Neuroendocrinology of memory and cognitive function

Handbook of Neurochemistry and Molecular Neurobiology: Behavioral Neurochemistry, Neuroendocrinology and Molecular Neurobiology

Volumn , Issue , 2007, Pages 775-800

  Luine, V N ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84900657254     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-30405-2_21     Document Type: Chapter

References (163)

1. Akama KT, McEwen BS. 2003. Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J Neurosci 23:2333-2339.
2. Anderson GL, Limacher M, Assaf AR, Bassford T, Beresford SA, et al. 2004. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA 291:1701-1712.
3. Arnold AP. 2004. Sex chromosomes and brain gender. Nat Rev Neurosci 5:701-708.
4. Bailey CH, Kandel ER, Si, K. 2004. The persistence of longterm memory: a molecular approach to self-sustaining changes in learning-induced synaptic growth. Neuron 44:49-57.
5. Baker KB, Kim JJ. 2002. Effects of stress and hippocampal NMDA receptor antagonism on recognition memory in rats. Learn Mem 9:58-65.
6. Beck KD, Luine VN. 1999. Food deprivation modulates chronic stress effects on object recognition in male rats: role of monoamines and amino acids. Brain Res 830:56-71.
7. Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, 2005. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 2004 Dec. 23 (Epub ahead of print).
8. Berry B, McMahan R, Gallagher M. 1997. Spatial learning and memory at defined points of the estrous cycle: effects on performance of a hippocampal-depedent task. Behav Neurosci 11:267-274.
9. Bi R, Broutman G, Foy MR, Thompson RF, Baudry M. 2000. The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc Natl Acad Sci USA 97:3602-3607.
10. Bi R, Foy MR, Vouimba RM, Thompson RF, Baudry M. 2001. Cyclic changes in estradiol regulate synaptic plasticity through the MAPkinase pathway. Proc Natl Acad Sci USA 98:13391-13395.
11. Bisagno V, Ferguson D, Luine VN. 2003. Chronic d-amphetamine induces sexually dimorphic effects on locomotion, recognition memory and brain monoamines. Pharmac Biochem Behav 74:859-867.
12. Bisagno V, Grill CA, Piroli GG, Giraldo P, McEwen BS, et al. 2004. Chronic stress alters the behavioral and neural effects of amphetamine. Pharmac Biochem Behav 78:541-550.
13. Blaustein JD. 1992. Cytoplasmic estrogen receptors in rat brain: immunocytochemical evidence using three antibodies with distinct epitopes. Endocrinology 131:1336-1342.
14. Bowman RE, Beck KD, Luine VN. 2003. Chronic stress effects on memory: sex differences in performance and monoamines. Horm Behav 43:48-59.
15. Bowman RE, Ferguson D, Luine VN. 2002. Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats. Neuroscience 113:401-410.
16. Bowman RE, MacLusky NJ, Sarmiento Y, Frankfurt M, Gordon M, et al. 2004. Sexually dimorphic effects of prenatal stress on cognition, hormonal responses and central neurotransmitters. Endocrinology 145:3778-3787.
17. Bowman RE, Zrull MC, Luine VN. 2001. Chronic restraint stress enhances radial arm maze performance in female rats. Brain Res 904, 279-289.
18. Cahill L, Haier RJ, White NS, Fallon J, Kilpatrick L, et al. 2001. Sex-related difference in amygdala activity during emotionally influenced memory storage. Neurobiol Learn Mem 75:1-9.
19. Carter CS, Lederhendler II, Kirkpatrick B. 1997. Integrative neurobiologoy of affiliation. Vol. 807. New York: New York Academy of Sciences.
20. Coburn-Litvak PS, Tata DA, Gorby HE, McCloskey DP, Richardson G, et al. 2004. Chronic corticosterone affects brain weight, and mitochondrial, but not glial volume fraction in hippocampal area CA3. Neuroscience 124:429-438.
21. Conrad CD, Galea LA, Kuroda Y, McEwen BS. 1996. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci 110:1321-1334.
