Interactive effects of age and estrogen on cortical neurons: Implications for cognitive aging

Neuroscience

Volumn 191, Issue , 2011, Pages 148-158

  Bailey, M E ^a   Wang, A C J ^a   Hao, J ^a,b   Janssen, W G M ^a   Hara, Y ^a   Dumitriu, D ^a   Hof, P R ^a   Morrison, J H ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b HEBEI MEDICAL UNIVERSITY   (China)

Author keywords

Aging; Cognition; Estrogen; Hormone replacement therapy; Prefrontal cortex; Primate

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA;

AGING; ANIMAL BEHAVIOR; BRAIN CELL; BRAIN REGION; COGNITION; DENDRITIC SPINE; ESTROGEN ACTIVITY; HIPPOCAMPUS; NERVE CELL PLASTICITY; NEUROANATOMY; NEUROMODULATION; NONHUMAN; OVARIECTOMY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; RHESUS MONKEY; SIGNAL TRANSDUCTION; TASK PERFORMANCE;

AGING; ANIMALS; COGNITION; DENDRITIC SPINES; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; HIPPOCAMPUS; HUMANS; MACACA MULATTA; MALE; NEURONS; OVARIECTOMY; PREFRONTAL CORTEX; RATS; REACTION TIME;

EID: 80052269569     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.05.045     Document Type: Review

References (114)

