The hormone therapy, Premarin, impairs hippocampus-dependent spatial learning and memory and reduces activation of new granule neurons in response to memory in female rats

Neurobiology of Aging

Volumn 34, Issue 3, 2013, Pages 986-1004

  Barha, Cindy K ^a   Galea, Liisa A M ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adult hippocampal neurogenesis; Conjugated equine estrogens; Females; Hormone therapy; immediate early genes; Premarin; Spatial reference memory; Spatial working memory; Zif268

Indexed keywords

CONJUGATED ESTROGEN; ESTRADIOL; ESTRONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN FUNCTION; BRAIN SIZE; CELL ACTIVATION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DOSE RESPONSE; DRUG EFFECT; DRUG MEGADOSE; FEMALE; GENE EXPRESSION; GRANULE CELL; HIPPOCAMPUS; LEARNING; LOCOMOTION; LOW DRUG DOSE; MEMORY CONSOLIDATION; MENOPAUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; RAT; REFERENCE MEMORY; SPATIAL MEMORY; TRAINING; WORKING MEMORY; ZIF268 GENE;

ANIMALS; BEHAVIOR, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; ESTROGENS, CONJUGATED (USP); FEMALE; HIPPOCAMPUS; MAZE LEARNING; MEMORY; NEUROGENESIS; RATS; RATS, LONG-EVANS;

EID: 84870512962     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.07.009     Document Type: Article

References (113)

1. Acosta J.I., Mayer L., Talboom J.S., Zay C., Scheldrup M., Castillo J., Demers L.M., Enders C.K., Bimonte-Nelson H.A. Premarin improves memory, prevents scopolamine-induced amnesia and increases number of basal forebrain choline acetyltransferase positive cells in middle-aged surgically menopausal rats. Horm. Behav 2009, 55:454-464.
2. Acosta J.I., Mayer L.P., Braden B.B., Nonnenmacher S., Mennenga S.E., Bimonte-Nelson H.A. The cognitive effects of conjugated equine estrogens depend on whether menopause etiology is transitional or surgical. Endocrinology 2010, 151:3795-3804.
3. Aztiria E., Capodieci G., Arancio L., Leanza G. Extensive training in a maze task reduces neurogenesis in the adult rat dentate gyrus probably as a result of stress. Neurosci. Lett 2007, 416:133-137.
4. Baddeley A. Working memory and language: an overview. J. Commun. Disord 2003, 36:189-208.
5. Bannerman D.M., Niewoehner B., Lyon L., Romberg C., Schmitt W.B., Taylor A., Sanderson D.J., Cottam J., Sprengel R., Seeburg P.H., Köhr G., Rawlins J.N. NMDA receptor subunit NR2A is required for rapidly acquired spatial working memory but not incremental spatial reference memory. J. Neurosci 2008, 28:3623-3630.
6. Barha C.K., Brummelte S., Lieblich S.E., Galea L.A. Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus 2011, 21:1216-1227.
7. Barha C.K., Dalton G.L., Galea L.A. Low doses of 17alpha-estradiol and 17beta-estradiol facilitate, whereas higher doses of estrone and 17alpha- and 17beta-estradiol impair, contextual fear conditioning in adult female rats. Neuropsychopharmacology 2010, 35:547-559.
8. Barha C.K., Galea L.A. Influence of different estrogens on neuroplasticity and cognition in the hippocampus. Biochim. Biophys. Acta 2010, 1800:1056-1067.
9. Barha C.K., Galea L.A. Motherhood alters the cellular response to estrogens in the hippocampus later in life. Neurobiol. Aging 2011, 32:2091-2095.
10. Barha C.K., Ishrat T., Epp J.R., Galea L.A., Stein D.G. Progesterone treatment normalizes the levels of cell proliferation and cell death in the dentate gyrus of the hippocampus after traumatic brain injury. Exp. Neurol 2011, 231:72-81.