22. Conrad CD, Grote KA, Hobbs RJ, Ferayorni A. 2003. Sex differences in spatial and non-spatial Y-maze performance after chronic stress. Neurobiol Learn Mem 79:32-40.
23. Conrad CD, Jackson JL, Wieczorek L, Baran SE, Harman JS, et al. 2004. Acute restraint stress impairs spatial memory in male but not female rats: influence of estrous cycle. Pharmac Biochem Behav 78:569-579.
24. Daniel JM, Fader AJ, Spencer A, Dohanich GP. 1997. Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm Behav 32:217-225.
25. Daniel JM, Dohanich GP. 2001. Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 21:6949-6956.
26. Daniel JM, Lee DC. 2004. Estrogen replacement in ovariectomized rats affects strategy selection in the Morris water maze. Neurobiol Learn Mem 82:142-19l.
27. Daniel JM, Winsauer PJ, Moerschbaecher JM. 2003. Castration in rats impairs performance during acquisition of a working memory task and exacerbates deficits in working memory produced by scopolamine and mecamylamine. Psychopharm 170:294-300.
28. de Kloet ER. 2004. Hormones and the stressed brain. Ann NY Acad Sci 1018:1-15.
29. deKloet ER, Azmitia EC, Landfield PW. (editors) 1994. Brain corticosteroid receptors: studies on the mechanism, function and neurotoxicity of corticosteroid action, Ann NY Acad Sci 746.
30. De Kloet ER, Oitzl MS, Joels M. 1999. Stress and cognition: are corticostereoids good or bad guys? Trends Neurosci 22:422-426.
31. Diamond DM, Par CR, Herman KL, Rose GM. 1999. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9:942-952.
32. Dohanich GP. 2002. Gonadal steroids, learning and memory. Hormones, brain and behavior. San Diego: Academic Press; pp. 265-327.
33. Dohanich GP, Fader AJ, Javorsky DJ. 1994. Estrogen and estrogen-progesterone treatments counteract the effect of scopolamine on reinforced T-maze alternation in female rats. Behav Neurosci 108:988-992.
34. Edinger KL, Lee B, Frye CA. 2004. Mnemonic effects of testosterone and its 5α-reduced metabolites in the conditioned fear and inhibitory avoidance tasks. Pharmac Biochem Behav 78:559-568.
35. Ennaceur A, Aggleton JP. 1994. Spontaneous recognition of object configurationsin rats: effects of fornix lesions. Exp Brain Res 100:85-92.
36. Ennaceur A, Neave N, Aggleton JP. 1997. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 113:509-519.
37. Everett JW. 1965. Ovulation in rats from preoptic stimulation through platinum electrodes. Important of duration and spread of stimuli. Endocrinology 76:1195.
38. Fader AJ, Johnson PEM, Dohanich GP. 1999. Estrogen improves working but not reference memory and prevents amnestic effects of scopolamine on a radial-arm maze. Pharmacl Biochem Behav 62:711-717.
39. Ferguson D, Dumas T, Sapolsky RM. 2004. Gene therapy to spare cognition from the disruptive effects of stress. Program No. 770.10. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience.
40. Fillit H, Luine V. 1997. The neurobiology of gonadal hormones and cognitive decline in late life. Maturitas 26:159-164.
41. Frick KM, Fernandez SM, Bennett JC, Prange-Kiel J, Maclusky NJ, et al. 2004. Behavioral training interferes with the ability of gonadal hormones to increase CAI spine synapse density in ovariectomized female rats. European J Neurosci 19:1-7.
42. Frye CA. 1995. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol Behav 57:5-14.
43. Frye CA, Wawrzycki J. 2003. Effect of prenatal stress and gonadal hormone condition on depressive behaviors of female and male rats. Horm Behav. 44:319-26.
44. Galea LA, McEwen BS, Tanapat P, Deak T, Spencer RL, et al. 1997. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 81:689-697.