1. Adams M.M., Fink S.E., Shah R.A., Janssen W.G., Hayashi S., Milner T.A., McEwen B.S., Morrison J.H. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci 2002, 22:3608-3614.
2. Adams M.M., Shah R.A., Janssen W.G., Morrison J.H. Different modes of hippocampal plasticity in response to estrogen in young and aged female rats. Proc Natl Acad Sci U S A 2001, 98:8071-8076.
3. Ancelin M.L., Ritchie K. Lifelong endocrine fluctuations and related cognitive disorders. Curr Pharm Des 2005, 11:4229-4252.
4. Bagger Y.Z., Tankó L.B., Alexandersen P., Qin G., Christiansen C. Early postmenopausal hormone therapy may prevent cognitive impairment later in life. Menopause 2005, 12:12-17. PERF Study Group.
5. Berman K.F., Schmidt P.J., Rubinow D.R., Danaceau M.A., Van Horn J.D., Esposito G., Ostrem J.L., Weinberger D.R. Modulation of cognition-specific cortical activity by gonadal steroids: a positron-emission tomography study in women. Proc Natl Acad Sci U S A 1997, 94:8836-8841.
6. Bermejo-Pareja F., Benito-León J., Vega S., Medrano M.J., Román G.C. Incidence and subtypes of dementia in three elderly populations of central Spain. J Neurol Sci 2008, 264:63-72. Neurological Disorders in Central Spain (NEDICES) Study Group.
7. Buist D.S., Newton K.M., Miglioretti D.L., Beverly K., Connelly M.T., Andrade S., Hartsfield C.L., Wei F., Chan K.A., Kessler L. Hormone therapy prescribing patterns in the United States. Obstet Gynecol 2004, 104:1042-1050.
8. Carlson M.C., Zandi P.P., Plassman B.L., Tschanz J.T., Welsh-Bohmer K.A., Steffens D.C., Bastian L.A., Mehta K.M., Breitner J.C. Hormone replacement therapy and reduced cognitive decline in older women: the Cache County Study. Neurology 2001, 57:2210-2216. Cache County Study Group.
9. Chang Y.M., Rosene D.L., Killiany R.J., Mangiamele L.A., Luebke J.I. Increased action potential firing rates of layer 2/3 pyramidal cells in the prefrontal cortex are significantly related to cognitive performance in aged monkeys. Cereb Cortex 2005, 15:409-418.
10. Divac I., Warren J.M. Delayed response by frontal monkeys in the Nencki testing situation. Neuropsychologia 1971, 9:209-217.
11. Dominguez R., Liu R., Baudry M. 17-Beta-estradiol-mediated activation of extracellular-signal regulated kinase, phosphatidylinositol 3-kinase/protein kinase B-Akt and N-methyl-d-aspartate receptor phosphorylation in cortical synaptoneurosomes. J Neurochem 2007, 101:232-240.
12. Duan H., Wearne S.L., Rocher A.B., Macedo A., Morrison J.H., Hof P.R. Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb Cortex 2003, 13:950-961.
13. Dufau M.L., Hodgen G.D., Goodman A.L., Catt K.J. Bioassay of circulating luteinizing hormone in the rhesus monkey: comparison with radioimmunoassay during physiological changes. Endocrinology 1977, 100:1557-1565.
14. Dumitriu D., Hao J., Hara Y., Kaufmann J., Janssen W.G., Lou W., Rapp P.R., Morrison J.H. Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. J Neurosci 2010, 30:7507-7515.
15. Epting L.K., Overman W.H. Sex-sensitive tasks in men and women: a search for performance fluctuations across the menstrual cycle. Behav Neurosci 1998, 112:1304-1317.
16. Farrag A.K., Khedr E.M., Abdel-Aleem H., Rageh T.A. Effect of surgical menopause on cognitive functions. Dement Geriatr Cogn Disord 2002, 13:193-198.
17. Funakoshi T., Yanai A., Shinoda K., Kawano M.M., Mizukami Y. G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun 2006, 346:904-910.
18. Ganeshina O., Berry R.W., Petralia R.S., Nicholson D.A., Geinisman Y. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J Comp Neurol 2004, 468:86-95.
19. Geinisman Y., deToledo-Morrell L., Morrell F. Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segmented postsynaptic densities. Brain Res 1991, 566:77-88.
20. Gingerich S., Kim G.L., Chalmers J.A., Koletar M.M., Wang X., Wang Y., Belsham D.D. Estrogen receptor alpha and G-protein coupled receptor 30 mediate the neuroprotective effects of 17beta-estradiol in novel murine hippocampal cell models. Neuroscience 2010, 170:54-66.
