (2009) Sexual reward in male rats: effects of sexual experience on conditioned place preferences associated with ejaculation and intromissions. Horm Behav 55: 93-97
198. Thomas RM, Hotsenpiller G, Peterson DA (2007) Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. J Neurosci 27: 2734-2743
199. Thorsell A, Michalkiewicz M, Dumont Y, Quirion R, Caberlotto L, Rimondini R, Mathe AA, Heilig M (2000) Behavioral insensitivity to restraint stress, absent fear suppression of behavior and impaired spatial learning in transgenic rats with hippocampal neuropeptide Y overexpression. Proc Natl Acad Sci U S A 96: 12852-12857
200. Tokuza Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47: 803-815
201. Tronel S, Belnoue L, Grosjean N, Revest JM, Piazza PV, Koehl M, Abrous DN (2012) Adultborn neurons are necessary for extended contextual discrimination. Hippocampus 22: 292-298
202. Vallieres L, Campbell IL, Gage FH, Sawchenko PE (2002) Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci 2: 486-492
203. Van Bokhoven P, Oomen CA, Hoogendijk WJ, Smit AB, Lucassen PJ, Spijker S (2011) Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late anti-depressant treatment. Eur J Neurosci 33: 1833-1840
204. Van Der Harst JE, Fermont PCJ, Bilstra AE, Spruijt BM (2003) Access to enriched housing is rewarding to rats as reflected by their anticipatory behavior. Animal Behavior 66: 493-504
205. 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
206. Van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034
207. Veena J, Srikumar BN, Mahati K, Bhagya V, Raju TR, Shankaranarayana Rao BS (2009a) Enriched environment restores hippocampal cell proliferation and ameliorates cognitive deficits in chronically stressed rats. J Neurosci Res 87: 831-843
208. Veena J, Srikumar BN, Raju TR, Shankaranarayana Rao BS (2009b) Exposure to enriched environment restores the survival and differentiation of new born cells in the hippocampus and ameliorates depressive symptoms in chronically stressed rats. Neurosci Lett 455: 178-182
209. Veena J, Rao BS, Srikumar BN (2011a) Regulation of adult neurogenesis in the hippocampus by stress, acetylcholine and dopamine. J Nat Sci Biol Med 2: 26-37
210. Veena J, Srikumar BN, Mahati K, Raju TR, Shankaranarayana Rao BS (2011b) Oxotremorine treatment restores hippocampal neurogenesis and ameliorates depression-like behavior in chronically stressed rats. Psychopharmacology 217: 239-253
211. Waldherr M, Neumann ID (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc Natl Acad Sci USA 104: 16681-16684
212. 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
213. Warner-Schmidt JL, Madsen TM, Duman RS (2008) Electroconvulsive seizure restores neurogenesis and hippocampus-dependent fear memory after disruption by irradiation. Eur J Neurosci 27: 1485-1493
214. Watanabe Y, Gould E, McEwen BS (1992) Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588: 341-345
215. Westenbroek C, Den Boer JA, Veenhuis M, Ter Horst GJ (2004) Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res Bull 64: 303-308
216. Windle RJ, Kershaw YM, Shanks N, Wood SA, Lightman SL, Ingram CD (2004) Oxytocin attenuates stressinduced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. J Neurosci 24: 2974-2982
217. Windle RJ, Gamble LE, Kershaw YM, Wood SA, Lightman SL, Ingram CD (2006) Gonadal steroid modulation of stress-induced hypothalamo-pituitary-adrenal activity and anxiety behavior: role of central oxytocin. Endocrinol 147: 2423-2431
218. 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: 1681-1689
219. Winocur G, Wojtowicz JM, Sekeres M, Snyder JS, Wang S (2006) Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16: 296-304
220. Wolf SA, Melnik A, Kempermann G (2011) Physical exercise increases adult neurogenesis and telomerase activity, and improves behavioral deficits in a mouse model of schizophrenia. Brain Behav Immun 25: 971-980
221. Wong EY, Herbert J (2006) Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 137: 83-92
222. Woolley CS, Gould E, Sakai RR, Spencer RL, McEwen BS (1991) Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat. Brain Res 554: 312-315
223. Xu Y, Ku B, Cui L, Li X, Barish PA, Foster TC, Ogle WO (2007) Curcumin reverses impaired hippocampal neurogenesis and increases serotonin receptor 1A mRNA and brain-derived neurotrophic factor expression in chronically stressed rats. Brain Res 1162: 9-18
224. Yang D, Li Q, Fang L, Cheng K, Zhang R, Zheng P, Zhan Q, Qi Z, Zhong S, Xie P (2011) Reduced neurogenesis and pre-synaptic dysfunction in the olfactory bulb of a rat model of depression. Neuroscience 192: 609-618
225. Yap JJ, Takase LF, Kochman LJ, Fornal CA, Miczek KA, Jacobs BL (2006) Repeated brief social defeat episodes in mice: effects on cell proliferation in the dentate gyrus. Behav Brain Res 172: 344-350
226. Yi SS, Hwang IK, Yoo KY, Park OK, Yu J, Yan B, Kim IY, Kim YN, Pai T, Song W, Lee IS, Won MH, Seong JK, Yoon YS (2009) Effects of treadmill exercise on cell proliferation and differentiation in the subgranular zone of the dentate gyrus in a rat model of type II diabetes. Neurochem Res 34: 1039-1046
227. Ying Z, Roy RR, Edgerton VR, Gomez-Pinilla F (2005) Exercise restores levels of neurotrophins and synaptic plasticity following spinal cord injury. Exp Neurol 193: 411-419
228. Young SZ, Taylor MM, Bordey A (2011) Neurotransmitters couple brain activity to subventricular zone neurogenesis. Eur J Neurosci 33: 1123-1132
229. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26: 3-11
230. Zigova T, Pencea V, Wiegand SJ, Luskin MB (1998) Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cel Neurosci 11: 234-245