Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging

Frontiers in Neuroendocrinology

Volumn 30, Issue 3, 2009, Pages 343-357

  Pawluski, Jodi L ^a   Brummelte, Susanne ^a   Barha, Cindy K ^a   Crozier, Tamara M ^a   Galea, Liisa A M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adult neurogenesis; Cell death; Cell proliferation; Cell survival; Corticosterone; Estrogen; Hippocampus; Postpartum; Pregnancy; Stress

Indexed keywords

CORTICOSTERONE; ESTRADIOL; PROGESTERONE; STEROID HORMONE;

ADULT ANIMAL; AGING; DENTATE GYRUS; ESTRUS CYCLE; FEMALE; HIPPOCAMPUS; LACTATION; LIFESPAN; MAMMAL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; RAT; REPRODUCTION; REVIEW; RODENT; SEX DIFFERENCE; STRESS; SUBVENTRICULAR ZONE;

ADULT STEM CELLS; AGING; ANIMALS; ESTROUS CYCLE; FEMALE; GONADAL STEROID HORMONES; HIPPOCAMPUS; LACTATION; NEUROGENESIS; PREGNANCY; PREGNANCY, ANIMAL; RODENTIA;

EID: 67651210695     PISSN: 00913022     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yfrne.2009.03.007     Document Type: Review

References (186)

1. Airan R.D., Meltzer L.A., Roy M., Gong Y., Chen H., and Deisseroth K. High-speed imaging reveals neurophysiological links to behavior in an animal model of depression. Science 317 (2007) 819-823
2. Akbari E.M., Chatterjee D., Levy F., and Fleming A.S. Experience-dependent cell survival in the maternal rat brain. Behav. Neurosci. 121 (2007) 1001-1011
3. Alonso R., Griebel G., Pavone G., Stemmelin J., Le F.G., and Soubrie P. Blockade of CRF(1) or V(1b) receptors reverses stress-induced suppression of neurogenesis in a mouse model of depression. Mol. Psychiat. 9 (2004) 278-286 224
4. Altman J., and Das G.D. Postnatal neurogenesis in the guinea-pig. Nature 214 (1967) 1098-1101
5. Atkinson H.C., and Waddell B.J. The hypothalamic-pituitary-adrenal axis in rat pregnancy and lactation: circadian variation and interrelationship of plasma adrenocorticotropin and corticosterone. Endocrinology 136 (1995) 512-520
6. Bakker J., and Baum M.J. Role for estradiol in female-typical brain and behavioral sexual differentiation. Front. Neuroendocrinol. 29 (2008) 1-16
7. Bale T.L. Stress sensitivity and the development of affective disorders. Horm. Behav. 50 (2006) 529-533
8. Banasr M., Hery M., Brezun J.M., and Daszuta A. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur. J. Neurosci. 14 (2001) 1417-1424
9. Bao A.M., Ji Y.F., Van Someren E.J., Hofman M.A., Liu R.Y., and Zhou J.N. Diurnal rhythms of free estradiol and cortisol during the normal menstrual cycle in women with major depression. Horm. Behav. 45 (2004) 93-102
10. Barha C.K., Pawluski J.L., and Galea L.A. Maternal care affects male and female offspring working memory and stress reactivity. Physiol. Behav. 92 (2007) 939-950
11. Barha C.K., Barker J.M., Brummelte S., Epp J.R., and Galea L.A.M. Hormone regulation of adult hippocampal neurogenesis in the mammalian brain. In: Pfaff D. (Ed). Hormones Brain and Behavior (2009), Academic Press/Elsevier, San Diego
12. Barha C.K., Lieblich S.E., and Galea L.A.M. Different forms of oestrogen rapidly upregulate hippocampal neurogenesis in the dentate gyrus of young female rats. J. Neuroendocrinol. 21 (2009) 155-166
13. Barker J.M., and Galea L.A. Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 152 (2008) 888-902
14. Bhavnani B.R., Berco M., and Binkley J. Equine estrogens differentially prevent neuronal cell death induced by glutamate. J. Soc. Gynecol. Investig. 10 (2003) 302-308
15. Bloch M., Daly R.C., and Rubinow D.R. Endocrine factors in the etiology of postpartum depression. Compr. Psychiat. 44 (2003) 234-246
16. Bowman R.E., Beck K.D., and Luine V.N. Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Horm. Behav. 43 (2003) 48-59
17. Brannvall K., Korhonen L., and Lindholm D. Estrogen-receptor-dependent regulation of neural stem cell proliferation and differentiation. Mol. Cell. Neurosci. 21 (2002) 512-520
18. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., and Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 467 (2003) 1-10
