Hormone regulation of adult hippocampal neurogenesis in the mammalian brain

Hormones, Brain and Behavior Online

Volumn , Issue , 2009, Pages 2165-2200

  Barha, C K ^a   Barker, J M ^a   Brummelte, S ^a   Epp, J R ^a   Galea, L A M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adrenal steroids; Bromodeoxyuridine; Cell proliferation; Cell survival; Dentate gyrus; Estrogen; Hippocampus; Neurogenesis; Stress; Testosterone

Indexed keywords

EID: 84884806160     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-008088783-8.00067-X     Document Type: Chapter

References (347)

1. Aimone J.B., Wiles J., Gage F.H. Potential role for adult neurogenesis in the encoding of time in new memories. Nature Neuroscience 2006, 9:723-727.
2. Altman J. Autoradiographic investigation of cell proliferation in brains of rats and cats. Anatomical Record 1963, 145:573.
3. Altman J., Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. Journal of Comparative Neurology 1965, 124:319-335.
4. Alvarez-Buylla A. Neurogenesis and plasticity in the CNS of adult birds. Experimental Neurology 1992, 115(1):110-114.
5. Alvarez-Buylla A., Lois C. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proceedings of the National Academy of Sciences of the United States of America 1993, 90:2074-2077.
6. Ambrogini P., Cuppini R., Cuppini C., et al. Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neuroscience Letters 2000, 286:21-24.
7. Ambrogini P., Lattanzi D., Ciuffoli S., et al. Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus. Brain Research 2004, 1017:21-31.
8. Amrein I., Dechmann D.K.N., Winter Y., Lipp H.-P. Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera). PLoS ONE 2007, 2:e455.
9. Amrein I., Slomianka L., Poletaeva I.I., Bologova N.V., Lipp H.-P. Marked species and age-dependent differences in cell proliferation and neurogenesis in the hippocampus of wild-living rodents. Hippocampus 2004, 14:1000-1010.
10. Azcoitia I., Sierra A., Garcia-Segura L.M. Localization of estrogen receptor beta-immunoreactivity in astrocytes of the adult rat brain. Glia 1999, 26(3):260-267.
11. Bakker J., Baum M.J. Role for estradiol in female-typical brain and behavioral sexual differentiation. Frontiers in Neuroendocrinology 2008, 29:1-16.
12. Bale T.L. Stress sensitivity and the development of affective disorders. Hormones and Behavior 2006, 50:529-533.
13. Banasr M., Hery M., Brezun J.M., Daszuta A. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. European Journal of Neuroscience 2001, 14:1417-1424.
14. Banasr M., Hery M., Printemps R., Daszuta A. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 2004, 29(3):450-460.
15. Barker J.M., Galea L.A.M. Estradiol differentially affects adult hippocampal neurogenesis in male and female rats when administered during different stages of cell maturation 2007, Programe No. 566.14.
16. Barker J.M., Galea L.A.M. Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 2008, 152:888-902.
17. Barker J.M., Wojtowicz J.M., Boosntra R. Where's my dinner? Adult neurogenesis in free-living food-storing rodents. Genes Brain Behavior 2005, 4:89-98.
18. Barnea A., Nottebohm F. Recruitment and replacement of hippocampal neurons in young and adult chickadees: An addition to the theory of hippocampal learning. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:714-718.
19. Barnes N.M., Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 1999, 38(8):1083-1152.
20. Bayer S.A., Yackel J.W., Puri P.S. Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 1982, 216:890-892.
21. Bhavnani B.R., Berco M., Binkley J. Equine estrogens differentially prevent neuronal cell death induced by glutamate. Journal of the Society for Gynecologic Investigation 2003, 10(5):302-308.
22. Bizon J.L., Gallagher M. Production of new cells in the rat dentate gyrus over the lifespan: Relation to cognitive decline. European Journal of Neuroscience 2003, 18:215-219.
23. Blurton-Jones M., Kuan P.N., Tuszynski M.H. Anatomical evidence for transsynaptic influences of estrogen on brain-derived neurotrophic factor expression. Journal of Comparative Neurology 2004, 468(3):347-360.
24. Boonstra R., Boag P.T. Spring declines in Microtus pennsylvanicus and the role of steroid hormones. The Journal of Animal Ecology 1992, 61:339-352.
25. Boonstra R., Galea L., Matthews S., Wojtowicz J.M. Adult neurogenesis in natural populations. Canadian Journal of Physiology and Pharmacology 2001, 79:297-302.
26. Boswald M., Harasim S., Maurer-Schultze B. Tracer dose and availability time of thymidine and bromodeoxyuridine: Application of bromodeoxyuridine in cell kinetic studies. Cell and Tissue Kinetics 1990, 23:169-181.
27. Bowman R.E., Beck K.D., Luine V.N. Chronic stress effects on memory: Sex differences in performance and monoaminergic activity. Hormones and Behavior 2003, 43:48-59.
28. Brännvall K., Bogdanovic N., Korhonen L., Linhlom D. 19-Nortestosterone influences neural stem cell proliferation and neurogenesis in the rat brain. European Journal of Neuroscience 2005, 21:871-878.
29. Bredy T.W., Grant R.J., Champagne D.L., Meaney M.J. Maternal care influences neuronal survival in the hippocampus of the rat. European Journal of Neuroscience 2003, 18:2903-2909.
30. Brenowitz E.A. Plasticity of the adult avian song control system. Annals of New York Academy of Sciences 2004, 1016:560-585.
31. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. Journal of Comparative Neurology 2003, 467:1-10.
32. Bruel-Jungerman E., Laroche S., Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. European Journal of Neuroscience 2005, 21:513-521.
33. Brummelte S., Pawluski J.L., 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. Hormones and Behavior 2006, 50:370-382.
34. Budziszewska B., Leskiewicz M., Kubera M., Jaworska-Feil L., Kajta M., Lason W. Estrone, but not 17beta-estradiol, attenuates kainate-induced seizures and toxicity in male mice. Experimental and Clinical Endocrinology and Diabetes 2001, 109(3):168-173.
35. Burt V.K., Stein K. Epidemiology of depression throughout the female life cycle. Journal of Clinical Psychiatry 2002, 63(7):9-15.
36. Cajal S.R.y Cajal's Degeneration and Regeneration of the Nervous System 1991, Oxford University Press, New York.
37. Cameron H.A., Woolley C.S., Gould E. Adrenal steroid receptor immunoreactivity in cells born in the adult rat dentate gyrus. Brain Research 1993, 611:342-346.
38. Cameron H.A., Woolley C.S., McEwen B.S., Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 1993, 56:337-344.
39. Cameron H.A., Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994, 61:203-209.
40. Cameron H.A., McEwen B.S., Gould E. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. Journal of Neuroscience 1995, 15:4687-4692.
41. Cameron H.A., Tanapat P., Gould E. Adrenal steroids and N-methyl-d-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 1998, 82:349-354.
42. Cameron H.A., McKay R.D. Restoring production of hippocampal neurons in old age. Nature Neuroscience 1999, 2:894-897.
43. Cameron H.A., McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. Journal of Comparative Neurology 2001, 435:406-417.
44. Campbell S., MacQueen G. The role of the hippocampus in the pathophysiology of major depression. Journal of Psychiatry and Neuroscience 2004, 29:417-426.
45. Carlén M., Cassidy R.M., Brismar H., Smith G.A., Enquist L.W., Frisén J. Functional integration of adult-born neurons. Current Biology 2002, 12:606-608.