21. Greendale G.A., Huang M.H., Wight R.G., Seeman T., Luetters C., Avis N.E., Johnston J., Karlamangla A.S. Effects of the menopause transition and hormone use on cognitive performance in midlife women. Neurology 2009, 72:1850-1857.
22. Greenough W.T., West R.W., DeVoogd T.J. Subsynaptic plate perforations: changes with age and experience in the rat. Science 1978, 202:1096-1098.
23. Gross C.G., Weiskrantz L. Evidence for dissociation of impairment on auditory discrimination and delayed response following lateral frontal lesions in monkeys. Exp Neurol 1962, 5:453-476.
24. Hammond R., Mauk R., Ninaci D., Nelson D., Gibbs R.B. Chronic treatment with estrogen receptor agonists restores acquisition of a spatial learning task in young ovariectomized rats. Horm Behav 2009, 56:309-314.
25. Hammond R., Nelson D., Gibbs R.B. GPR30 co-localizes with cholinergic neurons in the basal forebrain and enhances potassium-stimulated acetylcholine release in the hippocampus. Psychoneuroendocrinology 2011, 36:182-192.
26. Hampson E. Variations in sex-related cognitive abilities across the menstrual cycle. Brain Cogn 1990, 14:26-43.
27. Hao J., Rapp P.R., Janssen W.G., Lou W., Lasley B.L., Hof P.R., Morrison J.H. Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex. Proc Natl Acad Sci U S A 2007, 104:11465-11470.
28. Hao J., Rapp P.R., Leffler A.E., Leffler S.R., Janssen W.G., Lou W., McKay H., Roberts J.A., Wearne S.L., Hof P.R., Morrison J.H. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J Neurosci 2006, 26:2571-2578.
29. Hara Y, Park CS, Janssen WG, Roberts MT, Morrison JH, Rapp PR (in press) Synaptic correlates of memory and menopause in the hippocampal dentate gyrus in rhesus monkeys. Neurobiol Aging, in press.
30. Harris K.M., Jensen F.E., Tsao B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 1992, 12:2685-2705.
31. Hausmann M., Slabbekoorn D., Van Goozen S.H., Cohen-Kettenis P.T., Güntürkün O. Sex hormones affect spatial abilities during the menstrual cycle. Behav Neurosci 2000, 114:1245-1250.
32. Hazell G.G., Yao S.T., Roper J.A., Prossnitz E.R., O'Carroll A.M., Lolait S.J. Localisation of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues. J Endocrinol 2009, 202:223-236.
33. Henderson V.W. Alzheimer's disease and other neurological disorders. Climacteric 2007, 10:92-96.
34. Henderson V.W., Benke K.S., Green R.C., Cupples L.A., Farrer L.A. Postmenopausal hormone therapy and Alzheimer's disease risk: interaction with age. J Neurol Neurosurg Psychiatry 2005, 76:103-105. MIRAGE Study Group.
35. Henderson V.W., Guthrie J.R., Dudley E.C., Burger H.G., Dennerstein L. Estrogen exposures and memory at midlife: a population-based study of women. Neurology 2003, 60:1369-1371.
36. Herlitz A., Thilers P., Habib R. Endogenous estrogen is not associated with cognitive performance before, during, or after menopause. Menopause 2007, 14:425-431.
37. Herndon J.G., Moss M.B., Rosene D.L., Killiany R.J. Patterns of cognitive decline in aged rhesus monkeys. Behav Brain Res 1997, 87:25-34.
38. Hersh A.L., Stefanick M.L., Stafford R.S. National use of postmenopausal hormone therapy: annual trends and response to recent evidence. JAMA 2004, 291:47-53.
39. Hof P.R., Morrison J.H. The aging brain: morphomolecular senescence of cortical circuits. Trends Neurosci 2004, 27:607-613.
40. Hojo Y., Murakami G., Mukai H., Higo S., Hatanaka Y., Ogiue-Ikeda M., Ishii H., Kimoto T., Kawato S. Estrogen synthesis in the brain-role in synaptic plasticity and memory. Mol Cell Endocrinol 2008, 290:31-43.
41. Holtmaat A.J., Trachtenberg J.T., Wilbrecht L., Shepherd G.M., Zhang X., Knott G.W., Svoboda K. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 2005, 45:279-291.
42. Htun H., Holth L.T., Walker D., Davie J.R., Hager G.L. Direct visualization of the human estrogen receptor alpha reveals a role for ligand in the nuclear distribution of the receptor. Mol Biol Cell 1999, 10:471-486.