19. Brummelte S., Pawluski J.L., and Galea L.A. High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: a model of post-partum stress and possible depression. Horm. Behav. 50 (2006) 370-382
20. Brusco J., Wittmann R., de Azevedo M.S., Lucion A.B., Franci C.R., Giovenardi M., and Rasia-Filho A.A. Plasma hormonal profiles and dendritic spine density and morphology in the hippocampal CA1 stratum radiatum, evidenced by light microscopy, of virgin and postpartum female rats. Neurosci. Lett. 438 (2008) 346-350
21. Budziszewska B., Leskiewicz M., Kubera M., Jaworska-Feil L., Kajta M., and Lason W. Estrone, but not 17 beta-estradiol, attenuates kainate-induced seizures and toxicity in male mice. Exp. Clin. Endocrinol. Diab. 109 (2001) 168-173
22. Burt V.K., and Stein K. Epidemiology of depression throughout the female life cycle. J. Clin. Psychiat. 63 Suppl. 7 (2002) 9-15
23. Butcher R.L., Collins W.E., and Fugo N.W. Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17beta throughout the 4-day estrous cycle of the rat. Endocrinology 94 (1974) 1704-1708
24. Butz M., Lehmann K., Dammasch I.E., and Teuchert-Noodt G. A theoretical network model to analyse neurogenesis and synaptogenesis in the dentate gyrus. Neural Networks 19 (2006) 1490-1505
25. Cameron H.A., Woolley C.S., McEwen B.S., and Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56 (1993) 337-344
26. Cameron H.A., and Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61 (1994) 203-209
27. Cameron H.A., and McKay R.D. Restoring production of hippocampal neurons in old age. Nat. Neurosci. 2 (1999) 894-897
28. Cameron H.A., and McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435 (2001) 406-417
29. Carey M.P., Deterd C.H., de Koning J., Helmerhorst F., and de Kloet E.R. The influence of ovarian steroids on hypothalamic-pituitary-adrenal regulation in the female rat. J. Endocrinol. 144 (1995) 311-321
30. Carter C.S., Grippo A.J., Pournajafi-Nazarloo H., Ruscio M.G., and Porges S.W. Oxytocin vasopressin and sociality. Prog. Brain Res. 170 (2008) 331-336
31. Chakraborty T.R., and Gore A.C. Aging-related changes in ovarian hormones, their receptors, and neuroendocrine function. Exp. Biol. Med. (Maywood) 229 (2004) 977-987
32. Chiba S., Suzuki M., Yamanouchi K., and Nishihara M. Involvement of granulin in estrogen-induced neurogenesis in the adult rat hippocampus. J. Reprod. Dev. 53 (2007) 297-307
33. Chrousos G.P., Torpy D.J., and Gold P.W. Interactions between the hypothalamic-pituitary-adrenal axis and the female reproductive system: clinical implications. Ann. Intern. Med. 129 (1998) 229-240
34. Czeh B., Welt T., Fischer A.K., Erhardt A., Schmitt W., Muller M.B., Toschi N., Fuchs E., and Keck M.E. Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol. Psychiat. 52 (2002) 1057-1065
35. Darnaudery M., Perez-Martin M., Del Favero F., Gomez-Roldan C., Garcia-Segura L.M., and Maccari S. Early motherhood in rats is associated with a modification of hippocampal function. Psychoneuroendocrinology 32 (2007) 803-812
36. Drapeau E., Mayo W., Aurousseau C., Le Moal M., Piazza P.V., and Abrous D.N. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl. Acad. Sci. USA 100 (2003) 14385-14390
37. Driscoll I., Howard S.R., Stone J.C., Monfils M.H., Tomanek B., Brooks W.M., and Sutherland R.J. The aging hippocampus: a multi-level analysis in the rat. Neuroscience 139 (2006) 1173-1185
38. Dupret D., Revest J.M., Koehl M., Ichas F., De Giorgi F., Costet P., Abrous D.N., and Piazza P.V. Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE 3 (2008) e1959
39. Epp J.R., Spritzer M.D., and Galea L.A. Hippocampus-dependent learning promotes survival of new neurons in the dentate gyrus at a specific time during cell maturation. Neuroscience 149 (2007) 273-285
40. Ernst C., Olson A.K., Pinel J.P., Lam R.W., and Christie B.R. Antidepressant effects of exercise: evidence for an adult-neurogenesis hypothesis?. J. Psychiat. Neurosci. 31 (2006) 84-92
41. Falconer E.M., and Galea L.A. Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats. Brain Res. 975 (2003) 22-36