45. Garcia-Segura LM, Azcortia I, Don Carlos LC. 2001. Neuroprotection by estrogen. Prog Neurobiol 63:29-60.
46. Ge X, Hannan F, Xie Z, Feng C, Tully T, et al. 2004. Notch signaling in Drosophila long-term memory formation. Proc Natl Acad Sci USA 101:10172-10176.
47. Gibbs RB. 1999. Treatment with estrogen and progestereone affects relative levels of brain-derived neurotrophic factor mRNA and protein in different regions of the adult rat brain. Brain Res 844:20-27.
48. Gibbs RB. 2000. Basal forebrain cholinergic neurons are necessary for estrogen to enhance acquisition of a delayed matching-to-position T-maze task. Horm Behav 42:245-257.
49. Gibbs RB, Aggarwal P. 1998. Estrogen and basal forebrain cholinergic neurons: implications for brain aging and Alzheimer's disease-related cognitive decline. Horm Behav 334:98-111.
50. Gorski RA. 1971. Gonadal hormones and the perinatal development of neuroendocrine function. Frontiers in Neuroendocrinology. Martini L, Ganong WF. (editors), New York: Oxford Press; p. 237.
51. Gould E, Woolley CS, Frankfurt M, McEwen BS. 1990. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10:1286-1291.
52. Hampson E. 1990. Estrogen-related variations in human spatial and ariticulatory-motor skills. Psychoneuroendo 15:97-111.
53. Handa RJ, Burgess LH, Kerr JE, O'Keefe JA. 1994. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav 28:464-476.
54. Hao J, Janssen WG, Tang Y, Roberts JA, McKay H, et al. 2003. Estrogen increases the number of spinophilinimmunoreactive spines in the hippocampus of young and aged female rhesus monkeys. J Comp Neurol 465:540-550.
55. Helm KA, Hand JS, Gallagher M. 2002. Effects of cholinergic lesions produced by infusions of 192 IgG-saporin on glucocorticoid receptor mRNA expression in hippocampus and medial prefrontal cortex of the rat. Neuroscience 115:765-774.
56. Jensen E, Jacobson H. 1962. Basic guides to the mechanism of esrogen action. Rec Progr Horm Res 18:387-408.
57. Kaufer D, Ogle WO, Pincus ZS, Clark KL, Nicholas AC, et al. 2004. Restructuring the neuronal stress response with antiglucocorticoid gene delivery. Nat Neurosci 7:899-900.
58. Kimura D. 1992. Sex differences in the brain. Sci Am September: 119-125.
59. Kitraki E, Kremmyda O, Youlatos D, Alexis MN, Kittas C. 2004. Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restrain stress. Neuroscience 125:47-55.
60. Korol DL. 2004. Role of estrogen in balancing contributions from multiple memory systems. Neurobiol Learn Mem 82:309-323.
61. Kritzer MF, Kohama SG. 1998. Ovarian hormones influence morphology, distribution and density of tyrosine hydroxylase immunoreactive axons in the dorsolater prefrontal cortex of adult rhesus monkeys. J Comp Neurol 395:1-170.
62. Kritzer MF, McLaughlin PJ, Smirlis T, Robinson JK. 2001. Gonadectomy impairs T-maze acquisition in adult male rats. Horm Behav 39:167-174.
63. Kudielka BM, Hellhammer J, Hellhammer DH, Wolf OT, Pirke KM, et al. 1998. Sex differences in endocrine and psychological responses to psychosocial stress in healthy elderly subjects and the impact of a 2-week dehydroepiandrosterone treatment. J Clin Endocrinol Metab 83:1756-1761.
64. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, et al. 1997. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors a and β. Endocrinology 138:863-870.
65. Leranth C, Hajszan T, MacLusky NJ. 2004. Androgens increase spine synapse density in the CA1 hippocampal subfield of ovariectomized female rats. J Neurosci 24:495-499.
66. Leranth C, Shanabrough M, Horvath TL. 2000. Hormonal regulation of hippocampal spine synapse density involves subcortical mediation. Neuroscience 101:349-356.
67. Leranth C, Shanabrough M, Redmond DE. Jr. 2002. Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates. J Comp Neurol 447:34-42.