46. Carleton A., Petreanu L.T., Lansford R., Alvarez-Buylla A., Lledo P.M. Becoming a new neuron in the adult olfactory bulb. Nature Neuroscience 2003, 6:507-518.
47. Carter C.S., Witt D.M., Manock S.R., Adams K.A., Bahr J.M., Carlstead K. Hormonal correlates of sexual behavior and ovulation in male-induced and postpartum estrus in female prairie voles. Physiology and Behavior 1989, 46:941-948.
48. Chen T.L. Inhibition of growth and differentiation of osteoprogenitors in mouse bone marrow stromal cell cultures by increased donor age and glucocorticoid treatment. Bone 2004, 35:83-95.
49. Chiba S., Suzuki M., Yamanouchi K., Nishihara M. Involvement of granulin in estrogen-induced neurogenesis in the adult rat hippocampus. Journal of Reproduction and Development 2007, 53:297-307.
50. Christie B.R., Cameron H.A. Neurogenesis in the adult hippocampus. Hippocampus 2006, 16:199-207.
51. Clulow F.V., Mallory F.F. Oestrus and induced ovulation in the meadow vole. Microtus pennsylvanicus. Journal of Reproduction and Fertility 1970, 23:341-343.
52. Coe C.L., Kramer M., Czeh B., Gould E., Reeves A.J., Kirschbaum C., Fuchs E. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biological Psychiatry 2003, 54:1025-1034.
53. Conrad C.D., Galea L.A., Kuroda Y., McEwen B.S. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behavioral Neuroscience 1996, 110:1321-1334.
54. Contestabile A., Ciani E. Role of nitric oxide in the regulation of neuronal proliferation, survival and differentiation. Neurochemistry International 2004, 45:903-914.
55. Couillard-Despres S., Winner B., Karl C., et al. Targeted transgene expression in neuronal precursors: Watching young neurons in the old brain. European Journal of Neuroscience 2006, 24:1535-1545.
56. Cull-Candy S., Brickley S., Farrant M. NMDA receptor subunits: Diversity, development and disease. Current Opinion in Neurobiology 2001, 11(3):327-335.
57. Dalla C., Edgecomb C., Whetstone A.S., Shors T.J. Females do not express learned helplessness like males do. Neuropsychopharmacology 2007, 33(7):1559-1569.
58. Daniel J.M., Roberts S.L., Dohanich G.P. Effects of ovarian hormones and environment on radial maze and water maze performance of female rats. Physiology and Behavior 1999, 66:11-20.
59. Darnaudéry M., Perez-Martin M., Del Favero F., Gomez-Roldan C., Garcia-Segura L.M., Maccari S. Early motherhood in rats is associated with a modification of hippocampal function. Psychoneuroendocrinology 2007, 32(7):803-812.
60. Dayer A.G., Ford A.A., Cleaver K.M., Yassaee M., Cameron H.A. Short-term and long-term survival of new neurons in the rat dentate gyrus. Journal of Comparative Neurology 2003, 460:563-572.
61. Deak T., Nguyen K.T., Cotter C.S., Fleshner M., Watkins L.R., Maier S.F., Spencer R.L. Long-term changes in mineralocorticoid and glucocorticoid receptor occupancy following exposure to an acute stressor. Brain Research 1999, 847:211-220.
62. De Kloet E.R. Stress in the brain. European Journal of Pharmacology 2000, 405:187-198.
63. Dong H., Goico B., Martin M., Csernansky C.A., Bertchume A., Csernansky J.G. Modulation of hippocampal cell proliferation, memory, and amyloid plaque deposition in APPsw (Tg2576) mutant mice by isolation stress. Neuroscience 2004, 127:601-609.
64. Doetsch F., Alvarez-Buylla A. Network of tangential pathways for neuronal migration in adult mammalian brain. Proceedings of the National Academy of Sciences of the United States of America 1996, 93(25):14895-14900.
65. Drapeau E., Mayo W., Aurousseau C., Le Moal M., Piazza P.V., Abrous D.N. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:14385-14390.
66. Droste S.K., Gesing A., Ulbricht S., Muller M.B., Linthorst A.C., Reul J.M. Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis. Endocrinology 2003, 144:3012-3023.
67. Dupret D., Montaron M.F., Drapeau E., Aurousseau C., Le Moal M., Piazza P.V., Abrous D.N. Methylazoxymethanol acetate does not fully block cell genesis in the young and aged dentate gyrus. European Journal of Neuroscience 2005, 22:778-783.
68. Eichenbaum H. Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron 2004, 44:109-120.
69. Eisch A.J., Mandyam C.D. Adult neurogenesis: Can analysis of cell cycle proteins move us "Beyond BrdU"?. Current Pharmaceutical Biotechnology 2007, 8:147-165.
70. Epp J.R., Spritzer M.D., Galea L.A. Hippocampus-dependent learning promotes survival of new neurons in the dentate gyrus at a specific time during cell maturation. Neuroscience 2007, 149:273-285.
71. Eriksson P.S., Perfilieva E., Björk-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nature Medicine 1998, 4:1313-1317.
72. Esposito M.S., Piatti V.C., Laplagne D.A., Morgenstern N.A., Ferrari C.C., Pitossi F.J., Schinder A.F. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. Journal of Neuroscience 2005, 25:10074-10086.
73. Falconer E.M., Galea L.A. Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats. Brain Research 2003, 975:22-36.
74. Feng R., Rampon C., Tang Y.P., et al. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 2001, 32:911-926.
75. Fester L., Ribeiro-Gouveia V., Prange-Kiel J., von Schassen C., Böttner M., Jarry H., Rune G.M. Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis. Journal of Neurochemistry 2006, 97(4):1136-1144.
76. Finkelstein M., Weidenfeld J., Ne'eman Y., Samuni A., Mizrachi Y., Ben-Uzilio R. Comparative studies of the aromatization of testosterone and epitestosterone by human placental aromatase. Endocrinology 1981, 108(3):943-947.
77. Fischer A.K., von Rosenstiel R.P., Fuchs E., Goula D., Almeida O.F., Czeh B. The prototypic mineralocorticoid receptor agonist aldosterone influences neurogenesis in the dentate gyrus of the adrenalectomized rat. Brain Research 2002, 947:290-293.
78. Fowler C.D., Freeman M.E., Wang Z. Newly proliferated cells in the adult male amygdala are affected by gonadal steroid hormones. Journal of Neurobiology 2003, 57(3):257-269.
79. Francis F., KoulakoffA., Boucher D., et al. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 1999, 23:247-256.
80. Frye C.A. Estrus-associated decrements in a water maze task are limited to acquisition. Physiology and Behavior 1995, 57:5-14.
81. Fuchs E., Flugge G., Ohl F., Lucassen P., Vollmann-Honsdorf G.K., Michaelis T. Psychosocial stress, glucocorticoids, and structural alterations in the tree shrew hippocampus. Physiology and Behavior 2001, 73:285-291.
82. Fumagalli F., Molteni R., Racagni G., Riva M.A. Stress during development: Impact on neuroplasticity and relevance to psychopathology. Progress in Neurobiology 2007, 81:197-217.
83. Furuta M., Bridges R.S. Gestation-induced cell proliferation in the rat brain. Brain Research - Developmental Brain Research 2005, 156:61-66.