11. Barha C.K., Lieblich S.E., Galea L.A. Different forms of oestrogen rapidly upregulate cell proliferation in the dentate gyrus of adult female rats. J. Neuroendocrinol 2009, 21:155-166.
12. Barha C.K., Pawluski J.L., Galea L.A. Maternal care affects male and female offspring working memory and stress reactivity. Physiol. Behav 2007, 92:939-950.
13. Barker J.M., Galea L.A. 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.
14. Baum L.W. Sex, hormones, and Alzheimer's disease. J. Gerontol. A Biol. Sci. Med. Sci 2005, 60:736-743.
15. Bhavnani B.R., Berco M., Binkley J. Equine estrogens differentially prevent neuronal cell death induced by glutamate. J. Soc. Gynecol. Investig 2003, 10:302-308.
16. Bimonte-Nelson H.A., Acosta J.I., Talboom J.S. Neuroscientists as cartographers: mapping the crossroads of gonadal hormones, memory and age using animal models. Molecules 2010, 15:6050-6105.
17. Bittner D.M., Bittner V., Riepe M.W. Verbal episodic memory and endogenous estradiol: an association in patients with mild cognitive impairment and Alzheimer's disease. Curr. Gerontol. Geriatr. Res 2011, 2011:673012.
18. Bohacek J., Daniel J.M. Increased daily handling of ovariectomized rats enhances performance on a radial-maze task and obscures effects of estradiol replacement. Horm. Behav 2007, 52:237-243.
19. Brandt M.D., Maass A., Kempermann G., Storch A. Physical exercise increases Notch activity, proliferation and cell cycle exit of type-3 progenitor cells in adult hippocampal neurogenesis. Eur. J. Neurosci 2010, 32:1256-1264.
20. Brinton R.D. Investigative models for determining hormone therapy-induced outcomes in brain: evidence in support of a healthy cell bias of estrogen action. Ann. N. Y. Acad. Sci 2005, 1052:57-74.
21. Brinton R.D. The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci 2008, 31:529-537.
22. Brinton R.D., Chen S., Montoya M., Hsieh D., Minaya J. The estrogen replacement therapy of the Women's Health Initiative promotes the cellular mechanisms of memory and neuronal survival in neurons vulnerable to Alzheimer's disease. Maturitas 2000, 34(Suppl 2):S35-S52.
23. Brown J.P., Couillard-Després S., Cooper-Kuhn C.M., Winkler J., Aigner L., Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol 2003, 467:1-10.
24. Browne C., Tobin J.R., Voytko M.L. Effects of two years of conjugated equine estrogens on cholinergic neurons in young and middle-aged ovariectomized monkeys. Brain Res 2009, 1264:13-23.
25. Brummelte S., Galea L.A. Chronic corticosterone during pregnancy and postpartum affects maternal care, cell proliferation and depressive-like behavior in the dam. Horm. Behav 2010, 58:769-779.
26. Buckner R.L. Memory and executive function in aging and AD: multiple factors that cause decline and reserve factors that compensate. Neuron 2004, 44:195-208.
27. Budziszewska B., Leśkiewicz M., Kubera M., Jaworska-Feil L., Kajta M., Lasoń W. Estrone, but not 17 beta-estradiol, attenuates kainate-induced seizures and toxicity in male mice. Exp. Clin. Endocrinol. Diabetes 2001, 109:168-173.
28. 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.
29. Chawla M.K., Guzowski J.F., Ramirez-Amaya V., Lipa P., Hoffman K.L., Marriott L.K., Worley P.F., McNaughton B.L., Barnes C.A. Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 2005, 15:579-586.
30. Chen S., Nilsen J., Brinton R.D. Dose and temporal pattern of estrogen exposure determines neuroprotective outcome in hippocampal neurons: therapeutic implications. Endocrinology 2006, 147:5303-5313.
31. Clelland C.D., Choi M., Romberg C., Clemenson G.D., Fragniere A., Tyers P., Jessberger S., Saksida L.M., Barker R.A., Gage F.H., Bussey T.J. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009, 325:210-213.