68. Levin ER. 2002. Cellular functions of plasma membrane estrogen receptors. Steroids 67:471-475.
69. Li C, Brake WG, Romeo RD, Dunlop JC, Gordon M, et al. 2004. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc Natl Acad Sci USA 101:2185-2190.
70. Luconi M, Forti G, Baldi E. 2002. Genomic and nongenomic effects of estrogens: molecular mechanisms of action and clinical implications for male reproduction. J Steroid Biochem Molec Biol 80:369-381.
71. Luine V, Harding CF. (Editors) 1994. Hormonal restructuring of the adult brain: Basic and clinical perspectives. Ann NY Acad Sci 743.
72. Luine V, Hearns M. 1990. Spatial memory deficits in aged rats: Contributions of the cholinergic system assessed by ChAT. Brain Res 523:321-324.
73. Luine V, Martinez C, Villegas M, Magarinos AM, McEwen B. 1996. Restraint stress reversibly enhances spatial memory performance, Physiology and Behavior 59:27-32.
74. Luine V, Richards ST, Wu VY, Beck K. 1998. Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm Behav 34:149-162.
75. Luine V, Rodriguez M. 1994. Effects of estradiol on radial arm maze performance of young and aged rats. Behav Neural Biol 62:230-236.
76. Luine V, Villegas M, Martinez C, McEwen BS. 1994. Repeated stress causes reversible impairments of spatial memory performance. Brain Res 639:167-170.
77. Luine VN. 1985. Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp Neurol 89:484-490.
78. Luine VN. 1994. Steroid hormone influences on spatial memory. Ann NY Acad Sci 743:201-211.
79. Luine VN. 1997. Steroid hormone modulation of hippocampal dependent spatial memory. Stress 2:21-36.
80. Luine VN. 2002. Sex differences in chronic stress effects on memory in rats. Stress 5:205-216.
81. Luine VN, Jacome LF, Maclusky NJ. 2003. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144:2836-2844.
82. Luine VN, Khylchevskaya RI, McEwen BS. 1975. Effects of gonadal steroids on activities of Monoamine oxidase and Choline acetylase in rat brain. Brain Res 86:293-306.
83. Lupien SJ, Nair NP, Briere S, Maheu F, Tu MT, et al. 1999. Increased cortisol levels and impaired cognition in human aging: implication for depression and dementia in later life. Rev Neurosci 10:117-139.
84. MacLusky N, Luine VN, Hajszan T, Leranth C. 2005. The 17 a and b isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats. Endocrinology 146:287-293.
85. MacLusky NJ, Yuan H, Elliott J, Brown TJ. 1996. Sex differences in corticosteroid binding in the rat brain: an in vitro autoradiographic study. Brain Res 708:71-81.
86. Maki PM, Resnick SM. 2001. Effects of estrogen on patterns of brain activity at rest and during cognitive activity: a review of neuroimaging studies. Neuroimage 14:789-801.
87. Markham JA, Juraska JM. 2002. Aging and sex influence the anatomy of rat anterior cingulated cortex. Neurobiol Aging 23:579-588.
88. Matsumoto A (Ed). 1999 Sexual Differentiation of the Brain. CRC Press. See this multi-author book for in depth understanding of sexual differentiation of the brain.
89. Micevych PE, Hammer RP Jr. (Editors) 1995. Neurobiological Effects of Sex Steroid Hormones. Cambridge University Press. See this multi-author book for articles on all aspects of gonadal steroid regulation of sexual behavior.
90. McCormick CM, Furey BF, Child M, Sawyer MJ, Donohue SM. 1998. Neonatal sex hormones have 'organizational' effects on the hypothalamic-pituitary-adrenal axis of male rats. Brain Res Dev 105:295-307.
91. McEwen BS. 2000. The neurobiology of stress: from serendipity to clinical relevance. Brain Res 886:172-189.
92. McEwen BS. 2001. Invited review: estrogens effects on the brain: multiple sites and molecular mechanisms. J Appl Physiol 91:2785-2801.