84. Gage F.H. Mammalian neural stem cells. Science 2000, 287:1433-1438.
85. Gage F.H., Ray J., Fisher L.J. Isolation, characterization and use of stem cells from the CNS. Annual Review of Neuroscience 1995, 18:159-192.
86. Gahr M. Sexual differentiation of the vocal control system of birds. Advances in Genetics 2007, 59:67-105.
87. Galea L.A. Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Research Reviews 2007, 57:332-341.
88. Galea L.A., McEwen B.S. Sex and seasonal differences in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 1999, 89(3):955-964.
89. Galea L.A., Spritzer M.D., Barker J.M., Pawluski J.L. Gonadal hormone modulation of hippocampal neurogenesis in the adult. Hippocampus 2006, 16(3):225-232.
90. Galea L.A., Wide J.K., Paine T.A., Holmes M.M., Ormerod B.K., Floresco S.B. High levels of estradiol disrupt conditioned place preference learning, stimulus response learning and reference memory but have limited effects on working memory. Behavioural Brain Research 2001, 126(1-2):115-126.
91. Galea L.A.M., Kavaliers M., Ossenkopp K.-P. Sexually dimorphic spatial learning in meadow voles. Microtus pennsylvanicus and deer mice, Peromyscus maniculatus. Journal of Experimental Biology 1996, 199:195-200.
92. Galea L.A.M., McEwen B.S., Tanapat P., Deak T., Spencer R.L., Dhabar F.S. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 1997, 81:689-697.
93. Garcia A., Steiner B., Kronenberg G., Bick-Sander A., Kempermann G. Age-dependent expression of glucocorticoid and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 2004, 3:363-371.
94. Gerlach J.L., McEwen T. Rat brain binds adrenal steroid hormone: Radioautography of hippocampus with corticosterone. Science 1980, 175:1133-1136.
95. Gerlach, Aurich J.E. Regulation of seasonal reproductive activity in the stallion, ram and hamster. Animal Reproduction Science 2000, 58:197-213.
96. Gleeson R.G., Lin P.T., Flanagan L.A., Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999, 23:257-271.
97. Gould E., Woolley C.S., Cameron H.A., Daniels D.C., McEwen B.S. Adrenal steroids regulate postnatal development of the rat dentate gyrus: II. Effects of glucocorticoids and mineralocorticoids on cell birth. Journal of Comparative Neurology 1991, 313:486-493.
98. Gould E., Cameron H.A. The regulation of neuronal birth, migration and death in the rat dentate gyrus. Developmental Neuroscience (B.A.S.E.L) 1996, 18:22-35.
99. Gould E., McEwen B.S., Tanapat P., Galea L.A.M., Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. Journal of Neuroscience 1997, 17:2492-2498.
100. Gould E., Tanapat P., McEwen B.S., Flugge G., Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:3168-3171.
101. Gould E., Beylin A., Tanapat P., Reeves A., Shors T.J. Learning enhances adult neurogenesis in the hippocampal formation. Nature Neuroscience 1999, 2:260-265.
102. Gould E., Tanapat P., Rydel T., Hastings N. Regulation of hippocampal neurogenesis in adulthood. Biological Psychiatry 2000, 48(8):715-720.
103. Gould E., Vail N., Wagers M., Gross C.G. Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:10910-10917.
104. Gould E. How widespread is adult neurogenesis in mammals?. Nature Reviews Neuroscience 2007, 8(6):481-488.
105. Green A., Galea L.A. Adult hippocampal cell proliferation is suppressed with estrogen withdrawal after a hormone-simulated pregnancy. Hormones and Behavior 2008, 54:203-211.
106. Gregus A., Wintink A.J., Davis A.C., Kalynchuk L.E. Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behavioural Brain Research 2005, 156:105-114.
107. Guerra-Araiza C., Villamar-Cruz O., González-Arenas A., Chavira R., Camacho-Arroyo I. Changes in progesterone receptor isoforms content in the rat brain during the oestrous cycle and after oestradiol and progesterone treatments. Journal of Neuroendocrinology 2003, 15(10):984-990.
108. Hagihara K., Hirata S., Osada T., Hirai M., Kato J. Distribution of cells containing progesterone receptor mRNA in the female rat di- and telencephalon. An in situ hybridization study. Brain Research - Molecular Brain Research 1992, 14(3):239-249.
109. Hairston I.S., Little M.T., Scanlon M.D., Barakat M.T., Palmer T.D., Sapolsky R.M., Heller H.C. Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning. Journal of Neurophysiology 2005, 94:4224-4233.
110. Hamilton J.A., Halbreich U. Special aspects of neuropsychiatric illness in women: With a focus on depression. Annuual Review of Medicine 1993, 44:355-364.
111. Hastings N.B., Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. Journal of Comparative Neurology 1999, 413:146-154.
112. Hastings N.B., Gould E. Neurons inhibit neurogenesis. Nature Medicine 2003, 9:264-266.
113. Hattiangady B., Shetty A.K. Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiology of Aging 2008, 29(1):129-147.
114. Hayes N.L., Nowakowski R.S. Exploiting the dynamics of S-phase tracers in developing brain: Interkinetic nuclear migration for cells entering versus leaving the S-phase. Developmental Neuroscience 2000, 22:44-55.
115. Hayes N.L., Nowakowski R.S. Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Developmental Brain Research 2002, 134:77-85.
116. Heine V.M., Maslam S., Zareno J., Joels M., Lucassen P.J. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. European Journal of Neuroscience 2004, 19:131-144.
117. Herrick S.P., Waters E.M., Drake C.T., McEwen B.S., Milner T.A. Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus. Brain Research 2006, 1121:46-58.
118. Hildebrandt K., Teuchert-Noodt G., Dawirs R.R. A single neonatal dose of methamphetamine suppresses dentate granule cell proliferation in adult gerbils which is restored to control values by acute doses of haloperidol. Journal of Neural Transmission 1999, 106:549-558.
119. Hoffman G.E., Merchenthaler I., Zup S.L. Neuroprotection by ovarian hormones in animal models of neurological disease. Endocrine 2006, 29(2):217-231.
120. Hojo Y., Hattori T.A., Enami T., et al. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(3):865-870.
121. Holmes M.M., Galea L.A. Defensive behavior and hippocampal cell proliferation: Differential modulation by naltrexone during stress. Behavioral Neuroscience 2002, 116:160-168.
122. Holmes M.M., Galea L.A., Mistlberger R.E., Kempermann G. Adult hippocampal neurogenesis and voluntary running activity: Circadian and dose-dependent effects. Journal of Neuroscience Research 2004, 76:216-222.
123. Huang L.Y., DeVries G.J., Bittman E.L. Photoperiod regulates neuronal bromodeoxyuridine labeling in the brain of a seasonally breeding mammal. Journal of Neurobiology 1998, 36:410-420.
124. Huang G.J., Herbert J. Serotonin modulates the suppressive effects of corticosterone on proliferating progenitor cells in the dentate gyrus of the hippocampus in the adult rat. Neuropsychopharmacology 2005, 30:231-241.
125. Huang G.J., Herbert J. Stimulation of neurogenesis in the hippocampus of the adult rat by fluoxetine requires rhythmic change in corticosterone. Biological Psychiatry 2006, 59:619-624.
126. Isgor C., 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 2005, 134(3):847-856.
127. Jamieson P.M., Fuchs E., Flugge G., Seckl J.R. Attenuation of hippocampal 11beta-hydroxysteroid dehydrogenase type 1 by chronic psychosocial stress in the tree shrew. Stress 1997, 2:123-132.