32. Daniel J.M. Effects of oestrogen on cognition: what have we learned from basic research?. J. Neuroendocrinol 2006, 18:787-795.
33. Daniel J.M., Hulst J.L., Berbling J.L. Estradiol replacement enhances working memory in middle-aged rats when initiated immediately after ovariectomy but not after a long-term period of ovarian hormone deprivation. Endocrinology 2006, 147:607-614.
34. Diaz Brinton R., Chen S., Montoya M., Hsieh D., Minaya J., Kim J., Chu H.P. The women's health initiative estrogen replacement therapy is neurotrophic and neuroprotective. Neurobiol. Aging 2000, 21:475-496.
35. Drake E.B., Henderson V.W., Stanczyk F.Z., McCleary C.A., Brown W.S., Smith C.A., Rizzo A.A., Murdock G.A., Buckwalter J.G. Associations between circulating sex steroid hormones and cognition in normal elderly women. Neurology 2000, 54:599-603.
36. Eadie B.D., Redila V.A., Christie B.R. Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. J. Comp. Neurol 2005, 486:39-47.
37. Engler-Chiurazzi E., Tsang C., Nonnenmacher S., Liang W.S., Corneveaux J.J., Prokai L., Huentelman M.J., Bimonte-Nelson H.A. Tonic Premarin dose-dependently enhances memory, affects neurotrophin protein levels and alters gene expression in middle-aged rats. Neurobiol. Aging 2011, 32:680-697.
38. Epp J.R., Haack A.K., Galea L.A. Task difficulty in the Morris water task influences the survival of new neurons in the dentate gyrus. Hippocampus 2010, 20:866-876.
39. Epp J.R., Haack A.K., Galea L.A. Activation and survival of immature neurons in the dentate gyrus with spatial memory is dependent on time of exposure to spatial learning and age of cells at examination. Neurobiol. Learn. Mem 2011, 95:316-325.
40. Epp J.R., Scott N.A., Galea L.A. Strain differences in neurogenesis and activation of new neurons in the dentate gyrus in response to spatial learning. Neuroscience 2011, 172:342-354.
41. 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. Nat. Med 1998, 4:1313-1317.
42. Espeland M.A., Rapp S.R., Shumaker S.A., Brunner R., Manson J.E., Sherwin B.B., Hsia J., Margolis K.L., Hogan P.E., Wallace R., Dailey M., Freeman R., Hays J. Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 2004, 291:2959-2968. Women's Health Initiative Memory Study.
43. Fanselow M.S., Dong H.W. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65:7-19.
44. Frick K.M. Estrogens and age-related memory decline in rodents: what have we learned and where do we go from here?. Horm. Behav 2009, 55:2-23.
45. Frick K.M., Fernandez S.M., Harburger L.L. A new approach to understanding the molecular mechanisms through which estrogens affect cognition. Biochim. Biophys. Acta 2010, 1800:1045-1055.
46. Galea L.A., Uban K.A., Epp J.R., Brummelte S., Barha C.K., Wilson W.L., Lieblich S.E., 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 2008, 62:247-260.
47. Gibbs R.B. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol. Aging 2000, 21:107-116.
48. Gibbs R.B. Estrogen therapy and cognition: a review of the cholinergic hypothesis. Endocr. Rev 2010, 31:224-253.
49. Gibbs R.B., Gabor R. Estrogen and cognition: applying preclinical findings to clinical perspectives. J. Neurosci. Res 2003, 74:637-643.
50. Gleason C.E., Schmitz T.W., Hess T., Koscik R.L., Trivedi M.A., Ries M.L., Carlsson C.M., Sager M.A., Asthana S., Johnson S.C. Hormone effects on fMRI and cognitive measures of encoding: importance of hormone preparation. Neurology 2006, 67:2039-2041.
51. Gould E., McEwen B.S., Tanapat P., Galea L.A., Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci 1997, 17:2492-2498.