42. Fester L., Ribeiro-Gouveia V., Prange-Kiel J., von Schassen C., Bottner M., Jarry H., and Rune G.M. Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis. J. Neurochem. 97 (2006) 1136-1144
43. Figueiredo H.F., Ulrich-Lai Y.M., Choi D.C., and Herman J.P. Estrogen potentiates adrenocortical responses to stress in female rats. Am. J. Physiol. Endocrinol. Metab. 292 (2007) E1173-E1182
44. Fowler C.D., Liu Y., Ouimet C., and Wang Z. The effects of social environment on adult neurogenesis in the female prairie vole. J. Neurobiol. 51 (2002) 115-128
45. Freeman M.E., Kanyicska B., Lerant A., and Nagy G. Prolact structure, function, and regulation of secretion. Physiol. Rev. 80 (2000) 1523-1631
46. Furuta M., and Bridges R.S. Gestation-induced cell proliferation in the rat brain. Brain Res. Dev. Brain Res. 156 (2005) 61-66
47. Galea L., and McEwen B. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 89 (1999) 955-964
48. Galea L.A., McEwen B.S., Tanapat P., Deak T., Spencer R.L., and Dhabhar F.S. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 81 (1997) 689-697
49. Galea L.A., and McEwen B.S. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 89 (1999) 955-964
50. Galea L.A., Ormerod B.K., Sampath S., Kostaras X., Wilkie D.M., and Phelps M.T. Spatial working memory and hippocampal size across pregnancy in rats. Horm. Behav. 37 (2000) 86-95
51. Galea L.A., Spritzer M.D., Barker J.M., and Pawluski J.L. Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 16 (2006) 225-232
52. Galea L.A. Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res. Rev. 57 (2008) 332-341
53. Galea L.A., Uban K.A., Epp J.R., Brummelte S., Barha C.K., Wilson W.L., Lieblich S.E., and Pawluski J.L. Endocrine regulation of cognition and neuroplasticity: our pursuit to unveil the complex interaction between hormones, the brain, and behaviour. Can. J. Exp. Psychol. 62 (2008) 247-260
54. Gallo R.V., Babu G.N., Bona-Gallo A., vorshak-Harvey E., Leipheimer R.E., and Marco J. Regulation of pulsatile luteinizing hormone release during the estrous cycle and pregnancy in the rat. Adv. Exp. Med. Biol. 219 (1987) 109-130
55. Gascon E., Vutskits L., Jenny B., Durbec P., and Kiss J.Z. PSA-NCAM in postnatally generated immature neurons of the olfactory bulb: a crucial role in regulating p75 expression and cell survival. Development 134 (2007) 1181-1190
56. Gerlach T., and Aurich J.E. Aurich, regulation of seasonal reproductive activity in the stallion, ram and hamster. Anim. Reprod. Sci. 58 (2000) 197-213
57. Gould E., Woolley C.S., Cameron H.A., Daniels D.C., and McEwen B.S. Adrenal steroids regulate postnatal development of the rat dentate gyrus: II. Effects of glucocorticoids and mineralocorticoids on cell birth. J. Comp. Neurol. 313 (1991) 486-493
58. Gould E. How widespread is adult neurogenesis in mammals?. Nat. Rev. Neurosci. 8 (2007) 481-488
59. Green A.D., and Galea L.A. Adult hippocampal cell proliferation is suppressed with estrogen withdrawal after a hormone-simulated pregnancy. Horm. Behav. 54 (2008) 203-211
60. Guerra-Araiza C., Villamar-Cruz O., Gonzalez-Arenas A., Chavira R., and Camacho-Arroyo I. Changes in progesterone receptor isoforms content in the rat brain during the oestrous cycle and after oestradiol and progesterone treatments. J. Neuroendocrinol. 15 (2003) 984-990
61. Hagihara K., Hirata S., Osada T., Hirai M., and Kato J. Distribution of cells containing progesterone receptor mRNA in the female rat di- and telencephalon: an in situ hybridization study. Brain Res. Mol. Brain Res. 14 (1992) 239-249
62. Hastings N.B., and Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. J. Comp. Neurol. 413 (1999) 146-154
63. Heine V.M., Maslam S., Zareno J., Joels M., and Lucassen P.J. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur. J. Neurosci. 19 (2004) 131-144
64. Hojo Y., Hattori T.A., Enami T., Furukawa A., Suzuki K., Ishii H.T., Mukai H., Morrison J.H., Janssen W.G., Kominami S., Harada N., Kimoto T., and Kawato S. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proc. Natl. Acad. Sci. USA 101 (2004) 865-870
65. Holmes M.M., and Galea L.A. Defensive behavior and hippocampal cell proliferation: differential modulation by naltrexone during stress. Behav. Neurosci. 116 (2002) 160-168