93. McEwen BS, Alves SE. 1999. Estrogen actions in the central nervous system. Endocr Rev 20:279-307.
94. McEwen BS, Gould E, Orchinik M, Weiland NG, Woolley CS. 1995. Oestrogens and the structural and functional plasticity of neurons: implications for memory, ageing and neurodegenerative processes. Ciba Found Symp 191:52-73.
95. McEwen BS, Weiss JM, Schwartz LS. 1968. Selective retention of corticostereone by limbic structures in rat brain. Nature 22:911-912.
96. McGaugh JL. 1989. Disassociating learning and performance: drug and hormone enhancement of memory storage. Brain Res Bull 23:339-345.
97. McGaugh JL. 2000. Memory-a century of consolidation 2000. Science 287:248-251.
98. Micevych PE, Hammer RP Jr. (Editors) 1995. Neurobiological effects of sex steroid hormones. Cambridge University Press. See this multi-author book for articles on all aspects of gonadal steroid regulation of sexal behavior.
99. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagan LP, et al. 2001. Ultrastructural evidence that hippocampal α estrogen receptors are located at extranuclear sites. J Comp Neurol 429:355-371.
100. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, et al. 2003. Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144:2055-2067.
101. Mumby DG, Gaskin S, Glenn MJ, Schramek TE, Lehmann H. 2002. Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. Learn Mem 9:49-57.
102. Nelson HD, Humphrey LL, Nygren P, Teutsch SM, Allan JD. 2002. Postmenopausal hormone replacement therapy: scientific review. JAMA 288:872-881.
103. Nelson RJ. 2005. An introduction to behavioral endocrinology, Sinauer Assoc., 3rd Edition, Textbook provides excellent background material on Endocrinology. For this review see faceplates for listing of vertebrate steroid hormones; Chapter 11 on Stress, p. 557; Chapter 12 on Learning and Memory, p. 593 and Chapter 4 Sex Differences in Behavior: Animal Models and Humans, p. 183.
104. Ostlund H, Keller E. Hurd YL. 2003. Estrogen receptor gene expression in relation to neuropsychiatric disorders. Ann NY Acad Sci 1007:54-63.
105. Packard MG. 1998. Posttraining estrogen and memory modulation. Horm Behav 34:126-139.
106. Packard MG, Cahill L, McGaugh JL. 1994. Amygdala modulation of hippocampal-dependent and caudate nucleusdependent memory processes. Proc Natl Acad Sci USA 91:8477-8481
107. Packard MG, Teather, LA. 1997a. Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats. Neuroreport 8:3009-3013.
108. Packard MG, Teather LA. 1997b. Posttraining estradiol injections enhance memory in ovariectomized rats: cholinergic blockade and synergism. Neurobiol Learn Mem 68:172-188.
109. Park CR, Campbell AM, Diamond DAM. 2001. Chronic psychosocial stresss impairs learning and memory and increases sensitiveity to yohimbine in rats. Biol Psychiatry 50:994-1004.
110. Patchev VK, Almeida OF. 1998. Gender specificity in the neural regulation of the response to stress: new leads from classical paradigms. Mol Neurobiol 16:63-77.
111. Patchev VK, Hayashi S, Orikasa C, Almeida OF. 1995. Implications of estrogen-dependent brain organization for gender differences in hypothalamo-pituitary-adrenal regulation. FASEB J 9:419-423.
112. Payne JL. 2003. The role of estrogen in mood disorders in women. Int Rev Psyciatry 15:280-290.
113. Reznikov AG, Nosenko ND, Tarasenko LV, Sinitsyn PV, Polyakova LI. 2001. Early and long-term neuroendocrine effects of prenatal stress in male and female rats. Neurosci Behav Physiol 31:1-5.
114. Rhodes ME, Frye CA. 2004. Estrogen has mnemonic-enhancing effects in the inhibitory avoidance task. Pharmacol Biochem Behav 78:551-558.
115. Rissman EF, Heck AL, Leonard JE, Shupnik MA, Gustafsson JA. 2002. Disruption of estrogen receptor β gene impairs spatial learning in female mice. Proc Natl Acad Sci USA 99:3996-4001.
116. Roof RL, Havens MD. 1992. Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Res 572:310-313.
117. Roozendaal B, McReynolds JM, McGaugh JL. 2004. The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J Neurosci 24:1385-1392.
118. Sandstrom NJ, Williams CL. 2001. Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 115:384-393.
119. Sandstrom NJ, Williams CL. 2004. Spatial memory retention is enhanced by acute and continuous estradiol replacement. Horm Behav 45:128-135.
120. Seeman TE, McEwen BS, Singer BH. 1997. Increase in urinary cortisol excretion and memory declinesL: MacArthur studies of successful aging. J Clin Endo Metab 82:2458-2465.
121. Sherwin BB. 2002. Estrogen and cognitive aging in women. Trends Pharmacol Sci 23:527-534.
122. Sherwin BB. 2003. Estrogen and cognitive function in women. Endocrin Reviews 24:133-151.
123. Shors TJ. 2001. Actue stress rapidly and persistently enhances memory formation in the male rat. Neurobiol Learn Mem 75:1929.
124. Shors TJ, Chua C, Falduto J. 2001. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 21:6292-6297.
125. Shors TJ, Weiss, Thompson RF. 1992. Stress-induced facilitation of classical conditioning. Science 257:537-539.
126. Shughrue PJ, Lane MV, Merchenthaler I. 1997. Comparative distribution of estrogen receptor-a and -β in the rat central nervous system. J Comp Neurol 388:507-525.
127. Shughrue PJ, Lane MV, Merchenthaler I. 1999. Biologically active estrogen receptor-β: evidence from in vivo autoradiographic studies with estrogen receptor α-knockout mice. Endocrinology 140:2613-2620.
128. Singh M. 2001. Ovarian hormones elicit phosphorylation of Akt and extracellular-signal regulated kinase in explants of the cerebral cortex. Endocrine 14:407-415.
129. Singh M, Meyer EM, Millard WJ, Simpkins JW. 1994. Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res 644:305-312.
130. Slooter AJ, Bronzova J, Witteman JC, Van Broeckhoven C, Hofman A, et al. 1999. Estrogen use and early onset Alzheimer's disease: a population-based study. J Neurol Neurosurg Psychiatry 67:779-781.
131. Smith CL, O'Malley. 2004. Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endo Rev 25:45-71.
132. Stackman WR, Blasberg ME, Langan CJ, Clark AS. 1997. Stability of spatial working memory across the estrous cycle of Long-Evens rats. Neurobiol Learn Mem 67:167-171.
133. Steckler T, Drinkenburgh WHIM, Sahgal A, Aggleton JPP. 1998. Recognition memory in rats-II. Neuroanatomical substrates. Prog Neurobiol 54:313-332.
134. Szuran TF, Pliska V, Pokorny J, Welzl H. 2000. Prenatal stress in rats: effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol Behav 71:353-362.
135. Tang Y, Janssen W, Hao J, Roberts JA, McKay H, et al. 2004. Estrogen replacement increase spinophilin-immunoreactive spine number in the prefrontal cortex of female rhesus monkeys. Cerebral Cortex 14:215-223.
136. Tanapat P, Hastings NB, Reeves AJ, Gould E. 1999. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792-5801.
137. Tierney MC, Luine VN. 1997. New Concepts in Hormone Replacement: Selective Estrogen Receptor Modulators (SERMS) IV. Effects of estrogens and antiestrogens on the CNS. Supplement to J Can Soc Of Gyn and Obst 19:46-56.
138. Toran-Allerand CD, Guan X, MacLusky NJ, Horvath TL, Diano S, Singh M, Connolly ES, Nethrapalli TS, Tinnikov AA, 2002. ER-X: a novel, plasma membraneassociated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J Neurosci 22:8391-8401.
139. Toran-Allerand CD, Singh M, Setalo G Jr. 1999. Novel mechanisms of estrogen action in the brain: new players in an old story. Front Neuroendocrinol 20:97-121.