128. Jessberger S., Kempermann G. Adult-born hippocampal neurons mature into activity-dependent responsiveness. European Journal of Neuroscience 2003, 18:2707-2712.
129. Jessberger S., Nakashima K., Clemenson G.D., et al. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. Journal of Neuroscience 2007, 27:5967-5975.
130. Jin K., Peel A.L., Mao X.O., Xie L., Cottrell B.A., Henshall D.C., Greenberg D.A. Increased hippocampal neurogenesis in Alzheimer's disease. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(1):343-347.
131. Jin M., Jin F., Zhang L., Chen Z., Huang H. Two estrogen replacement therapies differentially regulate expression of estrogen receptors alpha and beta in the hippocampus and cortex of ovariectomized rat. Brain Research - Molecular Brain Research 2005, 142(2):107-114.
132. Joels M., Karst H., Alfarez D., et al. Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 2004, 7:221-231.
133. Kajantie E., Phillips D.I. The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 2006, 31:151-178.
134. Kalita K., Szymczak S., Kaczmarek L. Non-nuclear estrogen receptor beta and alpha in the hippocampus of male and female rats. Hippocampus 2005, 15(3):404-412.
135. Kalynchuk L.E., Gregus A., Boudreau D., Perrot-Sinal T.S. Corticosterone increases depression-like behavior, with some effects on predator odor-induced defensive behavior, in male and female rats. Behavioral Neuroscience 2004, 118:1365-1377.
136. Kambo J.S., Galea L.A. Activational levels of androgens influence risk assessment behaviour but do not influence stress-induced suppression in hippocampal cell proliferation in adult male rats. Behavioural Brain Research 2006, 175(2):263-270.
137. Kaplan M.S., Hinds J.W. Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs. Science 1977, 197:1092-1094.
138. Karishma K.K., Herbert J. Dehydroepiandrosterone (DHEA) stimulates neurogenesis in the hippocampus of the rat, promotes survival of newly formed neurons and prevents corticosterone-induced suppression. European Journal of Neuroscience 2002, 16(3):445-453.
139. Kee N., Sivalingam S., Boonstra R., Wojtowicz J.M. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. Journal of Neuroscience Methods 2002, 115:97-105.
140. Kee N., Teixeira C.M., Wang A.H., Frankland P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nature Neuroscience 2007, 10:355-362.
141. Keith J.R., Wu Y., Epp J.R., Sutherland R.J. Fluoxetine and the dentate gyrus: Memory, recovery of function, and electrophysiology. Behavioural Pharmacology 2007, 18:521-531.
142. Kempermann G., Gast D., Kronenberg G., Yamaguchi M., Gage F.H. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 2003, 130:391-399.
143. Kempermann G., Jessberger S., Stiner B., Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends in Neurosciences 2004, 27:447-452.
144. Kempermann G., Kuhn H.G., Gage F.H. Experience-induced neurogenesis in the senescent dentate gyrus. Journal of Neuroscience 1998, 18:3206-3212.
145. Kim J.B., Ju J.Y., Kim J.H., Kim T.Y., Yang B.H., Lee Y.S., Son H. Dexamethasone inhibits proliferation of adult hippocampal neurogenesis in vivo and in vitro. Brain Research 2004, 1027:1-10.
146. Klempin F., Kempermann G. Adult hippocampal neurogenesis and aging. European Archives of Psychiatry and Clinical Neuroscience 2007, 257(5):271-280.
147. Koike S., Sakai M., Muramatsu M. Molecular cloning and characterization of rat estrogen receptor cDNA. Nucleic Acids Research 1987, 15(6):2499-2513.
148. Konradi C., Heckers S. Molecular aspects of glutamate dysregulation: Implications for schizophrenia and its treatment. Pharmacy and Therapeutics 2003, 97(2):153-179.
149. Koo J.W., Park C.H., Choi S.H., Kim N.J., Kim H.S., Choe J.C., Suh Y.H. The postnatal environment can counteract prenatal effects on cognitive ability, cell proliferation, and synaptic protein expression. Federation of American Societies for Experimental Biology 2003, 17:1556-1558.
150. Krugers H.J., van der Linden S., van Olst E., Alfarez D.N., Maslam S., Lucassen P.J., Joels M. Dissociation between apoptosis, neurogenesis, and synaptic potentiation in the dentate gyrus of adrenalectomized rats. Synapse 2007, 61:221-230.
151. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. Journal of Neuroscience 1996, 16(6):2027-2033.
152. Kuiper G.J.M., Enmark E., Pelto-Huikko M., Nilsson S., Gustafsson J. Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:5925-5930.
153. Kulkarni V.A., Jha S., Vaidya V.A. Depletion of norepinephrine decreases the proliferation, but does not influence the survival and differentiation, of granule cell progenitors in the adult rat hippocampus. European Journal of Neuroscience 2002, 16:2008-2012.
154. Lagace D.C., Fischer S.J., Eisch A.J. Gender and endogenous levels of estradiol do not influence adult hippocampal neurogenesis in mice. Hippocampus 2007, 17:175-180.
155. Laplagne D.A., Kamienkowski J.E., Espósito M.S., Piatti V.C., Zhao C., Gage F.H., Schinder A.F. Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. European Journal of Neuroscience 2007, 25:2973-2981.
156. Lathe R. Hormones and the hippocampus. Journal of Endocrinology 2001, 169:205-231.
157. Lavenex P., Steele M.A., Jacobs L.F. The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels. European Journal of Neuroscience 2000, 12:643-648.
158. Lee H.J., Kim J.W., Yim S.V., et al. Fluoxetine enhances cell proliferation and prevents apoptosis in dentate gyrus of maternally separated rats. Molecular Psychiatry 2001, 6:725-728.
159. Lee K.J., Kim S.J., Kim S.W., et al. Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Experimental and Molecular Medicine 2006, 38:44-54.
160. Lee K.S., Lim B.V., Jang M.H., et al. Hypothermia inhibits cell proliferation and nitric oxide synthase expression in rats. Neuroscience Letters 2002, 329:53-56.
161. Lehmann K., Butz M., Teuchert-Noodt G. Offer and demand: Proliferation and survival of neurons in the dentate gyrus. European Journal of Neuroscience 2005, 21:3205-3216.
162. Lemaire V., Aurousseau C., Moal M.L., Abrous D.N. Behavioral trait of reactivity to novelty is related to hippocampal neurogenesis. European Journal of Neuroscience 1999, 11:4006-4014.
163. Lemaire V., Koehl M., Le Moal M., Abrous D.N. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:11032-11037.
164. Lemaire V., Lamarque S., Le Moal M., Piazza P.V., Abrous D.N. Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biological Psychiatry 2006, 59:786-792.
165. Leuner B., Mendolia-Loffredo S., Kozorovitskiy Y., Samburg D., Gould E., Shors T.J. Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. Journal of Neuroscience 2004, 24:7477-7481.
166. Leuner B., Mirescu C., Noiman L., Gould E. Maternal experience inhibits the production of immature neurons in the hippocampus during the postpartum period through elevations in adrenal steroids. Hippocampus 2007, 17:434-442.
167. Levine S. Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. European Journal of Pharmacology 2000, 405:149-160.
168. Levin-Allerhand J.A., Lominska C.E., Wang J., Smith J.D. 17α-Estradiol and 17β-estradiol treatments are effective in lowering cerebral amyloid-β levels in AβPPSWE transgenic mice. Journal of Alzheimer's Disease 2002, 4:449-457.