66. Huang G.J., and Herbert J. Stimulation of neurogenesis in the hippocampus of the adult rat by fluoxetine requires rhythmic change in corticosterone. Biol. Psychiat. 59 (2006) 619-624
67. Isgor C., and Watson S.J. Estrogen receptor alpha and beta mRNA expressions by proliferating and differentiating cells in the adult rat dentate gyrus and subventricular zone. Neuroscience 134 (2005) 847-856
68. Jaako-Movits K., Zharkovsky T., Pedersen M., and Zharkovsky A. Decreased hippocampal neurogenesis following olfactory bulbectomy is reversed by repeated citalopram administration. Cell. Mol. Neurobiol. 26 (2006) 1559-1570
69. Jessberger S., Romer B., Babu H., and Kempermann G. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp. Neurol. 196 (2005) 342-351
70. Jessberger S., Nakashima K., Clemenson Jr. G.D., Mejia E., Mathews E., Ure K., Ogawa S., Sinton C.M., Gage F.H., and Hsieh J. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J. Neurosci. 27 (2007) 5967-5975
71. Kajantie E., and Phillips D.I. The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 31 (2006) 151-178
72. Kempermann G., Kuhn H.G., and Gage F.H. Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 18 (1998) 3206-3212
73. Kimble D.P., Rogers L., and Hendrickson C.W. Hippocampal lesions disrupt maternal, not sexual, behavior in the albino rat. J. Comp. Physiol. Psychol. 63 (1967) 401-407
74. Kinsley C.H., Madonia L., Gifford G.W., Tureski K., Griffin G.R., Lowry C., Williams J., Collins J., McLearie H., and Lambert K.G. Motherhood improves learning and memory. Nature 402 (1999) 137-138
75. Kinsley C.H., Trainer R., Stafisso-Sandoz G., Quadros P., Marcus L.K., Hearon C., Meyer E.A., Hester N., Morgan M., Kozub F.J., and Lambert K.G. Motherhood and the hormones of pregnancy modify concentrations of hippocampal neuronal dendritic spines. Horm. Behav. 49 (2006) 131-142
76. Klempin F., and Kempermann G. Adult hippocampal neurogenesis and aging. Eur. Arch. Psychiat. Clin. Neurosci. 257 (2007) 271-280
77. Krugers H.J., van der L.S., van O.E., Alfarez D.N., Maslam S., Lucassen P.J., and Joels M. Dissociation between apoptosis, neurogenesis, and synaptic potentiation in the dentate gyrus of adrenalectomized rats. Synapse 61 (2007) 221-230
78. Kudielka B.M., and Kirschbaum C. Sex differences in HPA axis responses to stress: a review. Biol. Psychol. 69 (2005) 113-132
79. Kuhn H.G., Dickinson-Anson H., and Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16 (1996) 2027-2033
80. Kuipers S.D., Trentani A., Westenbroek C., Bramham C.R., Korf J., Kema I.P., Ter Horst G.J., and Den Boer J.A. Unique patterns of FOS, phospho-CREB and BrdU immunoreactivity in the female rat brain following chronic stress and citalopram treatment. Neuropharmacology 50 (2006) 428-440
81. Lagace D.C., Fischer S.J., and Eisch A.J. Gender and endogenous levels of estradiol do not influence adult hippocampal neurogenesis in mice. Hippocampus 17 (2007) 175-180
82. Larsen C.M., Kokay I.C., and Grattan D.R. Male pheromones initiate prolactin-induced neurogenesis and advance maternal behavior in female mice. Horm. Behav. 53 (2008) 509-517
83. Lee K.J., Kim S.J., Kim S.W., Choi S.H., Shin Y.C., Park S.H., Moon B.H., Cho E., Lee M.S., Chun B.G., and Shin K.H. Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp. Mol. Med. 38 (2006) 44-54
84. Leuner B., Mirescu C., Noiman L., and Gould E. Maternal experience inhibits the production of immature neurons in the hippocampus during the postpartum period through elevations in adrenal steroids. Hippocampus 17 (2007) 434-442
85. Levin-Allerhand J.A., Lominska C.E., Wang J., and Smith J.D. 17Alpha-estradiol and 17beta-estradiol treatments are effective in lowering cerebral amyloid-beta levels in AbetaPPSWE transgenic mice. J. Alzheimers Dis. 4 (2002) 449-457
86. Lopes da Silva F.H., Gorter J.A., and Wadman W.J. Kindling of the hippocampus induces spatial memory deficits in the rat. Neurosci. Lett. 63 (1986) 115-120
87. Luine V.N., Jacome L.F., and Maclusky N.J. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144 (2003) 2836-2844