43. Jacobs B., Driscoll L., Schall M. Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J Comp Neurol 1997, 386:661-680.
44. Jacome L.F., Gautreaux C., Inagaki T., Mohan G., Alves S., Lubbers L.S., Luine V. Estradiol and ERβ agonists enhance recognition memory, and DPN, an ERβ agonist, alters brain monoamines. Neurobiol Learn Mem 2010, 94:488-498.
45. Kasai H., Matsuzaki M., Noguchi J., Yasumatsu N., Nakahara H. Structure-stability-function relationships of dendritic spines. Trends Neurosci 2003, 26:360-368.
46. Kato I., Toniolo P., Akhmedkhanov A., Koenig K.L., Shore R., Zeleniuch-Jacquotte A. Prospective study of factors influencing the onset of natural menopause. J Clin Epidemiol 1998, 51:1271-1276.
47. Keenan P.A., Ezzat W.H., Ginsburg K., Moore G.J. Prefrontal cortex as the site of estrogen's effect on cognition. Psychoneuroendocrinology 2001, 26:577-590.
48. Kimura D. Estrogen replacement therapy may protect against intellectual decline in postmenopausal women. Horm Behav 1995, 29:312-321.
49. Lacreuse A., Herndon J.G. Estradiol selectively affects processing of conspecifics' faces in female rhesus monkeys. Psychoneuroendocrinology 2003, 28:885-905.
50. Lacreuse A., Herndon J.G., Moss M.B. Cognitive function in aged ovariectomized female rhesus monkeys. Behav Neurosci 2000, 114:506-513.
51. Lacreuse A., Kim C.B., Rosene D.L., Killiany R.J., Moss M.B., Moore T.L., Chennareddi L., Herndon J.G. Sex, age, and training modulate spatial memory in the rhesus monkey (Macaca mulatta). Behav Neurosci 2005, 119:118-126.
52. Lai Z.C., Moss M.B., Killiany R.J., Rosene D.L., Herndon J.G. Executive system dysfunction in the aged monkey: spatial and object reversal learning. Neurobiol Aging 1995, 16:947-954.
53. Leranth C., Hajszan T., Szigeti-Buck K., Bober J., MacLusky N.J. Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc Natl Acad Sci U S A 2008, 105:14187-14191.
54. Luebke J., Barbas H., Peters A. Effects of normal aging on prefrontal area 46 in the rhesus monkey. Brain Res Rev 2010, 62:212-232.
55. MacLennan A.H., Henderson V.W., Paine B.J., Mathias J., Ramsay E.N., Ryan P., Stocks N.P., Taylor A.W. Hormone therapy, timing of initiation, and cognition in women aged older than 60 years: the REMEMBER pilot study. Menopause 2006, 13:28-36.
56. Maki P.M., Rich J.B., Rosenbaum R.S. Implicit memory varies across the menstrual cycle: estrogen effects in young women. Neuropsychologia 2002, 40:518-529.
57. Maki P.M., Sundermann E. Hormone therapy and cognitive function. Hum Reprod Update 2009, 15:667-681.
58. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
59. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 2001, 4:1086-1092.
60. Matthews K., Cauley J., Yaffe K., Zmuda J.M. Estrogen replacement therapy and cognitive decline in older community women. J Am Geriatr Soc 1999, 47:518-523.
61. Milner T.A., Ayoola K., Drake C.T., Herrick S.P., Tabori N.E., McEwen B.S., Warrier S., Alves S.E. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol 2005, 491:81-95.
62. Milner T.A., McEwen B.S., Hayashi S., Li C.J., Reagan L.P., Alves S.E. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 2001, 429:355-371.
63. Moore T.L., Killiany R.J., Herndon J.G., Rosene D.L., Moss M.B. Impairment in abstraction and set shifting in aged rhesus monkeys. Neurobiol Aging 2003, 24:125-134.
64. Mordecai K.L., Rubin L.H., Maki P.M. Effects of menstrual cycle phase and oral contraceptive use on verbal memory. Horm Behav 2008, 54:286-293.
65. Morrison J.H., Hof P.R. Life and death of neurons in the aging brain. Science 1997, 278:412-419.
66. Moss M.B., Killiany R.J., Lai Z.C., Rosene D.L., Herndon J.G. Recognition memory span in rhesus monkeys of advanced age. Neurobiol Aging 1997, 8:13-19.