169. Lightman S.L., Windle R.J., Wood S.A., Kershaw Y.M., Shanks N., Ingram C.D. Peripartum plasticity within the hypothalamo-pituitary-adrenal axis. Progress in Brain Research 2001, 133:111-129.
170. Lindsey B.W., Tropepe V. A comparative framework for understanding the biological principles of adult neurogenesis. Progress in Neurobiology 2006, 80:281-307.
171. Linford N., Wade C., Dorsa D. The rapid effects of estrogen are implicated in estrogen-mediated neuroprotection. Journal of Neurocytology 2000, 29(5-6):367-374.
172. Liu D., Diorio J., Day J.C., Francis D.D., Meaney M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neuroscience 2000, 3:799-806.
173. Liu S.H., Wang J., Zhu D.Y., Fu Y.P., Lukowiak K., Lu V.M. Generation of functional inhibitory neurons in the adult rat hippocampus. Journal of Neuroscience 2003, 23:732-736.
174. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148.
175. Luine V.N., Beck K.D., Bowman R.E., Frankfurt M., Maclusky N.J. Chronic stress and neural function: Accounting for sex and age. Journal of Neuroendocrinology 2007, 19:743-751.
176. Luine V.N., Jacome L.F., MacLusky N.J. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 2003, 144(7):2836-2844.
177. Luo C.X., Jiang J., Zhou Q.G., et al. Voluntary exercise-induced neurogenesis in the postischemic dentate gyrus is associated with spatial memory recovery from stroke. Journal of Neuroscience Research 2007, 85:1637-1646.
178. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993, 11:173-189.
179. Lynch M.A. Long-term potentiation and memory. Physiological Reviews 2004, 84:87-136.
180. Maccari S., Darnaudery M., Morley-Fletcher S., Zuena A.R., Cinque C., Van Reeth O. Prenatal stress and long-term consequences: Implications of glucocorticoid hormones. Neuroscience and Biobehavioral Reviews 2003, 27:119-127.
181. MacLusky N.J., Luine V.N., Hajszan T., Leranth C. The 17α and 17β isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats. Endocrinology 2005, 146(1):287-293.
182. Mak G.K., Enwere E.K., Gregg C., Pakarainen T., Poutanen M., Huhtaniemi I., Weiss S. Male pheromone-stimulated neurogenesis in the adult female brain: Possible role in mating behavior. Nature Neuroscience 2007, 10(8):1003-1011.
183. Malberg J.E. Implications of adult hippocampal neurogenesis in anti-depressant action. Journal of Psychiatry and Neuroscience 2004, 29:196-205.
184. Malberg J.E., Duman R.S. Cell proliferation in adult hippocampus is decreased by inescapable stress: Reversal by fluoxetine treatment. Neuropsychopharmacology 2003, 28:1562-1571.
185. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. Journal of Neuroscience 2000, 20:9104-9110.
186. Mandyam C.D., Harburg G.C., Eisch A.J. Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zone. Neuroscience 2007, 146:108-122.
187. Manganas L.N., Zhang X., Li Y., et al. Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science 2007, 318:980-985.
188. Markakis E.A., Gage F.H. Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. Journal of Comparative Neurology 1999, 406:449-460.
189. Marshall G.P., Reynolds B.A., Laywell E.D. Using the neurosphere assay to quantify neural stem cells in vivo. Current Pharmaceutical Biotechnology 2007, 8:141-145.
190. Mastorakos G., Sakkas E.G., Xydakis A.M., Creatsas G. Pitfalls of the WHIs: Women's health initiative. Annals of the New York Academy of Sciences 2006, 1092:331-340.
191. Mayer J.L., Klumpers L., Maslam S., de Kloet E.R., Joels M., Lucassen P.J. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalises the corticosterone-induced reduction of adult hippocampal neurogenesis. Journal of Neuroendocrinology 2006, 18:629-631.
192. Mayo W., Lemaire V., Malaterre J., et al. Pregnenolone sulfate enhances neurogenesis and PSA-NCAM in young and aged hippocampus. Neurobiology of Aging 2005, 26:103-114.
193. Mazzucco C.A., Lieblich S.E., Bingham B.I., Williamson M.A., Viau V., Galea L.A. Both estrogen receptor alpha and estrogen receptor beta agonists enhance cell proliferation in the dentate gyrus of adult female rats. Neuroscience 2006, 141(4):1793-1800.
194. McConkey D.J., Nicotera P., Hartzell P., Bellomo G., Wyllie A.H., Orrenius S. Glucocorticoids activate a suicide process in thymocytes through an elevation of cytosolic Ca2+ concentration. Archives of Biochemistry and Biophysics 1989, 269:365-370.
195. McDonald R.J., King A.L., Wasiak T.D., Zelinski E.L., Hong N.S. A complex associative structure formed in the mammalian brain during acquisition of a simple visual discrimination task: Dorsolateral striatum, amygdala, and hippocampus. Hippocampus 2007, 17:759-774.
196. McEwen B.S. Corticosteroids and hippocampal plasticity. Annals of the New York Acadamy of Sciences 1994, 746:134-142.
197. McEwen B.S., Weiss J.M., Schwartz B.S. Selective retention of corticosterone by limbic structure in rat brain. Nature 1968, 220:911-912.
198. McEwen, Milner T.A. Hippocampal formation: Shedding light on the influence of sex and stress on the brain. Brain Research Reviews 2007, 55(2):343-355.
199. McKay R. Stem cells in the central nervous system. Science 1997, 276:66-71.
200. Meshi D., Drew M.R., Saxe M., et al. Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nature Neuroscience 2006, 9:729-731.
201. Miller M.W., Nowakowski R.S. Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Research 1988, 457:44-52.
202. Mirescu C., Gould E. Stress and adult neurogenesis. Hippocampus 2006, 16:233-238.
203. Mirescu C., Peters J.D., Gould E. Early life experience alters response of adult neurogenesis to stress. Nature Neuroscience 2004, 7:841-846.
204. Mirescu C., Peters J.D., Noiman L., Gould E. Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:19170-19175.
205. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302:1760-1765.
206. Montaron M.F., Drapeau E., Dupret D., et al. Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiology of Aging 2006, 27:645-654.
207. Montaron M.F., Koehl M., Lemaire V., Drapeau E., Abrous D.N., Le Moal M. Environmentally induced long-term structural changes: Cues for functional orientation and vulnerabilities. Neurotoxicity Research 2004, 6:571-580.
208. Montaron M.F., Piazza P.V., Aurousseau C., Urani A., Le Moal M., Abrous D.N. Implication of corticosteroid receptors in the regulation of hippocampal structural plasticity. European Journal of Neuroscience 2003, 18:3105-3111.
209. Naftolin F., Horvath T.L., Jakab R.L., Leranth C., Harada N., Balthazart J. Aromatase immunoreactivity in axon terminals of the vertebrate brain. An immunocytochemical study on quail, rat, monkey and human tissues. Neuroendocrinology 1996, 63:149-155.
210. Nagy A.I., Ormerod B.K., Mazzucco C., Galea L.A.M. Estradiol-induced enhancement in cell proliferation is mediated through estrogen receptors in the dentate gyrus of adult female rats. Drug Development Research 2005, 66:142-149.
211. Nichols N.R., Zieba M., Bye N. Do glucocorticoids contribute to brain aging?. Brain Research Reviews 2001, 37:273-286.