140. Towart LA, Alves SE, Znamensky V, Hayashi S, McEwen BS, et al. 2003. Subcellular relationships between cholinergic terminals and estrogen receptor α in the dorsal hippocampus. J Comp Neurol 463:390-401.
141. Tsai M-J, O'Malley BW. 1994. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Ann Rev Biochem 63:451-486.
142. Turgeon JL, McDonnell DP, Martin KA, Wise PM. 2004. Hormone therapy: Physiological complexity belies therapeutic simplicity. Science 304:1269-1273.
143. Uno H, Tarara R, Else JG, Suleman MA, Sapolsky RM. 1989. Hippocampal damage associated with prolonged and fatal stress in primates. J Neurosci 9:1705-1711.
144. van Steensel B, van Binnendijk EP, Hornsby CDE. 1996. Partial colocalization of glucocorticoid and mineralocorticoids receptors in discrete compartments in nuclei of rat hippocampus neurons. J Cell Sci 109:787-792.
145. van Wimersma Greidanus TB, Rigter H. 1989. Hormonal regulation of learning performance. Psychoendocrinology, Brush, FB, Levine S. (editors), New York: Academic Press, Inc; pp. 271-304.
146. Voytko ML, Tinkler GP. 2004. Cognitive function and its neural mechanisms in nonhuman primate modesl of aging, Alzheimer disease and menopause Front Biosci 9:1899-1914.
147. Wade CB, Robinson S, Shapiro RA, Dorsa DM. 2001. Estrogen receptor (ER) α and ERβ exhibit unique pharmacologic properties when coupled to activation of the mitogenactivated protein kinase pathway. Endocrinology 142:2336-2342.
148. Warren SG, Juraska JM. 1997. Spatial and nonspatial learning across the rat estrous cycle. Behav Neurosci 111:259-266.
149. Wassertheil-Smoller S, Hendrix SL, Limacher M, Heiss G, Kooperberg C, et al. 2003. Effects of estrogen plus progestin on stroke in postmenopausal women: the Women's Health Initiative: a randomized trial. JAMA 289:2673-2684.
150. Watanabe Y, Gould E, McEwen BS. 1992. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588:341-345.
151. Wellman CL. 2001. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol 49:245-253.
152. White NM, McDonald RB. 2002. Theoretical Review: Multiple Parallel memory systems in the brain of the rat. Neurobiol Learn & Mem 77:125-184.
153. Wickelgren, I. 1997. Research News-Estrogen stakes claim to cognition, Science 276:675-678.
154. Williams CL, Barnett AM, Meck WH. 1990. Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav Neurosci 104:84-97.
155. Wise PM, Dubal DB, Wilson ME, Rau SW, Bottner M. 2001. Minireview: neuroprotective effects of estrogen-New insights into mechanisms of action. Endocrinology 142:969-973.
156. Wolf OT. 2003. HPA axis and memory. Best Pract Res Clin Endo And Metab 17:287-299.
157. Wolf OT, Schommer NC, Hellhammer DH, McEwen BS. Kirschbaum C. 2001. The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology 26:711-720.
158. Wood GE, Shors TJ. 1998. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proc Natl Acad Sci USA 95:4066-4071.
159. Woolley CS, McEwen BS. 1992. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12:2549-2554.
160. Yaffe K, Lui LY, Grady D, Cauley J, Kramer J, et al. 2000. Cognitive decline in women in relation to non-proteinbound oestradiol concentrations. Lancet 356:708-712.
161. Yaffe K, Lui LY, Zmuda J, Cauley J. 2002. Sex hormones and cognitive functionin older men. J Am Geriatr Soc 50:707-712.
162. Zec RF, Trivedi MA. 2002. Effects of hormone replacement therapy on cognitive aging and dementia risk in postmenopausal women: a review of ongoing large-scale, long-term clinical trials. Climacteric 5:122-134.
163. Znamensky V, Akama KT, McEwen BS, Milner TA. 2003. Estrogen levels regulate the subcellular distribution of phosphorylated Akt in hippocampal CA1 dendrites. J Neurosci 23:2340-2347.