52. Gundersen H.J., Jensen E.B. The efficiency of systematic sampling in stereology and its prediction. J. Microsc 1987, 147:229-263.
53. Henderson V.W. Estrogen-containing hormone therapy and Alzheimer's disease risk: understanding discrepant inferences from observational and experimental research. Neuroscience 2006, 138:1031-1039.
54. Henderson V.W. Action of estrogens in the aging brain: dementia and cognitive aging. Biochim. Biophys. Acta 2010, 1800:1077-1083.
55. Henderson V.W., Sherwin B.B. Surgical versus natural menopause: cognitive issues. Menopause 2007, 14:572-579.
56. Hogervorst E., Bandelow S. Sex steroids to maintain cognitive function in women after the menopause: a meta-analyses of treatment trials. Maturitas 2010, 66:56-71.
57. Hogervorst E., Williams J., Budge M., Riedel W., Jolles J. The nature of the effect of female gonadal hormone replacement therapy on cognitive function in post-menopausal women: a meta-analysis. Neuroscience 2000, 101:485-512.
58. Hogervorst E., Yaffe K., Richards M., Huppert F.A. Hormone replacement therapy to maintain cognitive function in women with dementia. Cochrane Database Syst. Rev 2009, 1. CD003799.
59. Jakubs K., Nanobashvili A., Bonde S., Ekdahl C.T., Kokaia Z., Kokaia M., Lindvall O. Environment matters: synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron 2006, 52:1047-1059.
60. Jessberger S., Nakashima K., Clemenson G.D., Mejia E., Mathews E., Ure K., Ogawa S., Sinton C.M., Gage F.H., Hsieh J. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J. Neurosci 2007, 27:5967-5975.
61. 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. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:343-347.
62. Joffe H., Hall J.E., Gruber S., Sarmiento I.A., Cohen L.S., Yurgelun-Todd D., Martin K.A. Estrogen therapy selectively enhances prefrontal cognitive processes: a randomized, double-blind, placebo-controlled study with functional magnetic resonance imaging in perimenopausal and recently postmenopausal women. Menopause 2006, 13:411-422.
63. 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. Nat. Neurosci 2007, 10:355-362.
64. Knowlton B.J., Shapiro M.L., Olton D.S. Hippocampal seizures disrupt working memory performance but not reference memory acquisition. Behav. Neurosci 1989, 103:1144-1147.
65. Koehl M., Abrous D.N. A new chapter in the field of memory: adult hippocampal neurogenesis. Eur. J. Neurosci 2011, 33:1101-1114.
66. Korol D.L. Role of estrogen in balancing contributions from multiple memory systems. Neurobiol. Learn. Mem 2004, 82:309-323.
67. Kronenberg G., Reuter K., Steiner B., Brandt M.D., Jessberger S., Yamaguchi M., Kempermann G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol 2003, 467:455-463.
68. Lebrun C.E., van der Schouw Y.T., de Jong F.H., Pols H.A., Grobbee D.E., Lamberts S.W. Endogenous oestrogens are related to cognition in healthy elderly women. Clin. Endocrinol. (Oxf.) 2005, 63:50-55.
69. Lee J., Duan W., Long J.M., Ingram D.K., Mattson M.P. Dietary restriction increases the number of newly generated neural cells, and induces BDNF expression, in the dentate gyrus of rats. J. Mol. Neurosci 2000, 15:99-108.
70. Maki P.M. Hormone therapy and cognitive function: is there a critical period for benefit?. Neuroscience 2006, 138:1027-1030.
71. Maki P.M., Gast M.J., Vieweg A.J., Burriss S.W., Yaffe K. Hormone therapy in menopausal women with cognitive complaints: a randomized, double-blind trial. Neurology 2007, 69:1322-1330.
72. Masoro E.J. Caloric restriction and aging: an update. Exp. Gerontol 2000, 35:299-305.
73. McNaughton B.L., Barnes C.A., Gerrard J.L., Gothard K., Jung M.W., Knierim J.J., Kudrimoti H., Qin Y., Skaggs W.E., Suster M., Weaver K.L. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J. Exp. Biol 1996, 199:173-185.
74. Olton D.S., Papas B.C. Spatial memory and hippocampal function. Neuropsychologia 1979, 17:669-682.
75. 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.
76. 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.
77. 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.
78. Park C.R., Zoladz P.R., Conrad C.D., Fleshner M., Diamond D.M. Acute predator stress impairs the consolidation and retrieval of hippocampus-dependent memory in male and female rats. Learn. Mem 2008, 15:271-280.
79. Patel N.V., Finch C.E. The glucocorticoid paradox of caloric restriction in slowing brain aging. Neurobiol. Aging 2002, 23:707-717.
80. Pawluski J.L., Brummelte S., Barha C.K., Crozier T.M., Galea L.A. Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging. Front. Neuroendocrinol 2009, 30:343-357.
81. 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. Behav. Brain Res 2006, 175:157-165.
82. Pawluski J.L., Walker S.K., Galea L.A. Reproductive experience differentially affects spatial reference and working memory performance in the mother. Horm. Behav 2006, 49:143-149.
83. Phillips S.M., Sherwin B.B. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology 1992, 17:485-495.
84. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol 2003, 463:3-33.
85. Ramírez-Rodríguez G., Klempin F., Babu H., Benítez-King G., Kempermann G. Melatonin modulates cell survival of new neurons in the hippocampus of adult mice. Neuropsychopharmacology 2009, 34:2180-2191.
86. Rapp S.R., Espeland M.A., Shumaker S.A., Henderson V.W., Brunner R.L., Manson J.E., Gass M.L., Stefanick M.L., Lane D.S., Hays J., Johnson K.C., Coker L.H., Dailey M., Bowen D. Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 2003, 289:2663-2672. WHIMS Investigators.
87. Rasgon N.L., Magnusson C., Johansson A.L., Pedersen N.L., Elman S., Gatz M. Endogenous and exogenous hormone exposure and risk of cognitive impairment in Swedish twins: a preliminary study. Psychoneuroendocrinology 2005, 30:558-567.
88. Resnick S.M., Espeland M.A., Jaramillo S.A., Hirsch C., Stefanick M.L., Murray A.M., Ockene J., Davatzikos C. Postmenopausal hormone therapy and regional brain volumes: the WHIMS-MRI Study. Neurology 2009, 72:135-142.
89. Rocca W.A., Grossardt B.R., Shuster L.T. Oophorectomy, menopause, estrogen treatment, and cognitive aging: clinical evidence for a window of opportunity. Brain Res 2011, 1379:188-198.
90. Rosi S., Vazdarjanova A., Ramirez-Amaya V., Worley P.F., Barnes C.A., Wenk G.L. Memantine protects against LPS-induced neuroinflammation, restores behaviorally-induced gene expression and spatial learning in the rat. Neuroscience 2006, 142:1303-1315.
91. Ryan J., Scali J., Carriere I., Ritchie K., Ancelin M.L. Hormonal treatment, mild cognitive impairment and Alzheimer's disease. Int. Psychogeriatr 2008, 20:47-56.
92. Saxe M.D., Malleret G., Vronskaya S., Mendez I., Garcia A.D., Sofroniew M.V., Kandel E.R., Hen R. Paradoxical influence of hippocampal neurogenesis on working memory. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:4642-4646.
93. Schoenfeld T.J., Gould E. Stress, stress hormones, and adult neurogenesis. Exp. Neurol 2012, 233:12-21.
94. Seshadri S., Zornberg G.L., Derby L.E., Myers M.W., Jick H., Drachman D.A. Postmenopausal estrogen replacement therapy and the risk of Alzheimer disease. Arch. Neurol 2001, 58:435-440.
95. Sherwin B.B. Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology 1988, 13:345-357.
96. Sherwin B.B. Estrogen therapy: is time of initiation critical for neuroprotection?. Nat. Rev. Endocrinol 2009, 5:620-627.
97. Sherwin B.B., Henry J.F. Brain aging modulates the neuroprotective effects of estrogen on selective aspects of cognition in women: a critical review. Front. Neuroendocrinol 2008, 29:88-113.
98. Shumaker S.A., Legault C., Kuller L., Rapp S.R., Thal L., Lane D.S., Fillit H., Stefanick M.L., Hendrix S.L., Lewis C.E., Masaki K., Coker L.H. Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 2004, 291:2947-2958. Women's Health Initiative Memory Study.
99. Shumaker S.A., Legault C., Rapp S.R., Thal L., Wallace R.B., Ockene J.K., Hendrix S.L., Jones B.N., Assaf A.R., Jackson R.D., Kotchen J.M., Wassertheil-Smoller S., Wactawski-Wende J. Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 2003, 289:2651-2662. WHIMS Investigators.
100. 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.
101. Spritzer M.D., Daviau E.D., Coneeny M.K., Engelman S.M., Prince W.T., Rodriguez-Wisdom K.N. Effects of testosterone on spatial learning and memory in adult male rats. Horm. Behav 2011, 59:484-496.
102. Sutherland R.J., Whishaw I.Q., Kolb B. A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat. Behav. Brain Res 1983, 7:133-153.
103. Talboom J.S., Williams B.J., Baxley E.R., West S.G., Bimonte-Nelson H.A. Higher levels of estradiol replacement correlate with better spatial memory in surgically menopausal young and middle-aged rats. Neurobiol. Learn. Mem 2008, 90:155-163.
104. 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. J. Comp. Neurol 2005, 481:252-265.
105. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res. Rev 2007, 53:198-214.
106. Tierney M.C., Oh P., Moineddin R., Greenblatt E.M., Snow W.G., Fisher R.H., Iazzetta J., Hyslop P.S., MacLusky N.J. A randomized double-blind trial of the effects of hormone therapy on delayed verbal recall in older women. Psychoneuroendocrinology 2009, 34:1065-1074.
107. Veiga S., Melcangi R.C., Doncarlos L.L., Garcia-Segura L.M., Azcoitia I. Sex hormones and brain aging. Exp. Gerontol 2004, 39:1623-1631.
108. Wood J.C., Jackson J.S., Jakubs K., Chapman K.Z., Ekdahl C.T., Kokaia Z., Kokaia M., Lindvall O. Functional integration of new hippocampal neurons following insults to the adult brain is determined by characteristics of pathological environment. Exp. Neurol 2011, 229:484-493.
109. Wroolie T.E., Kenna H.A., Williams K.E., Powers B.N., Holcomb M., Khaylis A., Rasgon N.L. Differences in verbal memory performance in postmenopausal women receiving hormone therapy: 17beta-estradiol versus conjugated equine estrogens. Am. J. Geriatr. Psychiatry 2011, 19:792-802.
110. Wysowski D.K., Golden L., Burke L. Use of menopausal estrogens and medroxyprogesterone in the United States, 1982-1992. Obstet. Gynecol 1995, 85:6-10.
111. Yaffe K., Grady D., Pressman A., Cummings S. Serum estrogen levels, cognitive performance, and risk of cognitive decline in older community women. J. Am. Geriatr. Soc 1998, 46:816-821.
112. Zhao L., Brinton R.D. Select estrogens within the complex formulation of conjugated equine estrogens (Premarin) are protective against neurodegenerative insults: implications for a composition of estrogen therapy to promote neuronal function and prevent Alzheimer's disease. BMC Neurosci 2006, 7:24.
113. Zhao L., Chen S., Brinton R.D. An estrogen replacement therapy containing nine synthetic plant-based conjugated estrogens promotes neuronal survival. Exp. Biol. Med. (Maywood) 2003, 228:823-835.