212. Nilsson M., Perfilieva E., Johansson U., Orwar O., Eriksson P.S. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. Journal of Neurobiology 1999, 39:569-578.
213. Nottebohm F. Neuronal replacement in adult brain. Brain Research Bulletin 2002, 57(6):737-749.
214. Nowakowski R.S., Lewin S.B., Miller M.W. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. Journal of Neurocytology 1989, 18:311-318.
215. Olariu A., Cleaver K.M., Cameron H.A. Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. Journal of Comparative Neurology 2007, 501(4):659-667.
216. Olariu A., Cleaver K.M., Shore L.E., Brewer M.D., Cameron H.A. A natural form of learning can increase and decrease the survival of new neurons in the dentate gyrus. Hippocampus 2005, 15:750-762.
217. Olson A.K., Eadie B.D., Ernst C., Christie B.R. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 2006, 16:250-260.
218. Ormerod B.K., 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 2001, 102:369-379.
219. Ormerod B.K., Galea L.A. Reproductive status influences the survival of new cells in the dentate gyrus of adult male meadow voles. Neuroscience Letters 2003, 346(1-2):25-28.
220. Ormerod B.K., Falconer E.M., Galea L.A. N-methyl-D-aspartate receptor activity and estradiol: Separate regulation of cell proliferation in the dentate gyrus of adult female meadow vole. Journal of Endocrinology 2003, 179(2):155-163.
221. Ormerod B.K., Lee T.T., Galea L.A. Estradiol initially enhances but subsequently suppresses (via adrenal steroids) granule cell proliferation in the dentate gyrus of adult female rats. Journal of Neurobiology 2003, 55(2):247-260.
222. Ormerod B.K., Lee T.T., Galea L.A. Estradiol enhances neurogenesis in the dentate gyri of adult male meadow voles by increasing the survival of young granule neurons. Neuroscience 2004, 128:645-654.
223. Overstreet-Wadiche L.S., Westbrook G.L. Functional maturation of adult-generated granule cells. Hippocampus 2006, 16:208-215.
224. Packard D.S., Menzies R.A., Skalko R.G. Incorporation of thymidine and its analogue, bromodeoxyuridine, into embryos and maternal tissues of the mouse. Differentiation 1973, 1:397-404.
225. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. Journal of Neuroscience 1997, 17:3727-3738.
226. Parker K.J., Schatzberg A.F., Lyons D.M. Neuroendocrine aspects of hypercortisolism in major depression. Hormones and Behavior 2003, 43:60-66.
227. Pawluski J.L., Galea L.A. Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam. Neuroscience 2007, 149:53-67.
228. Perez E.J., Cai Y.C., Covey D.F., Simpkins J.W. Neuroprotective effects of estratriene analogs: Structure-activity relationships and molecular optimization. Drug Development Research 2006, 66:78-92.
229. Perez-Martin M., Azcoitia I., Trejo J.L., Sierra A., 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. European Journal of Neuroscience 2003, 18(4):923-930.
230. Perez-Martin M., Salazar V., Castillo C., Ariznavarreta C., Azcoitia I., Garcia-Segura L.M., Tresguerres J.A. Estradiol and soy extract increase the production of new cells in the dentate gyrus of old rats. Experimental Gerontology 2005, 40:450-453.
231. Pham K., Nacher J., Hof P.R., McEwen B.S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. European Journal of Neuroscience 2003, 17:879-886.
232. Prickaerts J., Koopmens G., Blokland A., Scheepens A. Learning and adult neurogenesis: Survival with or without proliferation?. Neurobiology of Learning and Memory 2004, 81:1-11.
233. Ramirez-Amaya V., Marrone D.F., Gage F.H., Worley P.F., Barnes C.A. Integration of new neurons into functional neural networks. Journal of Neuroscience 2006, 26:12237-12241.
234. Rannevik G., Jeppsson S., Johnell O., Bjerre B., Laurell-Borulf Y., Svanberg L. A longitudinal study of the perimenopausal transition: Altered profiles of steroid and pituitary hormones, SHBG and bone mineral density. Maturitas 1995, 21(2):103-113.
235. Rao M.S., Hattiangady B., Abdel-Rahman A., Stanley D.P., Shetty A.K. Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. European Journal of Neuroscience 2005, 21:464-476.
236. Rao M.S., Hattiangady B., Shetty A.K. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 2006, 5:545-558.
237. Rao M.S., Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. European Journal of Neuroscience 2004, 19:234-246.
238. Reul J.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology 1985, 117:2505-2511.
239. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255:1707-1710.
240. Rochefort C., Gheusi G., Vincent J.D., Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. Journal of Neuroscience 2002, 22:2679-2689.
241. Roky R., Paut-Pagano L., Goffin V., Kitahama K., Valatx J.L., Kelly P.A., Jouvet M. Distribution of prolactin receptors in the rat forebrain. Immunohistochemical study. Neuroendocrinology 1996, 63(5):422-429.
242. Rosenblatt J.S., Mayer A.D., Giordano A.L. Hormonal basis during pregnancy for the onset of maternal behavior in the rat. Psychoneuroendocrinology 1988, 13:29-46.
243. Santarelli L., Saxe M., Gross C., et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003, 301:805-809.
244. Sapolsky R.M., Meaney M.J. Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Research 1986, 396:64-76.
245. Saravia F., Beauquis J., Pietranera L., DeNicola A.F. Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice. Psychoneuroendocrinology 2007, 32(5):480-492.
246. Saxe M.D., Battaglia F., Wang J.W., et al. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:17501-17506.
247. Schmidt M.H.H., Broll R., Bruch H.P., Bogler O., Duchrow K. The proliferation marker pKi-67 organizes the nucleolus during the cell cycle depending on Ran and cyclin B. Journal of Pathology 2003, 199:18-27.
248. Schmidt-Hieber C., Jonas P., Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 2004, 429:184-187.
249. Schmitz C., Rhodes M.E., Bludau M., et al. Depression: Reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress. Molecular Psychiatry 2002, 7:810-813.
250. Scholzen T., Gerdes J. The Ki-67 protein: From the known and the unknown. Journal of Cell Physiology 2000, 182:311-322.
251. Schwarz J.M., McCarthy M.M. Steroid-induced sexual differentiation of the developing brain: Multiple pathways, one goal. Journal of Neurochemistry 2008, 105(5):1561-1572.
252. Seaberg R.M., van der Kooy D. Stem and progenitor cells: The premature desertion of rigorous definitions. Trends in Neurosciences 2003, 26:125-131.
253. Seckl J.R. 11Beta-hydroxysteroid dehydrogenases: Changing glucocorticoid action. Current Opinion in Pharmacology 2004, 4:597-602.
254. Seri B., García-Verdugo J.M., McEwen B.S., Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. Journal of Neuroscience 2001, 21(18):7153-7160.
255. Sharp P.J. Photoperiodic regulation of seasonal breeding in birds. Annals of the New York Academy of Sciences 2005, 1040:189-199.
256. Shingo T., Gregg C., Enwere E., et al. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 2003, 299:117-120.
257. Shors T.J. Learning during stressful times. Learning and Memory 2004, 11:137-144.
258. Shors T.J. Stressful experience and learning across the lifespan. Annual Review of Psychology 2006, 57:55-85.
259. Shors T.J., Mathew J., Sisti H.M., Edgecomb C., BeckoffS., Dalla C. Neurogenesis and helplessness are mediated by controllability in males but not in females. Biological Psychiatry 2007, 62:487-495.
260. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001, 410:372-376.
261. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002, 12:578-584.
262. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. Journal of Comparative Neurology 1997, 388(4):507-525.
263. Sierra A. Neurosteroids: The StAR protein in the brain. Journal of Neuroendocrinology 2004, 16(9):787-793.
264. Sierra A., Lavaque E., Perez-Martin M., Azcoitia I., Hales D.B., Garcia-Segura L.M. Steroidogenic acute regulatory protein in the rat brain: Cellular distribution, developmental regulation and overexpression after injury. European Journal of Neuroscience 2003, 18(6):1458-1467.
265. Simpkins J.W., Yang S.H., Liu R., et al. Estrogen-like compounds for ischemic neuroprotection. Stroke 2004, 35:2648.
266. Singh M., Dykens J.A., Simpkins J.W. Novel mechanisms for estrogen-induced neuroprotection. Experimental Biology and Medicine (Maywood) 2006, 231(5):514-521.
267. Snyder J.S., Hong N.S., McDonald R.J., Wojtowicz J.M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005, 130:843-852.
268. Song H., Stevens C.F., Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature 2002, 417:39-44.
269. Spritzer M.D., Galea L.A. Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Developmental Neurobiology 2007, 67(10):1321-1333.
270. Stanfield B.B., Trice J.E. Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Experimental Brain Research 1988, 72:399-406.
271. Stone G.E., Miller O.J., Prescott D.M. H3-thymidine derivative pools in relation to macronuclear DNA synthesis in Tetrahymena pyriformis. Journal of Cell Biology 1965, 25:171-177.
272. Suzuki S., Brown C.M., Wise P.M. Mechanisms of neuroprotection by estrogen. Endocrinology 2006, 29(2):209-215.
273. Tabori N.E., Stewart L.S., Znamensky V., Romeo R.D., Alves S.E., McEwen B.S., Milner T.A. Ultrastructural evidence that androgen receptors are located at extranuclear sites in the rat hippocampal formation. Neuroscience 2005, 130:151-163.
274. Takahashi L.K. Prenatal stress: Consequences of glucocorticoids on hippocampal development and function. International Journal of Developmental Neuroscience 1998, 16:199-207.
275. Tanapat P., Galea L.A., Gould E. Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. International Journal of Developmental Neuroscience 1998, 16:235-239.
276. Tanapat P., Hastings N.B., Gould E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. Journal of Comparative Neurology 2005, 481(3):252-265.
277. Tanapat P., Hastings N.B., Reeves A.J., Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. Journal of Neuroscience 1999, 19:5792-5801.
278. Tanapat P., Hastings N.B., Rydel T.A., Galea L.A., Gould E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. Journal of Comparative Neurology 2001, 437:496-504.
279. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: Paradigms, pitfalls, limitations, and validation. Brain Research Reviews 2007, 53:198-214.
280. te Pas M.F., de Jong P.R., Verburg F.J. Glucocorticoid inhibition of C2C12 proliferation rate and differentiation capacity in relation to mRNA levels of the MRF gene family. Molecular Biology Reports 2000, 27:87-98.
281. Thomas R.M., Hotsenpiller G., Peterson D.A. Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. Journal of Neuroscience 2007, 27(11):2734-2743.
282. Toran-Allerand C.D. Estrogen and the brain: Beyond ER-alpha, ER-beta, and 17beta-estradiol. Annals of the New York Academy of Sciences 2005, 1052:136-144.
283. Toran-Allerand C.D., Guan X., MacLusky N.J., et al. ER-X: A novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. Journal of Neuroscience 2002, 22(19):8391-8401.
284. Toran-Allerand C.D., Tinnikov A.A., Singh R.J., Nethrapalli I.S. 17 alpha-estradiol: A brain-active estrogen?. Endocrinology 2005, 146(9):3843-3850.
285. Torbett B.E. Reporter genes: Too much of a good thing?. Journal of Gene Medicine 2002, 4:478-479.
286. Towart L.A., Alves S.E., Znamensky V., Hayashi S., McEwen B.S., Milner T.A. Subcellular relationships between cholinergic terminals and estrogen receptor-alpha in the dorsal hippocampus. Journal of Comparative Neurology 2003, 463(4):390-401.
287. Vallée M., Mayo W., Darnaudéry M., et al. Neurosteroids: Deficient cognitive performance in aged rats depends on low pregnenolone sulfate levels in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:14865-14870.
288. van der Kooy D., Weiss S. Why stem cells?. Science 2000, 287:1439-1441.
289. Van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience 1999, 2:266-270.
290. van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 2002, 415:1030-1034.
291. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. Journal of Neuroscience 2005, 25:8680-8685.
292. Veenema A.H., de Kloet E.R., de Wilde M.C., et al. Differential effects of stress on adult hippocampal cell proliferation in low and high aggressive mice. Journal of Neuroendocrinology 2007, 19:489-498.
293. Viau V., Meaney M.J. Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 1991, 129(5):2503-2511.
294. Viau V., Sharma S., Meaney M.J. Changes in plasma adrenocorticotropin, corticosterone, corticosteroid-binding globulin, and hippocampal glucocorticoid receptor occupancy/translocation in rat pups in response to stress. Journal of Neuroendocrinology 1996, 8:1-8.
295. Vollmayr B., Mahlstedt M.M., Henn F.A. Neurogenesis and depression: What animal models tell us about the link. European Archives of Psychiatry and Clinical Neuroscience 2007, 257:300-303.
296. Wade J., Arnold A.P. Sexual differentiation of the zebra finch song system. Annals of the New York Academy of Sciences 2004, 1016:540-559.
297. Walf A.A., Frye C.A. Antianxiety and antidepressive behavior produced by physiological estradiol regimen may be modulated by hypothalamic-pituitary-adrenal axis activity. Neuropsychopharmacology 2005, 30(7):1288-1301.
298. Walker C.D., Lightman S.L., Steele M.K., Dallman M.F. Suckling is a persistent stimulus to the adrenocortical system of the rat. Endocrinology 1992, 130:115-125.
299. Wang J.M., Johnston P.B., Ball B.G., Brinton R.D. The neurosteroid allopregnanolone promotes proliferation of rodent and human neural progenitor cells and regulates cell-cycle gene and protein expression. Journal of Neuroscience 2005, 25:4706-4718.
300. Wang L., Andersson S., Warner M., Gustafsson J. Morphological abnormalities in the brains of estrogen receptor β knockout mice. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(5):2792-2796.
301. Wang S., Scott B.W., Wojtowicz J.M. Heterogenous properties of dentate granule neurons in the adult rat. Journal of Neurobiology 2000, 42:248-257.
302. Warren S.G., Juraska J.M. Spatial and nonspatial learning across the rat estrous cycle. Behavioral Neuroscience 1997, 111:259-266.
303. Weiland N.G., Orikasa C., Hayashi S., McEwen B.S. Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. Journal of Comparative Neurology 1997, 388(4):603-612.
304. Weiss S., Dunne C., Hewson J., Wohl C., Wheatley M., Peterson A.C., Reynolds B.A. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. Journal of Neuroscience 1996, 16:7599-7609.
305. Westenbroek C., Den Boer J.A., Veenhuis M., Ter Horst G.J. Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Research Bulletin 2004, 64:303-308.
306. Wilbrecht L., Kirn J.R. Neuron addition and loss in the song system: Regulation and function. Annals of New York Academy of Sciences 2004, 1016:659-683.