67. Mukai H., Tsurugizawa T., Murakami G., Kominami S., Ishii H., Ogiue-Ikeda M., Takata N., Tanabe N., Furukawa A., Hojo Y., Ooishi Y., Morrison J.H., Janssen W.G., Rose J.A., Chambon P., Kato S., Izumi S., Yamazaki T., Kimoto T., Kawato S. Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. J Neurochem 2007, 100:950-967.
68. Nappi R.E., Sinforiani E., Mauri M., Bono G., Polatti F., Nappi G. Memory functioning at menopause: impact of age in ovariectomized women. Gynecol Obstet Invest 1999, 47:29-36.
69. Neese S.L., Korol D.L., Katzenellenbogen J.A., Schantz S.L. Impact of estrogen receptor alpha and beta agonists on delayed alternation in middle-aged rats. Horm Behav 2010, 58:878-890.
70. Nichols S.M., Bavister B.D., Brenner C.A., Didier P.J., Harrison R.M., Kubisch H.M. Ovarian senescence in the rhesus monkey (Macaca mulatta). Hum Reprod 2005, 20:79-83.
71. Nimchinsky E.A., Sabatini B.L., Svoboda K. Structure and function of dendritic spines. Annu Rev Physiol 2002, 64:313-353.
72. Noguchi J., Matsuzaki M., Ellis-Davies G.C., Kasai H. Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 2005, 46:609-622.
73. Pakkenberg B., Gundersen H.J. Neocortical neuron number in humans: effect of sex and age. J Comp Neurol 1997, 384:312-320.
74. Peters A., Kaiserman-Abramof I.R. The small pyramidal neuron of the rat cerebral cortex. The synapses upon dendritic spines. Z Zellforsch Mikrosk Anat 1969, 100:487-506.
75. Peters A., Sethares C., Luebke J.I. Synapses are lost during aging in the primate prefrontal cortex. Neuroscience 2008, 152:970-981.
76. Peters A., Sethares C., Moss M.B. The effects of aging on layer 1 in area 46 of prefrontal cortex in the rhesus monkey. Cereb Cortex 1998, 8:671-684.
77. Petrides M., Pandya D.N. Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns. Eur J Neurosci 1999, 11:1011-1036.
78. Phillips K., Silverman I. Differences in the relationship of menstrual cycle phase to spatial performance on two- and three-dimensional tasks. Horm Behav 1997, 32:167-175.
79. Phillips S.M., Sherwin B.B. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology 1992, 17:485-495.
80. Portin R., Polo-Kantola P., Polo O., Koskinen T., Revonsuo A., Irjala K., Erkkola R. Serum estrogen level, attention, memory and other cognitive functions in middle-aged women. Climacteric 1999, 2:115-123.
81. Postma A., Winkel J., Tuiten A., van Honk J. Sex differences and menstrual cycle effects in human spatial memory. Psychoneuroendocrinology 1999, 24:175-192.
82. Presty S.K., Bachevalier J., Walker L.C., Struble R.G., Price D.L., Mishkin M., Cork L.C. Age differences in recognition memory of the rhesus monkey (Macaca mulatta). Neurobiol Aging 1987, 8:435-440.
83. Rapp P.R. Visual discrimination and reversal learning in the aged monkey (Macaca mulatta). Behav Neurosci 1990, 104:876-884.
84. Rapp P.R., Amaral D.G. Evidence for task-dependent memory dysfunction in the aged monkey. J Neurosci 1989, 9:3568-3576.
85. Rapp P.R., Amaral D.G. Recognition memory deficits in a subpopulation of aged monkeys resemble the effects of medial temporal lobe damage. Neurobiol Aging 1991, 12:481-486.
86. Rapp P.R., Kansky M.T., Roberts J.A. Impaired spatial information processing in aged monkeys with preserved recognition memory. Neuroreport 1997, 8:1923-1928.
87. Rapp P.R., Morrison J.H., Roberts J.A. Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J Neurosci 2003, 23:5708-5714.
88. Roberts J.A., Gilardi K.V., Lasley B., Rapp P.R. Reproductive senescence predicts cognitive decline in aged female monkeys. Neuroreport 1997, 8:2047-2051.
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. Rosenberg L., Park S. Verbal and spatial functions across the menstrual cycle in healthy young women. Psychoneuroendocrinology 2002, 27:835-841.
91. Shamy JL, Habeck C, Hof PR, Amaral DG, Fong SG, Buonocore MH, Stern Y, Barnes CA, Rapp PR (in press) Volumetric correlates of spatiotemporal working and recognition memory impairment in aged Rhesus Monkeys. Cereb Cortex.
92. 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.
93. Sherwin B.B., Tulandi T. "Add-back" estrogen reverses cognitive deficits induced by a gonadotropin-releasing hormone agonist in women with leiomyomata uteri. J Clin Endocrinol Metab 1996, 81:2545-2549.
94. 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.
95. Spencer J.L., Waters E.M., Milner T.A., McEwen B.S. Estrous cycle regulates activation of hippocampal Akt, LIM kinase, and neurotrophin receptors in C57BL/6 mice. Neuroscience 2008, 155:1106-1119.
96. Sundermann E.E., Maki P.M., Bishop J.R. A review of estrogen receptor alpha gene (ESR1) polymorphisms, mood, and cognition. Menopause 2010, 17:874-886.
97. Szklo M., Cerhan J., Diez-Roux A.V., Chambless L., Cooper L., Folsom A.R., Fried L.P., Knopman D., Nieto F.J. Estrogen replacement therapy and cognitive functioning in the Atherosclerosis Risk in Communities (ARIC) Study. Am J Epidemiol 1996, 144:1048-1057.
98. Tang Y., Janssen W.G., Hao J., Roberts J.A., McKay H., Lasley B., Allen P.B., Greengard P., Rapp P.R., Kordower J.H., Hof P.R., Morrison J.H. Estrogen replacement increases spinophilin-immunoreactive spine number in the prefrontal cortex of female rhesus monkeys. Cereb Cortex 2004, 14:215-223.
99. ter Horst G.J. Estrogen in the limbic system. Vitam Horm 2010, 82:319-338.
100. Tinkler G.P., Voytko M.L. Estrogen modulates cognitive and cholinergic processes in surgically menopausal monkeys. Prog Neuropsychopharmacol Biol Psychiatry 2005, 29:423-431.
101. Toran-Allerand C.D. Novel sites and mechanisms of oestrogen action in the brain. Novartis Found Symp 2000, 230:56-69.
102. Uemura E. Age-related changes in prefrontal cortex of Macaca mulatta: synaptic density. Exp Neurol 1980, 69:164-172.
103. Van Esch E., Cline J.M., Buse E., Wood C.E., de Rijk E.P.C.T., Weinbauer G.F. Summary comparison of female reproductive system in human and the Cynomolgus monkey (Macaca fascicularis). Toxicol Pathol 2008, 36:171S-172S.
104. Vearncombe K.J., Pachana N.A. Is cognitive functioning detrimentally affected after early, induced menopause?. Menopause 2009, 16:188-198.
105. Verghese J., Kuslansky G., Katz M.J., Sliwinski M., Crystal H.A., Buschke H., Lipton R.B. Cognitive performance in surgically menopausal women on estrogen. Neurology 2000, 55:872-874.
106. Voytko M.L. Impairments in acquisition and reversals of two-choice discriminations by aged rhesus monkeys. Neurobiol Aging 1999, 20:617-627.
107. Voytko M.L., Murray R., Higgs C.J. Executive function and attention are preserved in older surgically menopausal monkeys receiving estrogen or estrogen plus progesterone. J Neurosci 2009, 29:10362-10370.
108. Voytko M. The effects of long-term ovariectomy and estrogen replacement therapy on learning and memory in monkeys (Macaca fascicularis). Behav Neurosci 2000, 114:1078-1087.
109. Wang A.C., Hara Y., Janssen W.G., Rapp P.R., Morrison J.H. Synaptic estrogen receptor-alpha levels in prefrontal cortex in female rhesus monkeys and their correlation with cognitive performance. J Neurosci 2010, 30:12770-12776.
110. Wolf O.T., Kudielka B.M., Hellhammer D.H., Törber S., McEwen B.S., Kirschbaum C. Two weeks of transdermal estradiol treatment in postmenopausal elderly women and its effect on memory and mood: verbal memory changes are associated with the treatment induced estradiol levels. Psychoneuroendocrinology 1999, 24:727-741.
111. Woolley C.S., Gould E., Frankfurt M., McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 1990, 10:4035-4039.
112. Yasumatsu N., Matsuzaki M., Miyazaki T., Noguchi J., Kasai H. Principles of long-term dynamics of dendritic spines. J Neurosci 2008, 28:13592-13608.
113. Zandi P.P., Carlson M.C., Plassman B.L., Welsh-Bohmer K.A., Mayer L.S., Steffens D.C., Breitner J.C. Hormone replacement therapy and incidence of Alzheimer disease in older women: the Cache County Study. JAMA 2002, 288:2123-2129. Cache County Memory Study Investigators.
114. Zhou Q., Homma K.J., Poo M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 2004, 44:749-757.