88. Luine V.N., Beck K.D., Bowman R.E., Frankfurt M., and Maclusky N.J. Chronic stress and neural function: accounting for sex and age. J. Neuroendocrinol. 19 (2007) 743-751
89. Ma W., Miao Z., and Novotny M.V. Role of the adrenal gland and adrenal-mediated chemosignals in suppression of estrus in the house mouse: the lee-boot effect revisited. Biol. Reprod. 59 (1998) 1317-1320
90. Macbeth A.H., Gautreaux C., and Luine V.N. Pregnant rats show enhanced spatial memory, decreased anxiety, and altered levels of monoaminergic neurotransmitters. Brain Res. 1241 (2008) 136-147
91. MacLusky N.J., Luine V.N., Hajszan T., and Leranth C. The 17alpha and 17beta isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats. Endocrinology 146 (2005) 287-293
92. Magiakou M.A., Mastorakos G., Webster E., and Chrousos G.P. The hypothalamic-pituitary-adrenal axis and the female reproductive system. Ann. NY Acad. Sci. 816 (1997) 42-56
93. Mak G.K., Enwere E.K., Gregg C., Pakarainen T., Poutanen M., Huhtaniemi I., and Weiss S. Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat. Neurosci. 10 (2007) 1003-1011
94. Malberg J.E., Eisch A.J., Nestler E.J., and Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20 (2000) 9104-9110
95. Mastorakos G., Pavlatou M.G., and Mizamtsidi M. The hypothalamic-pituitary-adrenal and the hypothalamic-pituitary-gonadal axes interplay. Pediatr. Endocrinol. Rev. 3 1 (2006) 172-181 Suppl. 1
96. Mazzucco C.A., Lieblich S.E., Bingham B.I., Williamson M.A., Viau V., and Galea L.A. Both estrogen receptor alpha and estrogen receptor beta agonists enhance cell proliferation in the dentate gyrus of adult female rats. Neuroscience 141 (2006) 1793-1800
97. McCormick C.M., and Mathews I.Z. HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol. Biochem. Behav. 86 (2007) 220-233
98. McEwen B. Estrogen actions throughout the brain. Recent Prog. Horm. Res. 57 (2002) 357-384
99. McEwen B.S. Neural gonadal steroid actions. Science 211 (1981) 1303-1311
100. McEwen B.S. Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur. J. Pharmacol. 583 (2008) 174-185
101. Merrill D.A., Karim R., Darraq M., Chiba A.A., and Tuszynski M.H. Hippocampal cell genesis does not correlate with spatial learning ability in aged rats. J. Comp. Neurol. 459 (2003) 201-207
102. Miller G.E., Chen E., and Zhou E.S. If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychol. Bull. 133 (2007) 25-45
103. Miller Jr. O.L., Stone G.E., and Prescott D.M. Autoradiography of soluble materials. J. Cell Biol. 23 (1964) 654-658
104. Mirescu C., and Gould E. Stress and adult neurogenesis. Hippocampus 16 (2006) 233-238
105. Mitra R., Sundlass K., Parker K.J., Schatzberg A.F., and Lyons D.M. Social stress-related behavior affects hippocampal cell proliferation in mice. Physiol. Behav. 89 (2006) 123-127
106. Montaron M.F., Drapeau E., Dupret D., Kitchener P., Aurousseau C., Le Moal M., Piazza P.V., and Abrous D.N. Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiol. Aging 27 (2006) 645-654
107. Nacher J., Alonso-Llosa G., Rosell D.R., and McEwen B.S. NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol. Aging 24 (2003) 273-284
108. Nacher J., Gomez-Climent M.A., and McEwen B. Chronic non-invasive glucocorticoid administration decreases polysialylated neural cell adhesion molecule expression in the adult rat dentate gyrus. Neurosci. Lett. 370 (2004) 40-44
109. Nagy A.I., Ormerod B.K., Mazzucco C.A., and Galea L.A.M. Estradiol-induced enhancement in cell proliferation is mediated through estrogen receptors in the dentate gyrus of adult female rats. Drug Dev. Res. 66 (2006) 142-149
110. Nichols N.R., Zieba M., and Bye N. Do glucocorticoids contribute to brain aging?. Brain Res. Brain Res. Rev. 37 (2001) 273-286
111. Nickerson K., Bonsess R.W., Douglas R.G., Condliffe E., and du Vigneaud P.V. Oxytocin and milk ejection. Am. J. Obstet. Gynecol. 67 (1954) 1028-1034
112. Nilsson M., Perfilieva E., Johansson U., Orwar O., and Eriksson P.S. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J. Neurobiol. 39 (1999) 569-578
113. Nowakowski R.S., and Hayes N.L. Numerology of neurogenesis: characterizing the cell cycle of neurostem cells. In: Gage FH K.G., and Song H. (Eds). Adult Neurogenesis (2008), Cold Spring Harbor Laboratory Press, Cold Spring Harbor 7-23
114. Numan M. Neural basis of maternal behavior in the rat. Psychoneuroendocrinology 13 (1988) 47-62
115. Oatridge A., Holdcroft A., Saeed N., Hajnal J.V., Puri B.K., Fusi L., and Bydder G.M. Change in brain size during and after pregnancy: study in healthy women and women with preeclampsia. AJNR Am. J. Neuroradiol. 23 (2002) 19-26
116. Olson A.K., Eadie B.D., Ernst C., and Christie B.R. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16 (2006) 250-260
117. Oomen C.A., Mayer J.L., de Kloet E.R., Joels M., and Lucassen P.J. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur. J. Neurosci. 26 (2007) 3395-3401
118. Ormerod B.K., and Galea L.A. Reproductive status influences cell proliferation and cell survival in the dentate gyrus of adult female meadow voles: a possible regulatory role for estradiol. Neuroscience 102 (2001) 369-379
119. Ormerod B.K., and Galea L.A. Reproductive status influences the survival of new cells in the dentate gyrus of adult male meadow voles. Neurosci. Lett. 346 (2003) 25-28
120. Ormerod B.K., Lee T.T., and Galea L.A. Estradiol initially enhances but subsequently suppresses (via adrenal steroids) granule cell proliferation in the dentate gyrus of adult female rats. J. Neurobiol. 55 (2003) 247-260
121. Ormerod B.K., Lee T.T., and Galea L.A. Estradiol enhances neurogenesis in the dentate gyri of adult male meadow voles by increasing the survival of young granule neurons. Neuroscience 128 (2004) 645-654
122. Parsons C.G., Stoffler A., and Danysz W. Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system - too little activation is bad, too much is even worse. Neuropharmacology 53 (2007) 699-723
123. Pawluski J.L., and Galea L.A. Hippocampal morphology is differentially affected by reproductive experience in the mother. J. Neurobiol. 66 (2006) 71-81
124. Pawluski J.L., Vanderbyl B.L., Ragan K., and Galea L.A. First reproductive experience persistently affects spatial reference and working memory in the mother and these effects are not due to pregnancy or 'mothering' alone. Behav. Brain Res. 175 (2006) 157-165
125. Pawluski J.L., Walker S.K., and Galea L.A. Reproductive experience differentially affects spatial reference and working memory performance in the mother. Horm. Behav. 49 (2006) 143-149
126. Pawluski J.L., and Galea L.A. Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam. Neuroscience 149 (2007) 53-67
127. Pawluski J.L., Charlier T.D., Lieblich S.E., Hammond G.L., and Galea L.A. Reproductive experience alters corticosterone and CBG levels in the rat dam. Physiol. Behav. 96 (2009) 108-114
128. Perez-Martin M., Azcoitia I., Trejo J.L., Sierra A., and Garcia-Segura L.M. An antagonist of estrogen receptors blocks the induction of adult neurogenesis by insulin-like growth factor-I in the dentate gyrus of adult female rat. Eur. J. Neurosci. 18 (2003) 923-930
129. Perez-Martin M., Salazar V., Castillo C., Ariznavarreta C., Azcoitia I., Garcia-Segura L.M., and Tresguerres J.A. Estradiol and soy extract increase the production of new cells in the dentate gyrus of old rats. Exp. Gerontol. 40 (2005) 450-453
130. Perez E., Liu R., Yang S.H., Cai Z.Y., Covey D.F., and Simpkins J.W. Neuroprotective effects of an estratriene analog are estrogen receptor independent in vitro and in vivo. Brain Res. 1038 (2005) 216-222
131. Pham K., Nacher J., Hof P.R., and McEwen B.S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 17 (2003) 879-886
132. Pollak D.D., Monje F.J., Zuckerman L., Denny C.A., Drew M.R., and Kandel E.R. An animal model of a behavioral intervention for depression. Neuron. 60 (2008) 149-161
133. Pollard I., and Cairncross K.D. Ultrastructural changes in the adenohypophysis, adrenal gland activity, and desynchronization of the oestrous cycle following unpredictable stress in the rat. Aust. J. Biol. Sci. 30 (1977) 559-572
134. Prickaerts J., Koopmans G., Blokland A., and Scheepens A. Learning and adult neurogenesis: survival with or without proliferation?. Neurobiol. Learn. Mem. 81 (2004) 1-11
135. Rannevik G., Jeppsson S., Johnell O., Bjerre B., Laurell-Borulf Y., and Svanberg L. A longitudinal study of the perimenopausal transition: altered profiles of steroid and pituitary hormones, SHBG and bone mineral density. Maturitas 21 (1995) 103-113
136. Rolls A., Schori H., London A., and Schwartz M. Decrease in hippocampal neurogenesis during pregnancy: a link to immunity. Mol. Psychiat. 13 (2008) 468-469
137. Rose'Meyer R.B., Mellick A.S., Garnham B.G., Harrison G.J., Massa H.M., and Griffiths L.R. The measurement of adenosine and estrogen receptor expression in rat brains following ovariectomy using quantitative PCR analysis. Brain Res. Brain Res. Protoc. 11 (2003) 9-18
138. Rosenblatt J.S., Mayer A.D., and Giordano A.L. Hormonal basis during pregnancy for the onset of maternal behavior in the rat. Psychoneuroendocrinology 13 (1988) 29-46
139. Ruscio M.G., Sweeny T.D., Hazelton J.L., Suppatkul P., Boothe E., and Carter C.S. Pup exposure elicits hippocampal cell proliferation in the prairie vole. Behav. Brain Res. 187 (2008) 9-16
140. Russell J.A., Douglas A.J., and Ingram C.D. Brain preparations for maternity - adaptive changes in behavioral and neuroendocrine systems during pregnancy and lactation. An overview. Prog. Brain Res. 133 (2001) 1-38
141. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., Belzung C., and Hen R. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301 (2003) 805-809
142. Saravia F., Beauquis J., Pietranera L., and De Nicola A.F. Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice. Psychoneuroendocrinology 32 (2007) 480-492
143. Saxe M.D., Battaglia F., Wang J.W., Malleret G., David D.J., Monckton J.E., Garcia A.D., Sofroniew M.V., Kandel E.R., Santarelli L., Hen R., and Drew M.R. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. USA 103 (2006) 17501-17506
144. Schmidt-Hieber C., Jonas P., and Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429 (2004) 184-187
145. Schule C. Neuroendocrinological mechanisms of actions of antidepressant drugs. J. Neuroendocrinol. 19 (2007) 213-226
146. Schwarz J.M., and McCarthy M.M. Steroid-induced sexual differentiation of the developing brain: multiple pathways, one goal. J. Neurochem. 105 (2008) 1561-1572
147. Seki T., and Arai Y. Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J. Neurosci. 13 (1993) 2351-2358
148. Shaikh A.A. Estrone and estradiol levels in the ovarian venous blood from rats during the estrous cycle and pregnancy. Biol. Reprod. 5 (1971) 297-307
149. Sharp P.J. Photoperiodic regulation of seasonal breeding in birds. Ann. NY Acad. Sci. 1040 (2005) 189-199
150. Shingo T., Gregg C., Enwere E., Fujikawa H., Hassam R., Geary C., Cross J.C., and Weiss S. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299 (2003) 117-120
151. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., and Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12 (2002) 578-584
152. Shors T.J. Stressful experience and learning across the lifespan. Ann. Rev. Psychol. 57 (2006) 55-85
153. Shors T.J., Mathew J., Sisti H.M., Edgecomb C., Beckoff S., and Dalla C. Neurogenesis and helplessness are mediated by controllability in males but not in females. Biol. Psychiat. 62 (2007) 487-495
154. Simpkins J.W., Yang S.H., Liu R., Perez E., Cai Z.Y., Covey D.F., and Green P.S. Estrogen-like compounds for ischemic neuroprotection. Stroke 35 (2004) 2648-2651
155. Singh M., Dykens J.A., and Simpkins J.W. Novel mechanisms for estrogen-induced neuroprotection. Exp. Biol. Med. (Maywood) 231 (2006) 514-521
156. Snyder J.S., Kee N., and Wojtowicz J.M. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J. Neurophysiol. 85 (2001) 2423-2431
157. Sohrabji F., Miranda R.C., and Toran-Allerand C.D. Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J. Neurosci. 14 (1994) 459-471
158. Spanswick S.C., Epp J.R., Keith J.R., and Sutherland R.J. Adrenalectomy-induced granule cell degeneration in the hippocampus causes spatial memory deficits that are not reversed by chronic treatment with corticosterone or fluoxetine. Hippocampus 17 (2007) 137-146
159. Spritzer M.D., and Galea L.A. Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Dev. Neurobiol. 67 (2007) 1321-1333
160. Steiner M., Dunn E., and Born L. Hormones and mood: from menarche to menopause and beyond. J. Affect. Disord. 74 (2003) 67-83
161. Tanapat P., Hastings N.B., Reeves A.J., and Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19 (1999) 5792-5801
162. Tanapat P., Hastings N.B., Rydel T.A., Galea L.A., and Gould E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J. Comp. Neurol. 437 (2001) 496-504
163. Tanapat P., Hastings N.B., and Gould E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J. Comp. Neurol. 481 (2005) 252-265
164. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res. Rev. 53 (2007) 198-214
165. Terlecki L.J., and Sainsbury R.S. Effects of fimbria lesions on maternal behavior in the rat. Physiol. Behav. 21 (1978) 89-97
166. Thomas R.M., Urban J.H., and Peterson D.A. Acute exposure to predator odor elicits a robust increase in corticosterone and a decrease in activity without altering proliferation in the adult rat hippocampus. Exp. Neurol. 201 (2006) 308-315
167. Thomas R.M., Hotsenpiller G., and Peterson D.A. Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. J. Neurosci. 27 (2007) 2734-2743
168. Thomas R.M., and Peterson D.A. Even neural stem cells get the blues: evidence for a molecular link between modulation of adult neurogenesis and depression. Gene Expr. 14 (2008) 183-193
169. Toran-Allerand C.D. Estrogen and the brain: beyond ER-alpha, ER-beta, and 17beta-estradiol. Ann. NY Acad. Sci. 1052 (2005) 136-144
170. van Praag H., Christie B.R., Sejnowski T.J., and Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci USA 96 (1999) 13427-13431
171. van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., and Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 415 (2002) 1030-1034
172. Viau V., and Meaney M.J. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 129 (1991) 2503-2511
173. Viau V. Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. J. Neuroendocrinol. 14 (2002) 506-513
174. Vollmayr B., Mahlstedt M.M., and Henn F.A. Neurogenesis and depression: what animal models tell us about the link. Eur. Arch. Psychiat. Clin. Neurosci. 257 (2007) 300-303
175. Voogt J.L., Sar M., and Meites J. Influence of cycling, pregnancy, labor, and suckling on corticosterone-ACTH levels. Am. J. Physiol. 216 (1969) 655-658
176. Wade J., and Arnold A.P. Sexual differentiation of the zebra finch song system. Ann. NY Acad. Sci. 1016 (2004) 540-559
177. Wang J.M., Johnston P.B., Ball B.G., and Brinton R.D. The neurosteroid allopregnanolone promotes proliferation of rodent and human neural progenitor cells and regulates cell-cycle gene and protein expression. J. Neurosci. 25 (2005) 4706-4718
178. Westenbroek C., Den Boer J.A., Veenhuis M., and Ter Horst G.J. Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res. Bull. 64 (2004) 303-308
179. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., and Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16 (2006) 296-304
180. Wong E.Y., and Herbert J. The corticoid environment: a determining factor for neural progenitors' survival in the adult hippocampus. Eur. J. Neurosci. 20 (2004) 2491-2498
181. Wong E.Y., and Herbert J. Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. Eur. J. Neurosci. 22 (2005) 785-792
182. Wong E.Y., and Herbert J. Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 137 (2006) 83-92
183. Woolley C.S., and McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 336 (1993) 293-306
184. Zhang C.L., Zou Y., He W., Gage F.H., and Evans R.M. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451 (2008) 1004-1007
185. Zhao H., Tian Z., Hao J., and Chen B. Extragonadal aromatization increases with time after ovariectomy in rats. Reprod. Biol. Endocrinol. 3 (2005) 6
186. Zhou J.N., and Swaab D.F. Activation and degeneration during aging: a morphometric study of the human hypothalamus. Microsc. Res. Tech. 44 (1999) 36-48