307. Williams B.M., Luo Y., Ward C., Redd K., Gibson R., Kuczaj S.A., McCoy J.G. Environmental enrichment: Effects on spatial memory and hippocampal CREB immunoreactivity. Physiology and Behavior 2001, 73:649-658.
308. Williams M.T., Inman-Wood S.L., Morford L.L., et al. Preweaning treatment with methamphetamine induces increases in both corticosterone and ACTH in rats. Neurotoxicology and Teratology 2000, 22:751-759.
309. Wilson I.A., Puolivali J., Heikkinen T., Riekkinen P. Estrogen and NMDA receptor antagonism: Effects upon reference and working memory. European Journal of Pharmacology 1999, 381:93-99.
310. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 2006, 16:296-304.
311. Wiskott L., Rasch M.J., Kempermann G. A functional hypothesis for adult hippocampal neurogenesis: Avoidance of catastrophic interference in the dentate gyrus. Hippocampus 2006, 16:329-343.
312. Wojtowicz J.M. Irradiation as an experimental tool in studies of adult neurogenesis. Hippocampus 2006, 16:261-266.
313. Wong E.Y., Herbert J. The corticoid environment: A determining factor for neural progenitors' survival in the adult hippocampus. European Journal of Neuroscience 2004, 20:2491-2498.
314. Wong E.Y., Herbert J. Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. European Journal of Neuroscience 2005, 22:785-792.
315. Woolley C.S. Acute effects of estrogen on neuronal physiology. Annual Review of Pharmacology and Toxicology 2007, 47:657-680.
316. Woolley C.S., McEwen B.S. Role of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. Journal of Comparative Neurology 1993, 336(2):293-306.
317. Zhang J., Inazu M., Tsuji E., Yamada E., Takeda H., Matsumiya T. Neurochemical characteristics and behavioral responses to psychological stress in ovariectomized rats. Pharmacological Research 1999, 39:455-461.
318. Zhang R.L., Zhang Z.G., Lu M., Wang Y., Yang J.J., Chopp M. Reduction of the cell cycle length by decreasing G1 phase and cell cycle reentry expand neuronal progenitor cells in the subventricular zone of adult rat after stroke. Journal of Cerebral Blood Flow and Metabolism 2006, 26:857-863.
319. Zhao C., Teng E.M., Summers R.G., Ming G.L., Gage F.H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. Journal of Neuroscience 2006, 26:3-11.
320. Zhao H., Tian Z., Hao J., Chen B. Extragonadal aromatization increases with time after ovariectomy in rats. Reproductive Biology and Endocrinology 2005, 3:6.
321. Zhao L., O'Neill K., Brinton R.D. Estrogenic agonist activity of ICI 182,780 (Faslodex) in hippocampal neurons: Implications for basic science understanding of estrogen signaling and development of estrogen modulators with a dual therapeutic profile. Journal of Pharmacology and Experimental Therapeutics 2006, 319(3):1124-1132.
322. Zhu B.T., Han G., Shim J., Wen Y., Jiang X. Quantitative structure-activity relationship of various endogenous estrogen metabolites for human estrogen receptor α and β subtypes: Insights into the structural determinants favoring a differential subtype binding. Endocrinology 2006, 147(9):4132-4150.
323. Arbogast L.A., Ben-Jonathan N. The preovulatory prolactin surge: An evaluation of the role of dopamine. Endocrinology 1988, 123(6):2690-2695.
324. Dietschy J.M., Turley S.D. Cholesterol metabolism in the brain. Current Opinion in Lipidology 2001, 12:105-119.
325. Edinger K.L., Lee B., Frye C.A. Mnemonic effects of testosterone and its 5α-reduced metabolites in the conditioned fear and inhibitory avoidance tasks. Pharmacology, Biochemistry, and Behavior 2004, 78(3):559-568.
326. Frye C.A., Bayon L.E., Pursnani N.K., Purdy R.H. The neurosteroids, progesterone and 3alpha,5alpha-THP, enhance sexual motivation, receptivity, and proceptivity in female rats. Brain Research 1998, 808(1):72-83.
327. Frye C.A., McCormick C.M. Androgens are neuroprotective in the dentate gyrus of adrenalectomized female rats. Stress 2000, 3:186-194.
328. Illenchuk T.T., Walters M.R. Rat uterine progesterone receptor analyzed by [3H]R5020 photoaffinity labeling, evidence that the A and B subunits are not equimolar. Endocrinology 1997, 120:1449-1456.
329. Kajta M., Budziszewska B., Marszal M., Lason W. Effects of 17-beta estradiol and estriol on NMDA-induced toxicity and apoptosis in primary cultures of rat cortical neurons. Journal of Physiology and Pharmacology 2001, 52(3):437-446.
330. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
331. Kinsley C.H., Madonia L., Gifford W., et al. Motherhood improves learning and memory. Nature 1999, 402(6758):137-138.
332. Kus L., Handa R.J., Hautman J.M., Beitz A.J. Castration increases [125I]MK801 binding in the hippocampus of male rats. Brain Research 1995, 683:270-274.
333. Leblanc P., Crumeyrolle M., Latouche J., et al. Characterization and distribution of receptors for gonadotropin releasing hormone in the rat hippocampus. Neuroendocrinology 1988, 48:482-488.
334. Leranth C., Petnehazy O., MacLusky N.J. Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. Journal of Neuroscience 2003, 23:1588-1592.
335. Leranth C., Hajszan T., MacLusky N.J. Androgens increase spine synapse density in the CA1 hippocampal subfield of ovariectomized female rats. Journal of Neuroscience 2004, 24:495-499.
336. Lubahn D.B., Moyer J.S., Golding T.S., Couse J.F., Korach K.S., Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proceedings of the National Academy of Sciences of the United States of America 1993, 90(23):11162-11166.
337. Luine V.N., Rhodes J.C. Gonadal hormone regulation of MAO and other enzymes in hypothalamic areas. Neuroendocrinology 1983, 36(3):235-241.
338. McClelland J.L., McNaughton B.L., O'Reilly R.C. Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Physiological Reviews 1995, 102:419-457.
339. McDonnell D.P., Norris J.D. Connections and regulation of the human estrogen receptor. Science 2002, 296(5573):1642-1644.
340. Naghdi N., Nafisty N., Majilessi N. The effects of interhippocampal testosterone and flutamide on spatial localization in the Morris water maze. Brain Research 2001, 897:44-51.
341. O'Reilly R.C., McClelland J.L. Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade-off. Hippocampus 1994, 4:661-682.
342. Pawluski J.L., Vanderbyl B.L., Ragan K., 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. Behavioural Brain Research 2006, 175(1):157-165.
343. Pawluski J.L., Walker S.K., Galea L.A. Reproductive experience differentially affects spatial reference and working memory performance in the mother. Hormones and Behavior 2006, 49(2):143-149.
344. Rhodes M.E., Frye C.A. ERbeta-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks. Neurobiology of Learning and Memory 2006, 85(2):183-191.
345. Sicotte N.L., Liva S.M., Klutch R., et al. Treatment of multiple sclerosis with the pregnancy hormone estriol. Annals of Neurology 2002, 52:421-428.
346. Simerly R.B., Chang C., Muramatsu M., Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: An in situ hybridization study. Journal of Comparative Neurology 1990, 294(1):76-95.
347. Sohrabji F., Miranda R.C., Toran-Allerand C.D. Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult