Neuroscientists as cartographers: Mapping the crossroads of gonadal hormones, memory and age using animal models

Molecules

Volumn 15, Issue 9, 2010, Pages 6050-6105

  Bimonte Nelson, Heather A ^a,b   Acosta, Jazmin I ^a,b   Talboom, Joshua S ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA ALZHEIMER S CONSORTIUM   (United States)

Author keywords

Aging; Androgens; Cognition; Estrogen; Progesterone

Indexed keywords

SEX HORMONE;

AGING; ANIMAL; ANIMAL MODEL; BRAIN MAPPING; HUMAN; MEMORY; METHODOLOGY; NEUROSCIENCE; REVIEW;

AGING; ANIMALS; BRAIN MAPPING; GONADAL HORMONES; HUMANS; MEMORY; MODELS, ANIMAL; NEUROSCIENCES;

EID: 77957309815     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules15096050     Document Type: Review

References (349)

1. U. S. Census Bureau. Population Information. http://www.census.gov/ipc/ www/world.html/. (accessed online on April 21, 2007.)
2. Erickson, C. A.; Barnes, C. A. The neurobiology of memory changes in normal aging. Exp. Gerontol. 2003, 38, 61-69.
3. Tulving, E.; Craik, F. I. The Oxford Handbook of Memory; Oxford University Press: New York, NY, USA, 2000.
4. Kausler, D. H. Learning and Memory in Normal Aging; Academic Press: New York, NY, USA, 1994.
5. Balota, D. A.; Dolan, P. O.; Duchek, J. M. Memory changes in healthy young and older adults. In The Oxford Handbook of Memory; Oxford University Press: New York, NY, USA, 2000. pp. 395-410.
6. Albert, M.; Duffy, F. H.; Naeser, M. Nonlinear changes in cognition with age and their neuropsychologic correlates. Can. J. Psychol. 1987, 41, 141-157.
7. Albert, M. S. Memory decline: the boundary between aging and age-related disease. Annal. Neurol. 2002, 51, 282-284.
8. Barnes, C. A. Memory changes during normal aging: Neurobiological correlates. In Neurobiology of Learning and Memory; Martinez, J. A., Jr.; Kesner, R. P., Eds.; Academic Press: San Diego, CA, USA, 1998; pp. 247-273.
9. Tolman, E. C. Cognitive maps in rats and men. Psychol. Rev. 1948, 55, 189-208.
10. O'Keefe, J.; Nadel, L. The Hippocampus as a Cognitive Map; Clarendon Press: Oxford, England, 1978.
11. Eichenbaum, H. A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 2000, 1, 41-50.
12. Burke, S. N.; Barnes, C. A. Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 2006, 7, 30-40.
13. Kabaso, D.; Coskren, P. J.; Henry, B. I.; Hof, P. R.; Wearne, S. L. The electrotonic structure of pyramidal neurons contributing to prefrontal cortical circuits in macaque monkeys is significantly altered in aging. Cereb. Cortex 2009, 19, 2248-2268.
14. Baddeley, A. D.; Hitch, G. J. Working Memory. In The Psychology of Learning and Motivation: Advances in Research and Theory; Bower, G. A., Ed.; Academic Press: New York, NY, USA, 1974; Volume 8, pp. 47-90.
15. Olton, D. S.; Becker, J. T.; Handelmann, G. E. Hippocampus, space, and memory. Behav. Brain Sci. 1979, 2, 313-365.
16. Armstrong, D. M.; Sheffield, R.; Buzsaki, G.; Chen, K. S.; Hersh, L. B.; Nearing, B.; Gage, F. H. Morphologic alterations of choline acetyltransferase- positive neurons in the basal forebrain of aged behaviorally characterized Fisher 344 rats. Neurobiol. Aging 1993, 14, 457-470.
17. Croll, S. D.; Ip, N. Y.; Lindsay, R. M.; Wiegand, S. J. Expression of BDNF and trkB as a function of age and cognitive performance. Brain Res. 1998, 812, 200-208.
18. Diana, G.; Domenici, M. R.; Scotti de Carolis, A.; Loizzo, A.; Sagratella, S. Reduced hippocampal CA1 Ca (2+)-induced long-term potentiation is associated with age-dependent impairment of spatial learning. Brain Res. 1995, 686, 107-110.
19. Fischer, W.; Bjorklund, A.; Chen, K.; Gage, F. H. NGF improves spatial memory in aged rodents as a function of age. J. Neurosci. 1991, 11, 1889-1906.
20. Hasenohrl, R. U.; Soderstrom, S.; Mohammed, A. H.; Ebendal, T.; Huston, J. P. Reciprocal changes in expression of mRNA for nerve growth factor and its receptors TrkA and LNGFR in brain of aged rats in relation to maze learning deficits. Exp. Brain Res. 1997, 114, 205-213.
21. Lindner, M. D.; Kearns, C. E.; Winn, S. R.; Frydel, B.; Emerich, D. F. Effects of intraventricular encapsulated hNGF-secreting fibroblasts in aged rats. Cell Transplant. 1996, 5, 205-223.
22. Nilsson, O. G.; Gage, F. H. Anticholinergic sensitivity in the aging rat septohippocampal system as assessed in a spatial memory task. Neurobiol. Aging 1993, 14, 487-497.
23. Quirion, R.; Wilson, A.; Rowe, W.; Aubert, I.; Richard, J.; Doods, H.; Parent, A.; White, N.; Meaney, M. J. Facilitation of acetylcholine release and cognitive performance by an M (2) - muscarinic receptor antagonist in aged memory-impaired. J. Neurosci. 1995, 15, 1455-1462.
24. Rapp, P. R.; Gallagher, M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc. Nat. Acad. Sci. USA 1996, 93, 9926-9930.
25. Sugaya, K.; Greene, R.; Personett, D.; Robbins, M.; Kent, C.; Bryan, D.; Skiba, E.; Gallagher, M.; McKinney, M. Septo-hippocampal cholinergic and neurotrophin markers in age-induced cognitive decline. Neurobiol. Aging 1998, 19, 351-361.
26. Croll, S. D.; Chesnutt, C. R.; Greene, N. A.; Lindsay, R. M.; Wiegand, S. J. Peptide immunoreactivity in aged rat cortex and hippocampus as a function of memory and BDNF infusion. Pharmacol. Biochem. Behav. 1999, 64, 625-635.
27. Timaras, P.; Quay, W.; Vernadakis, A. Hormones and Aging; CRC Press: New York, NY, USA, 1995.
28. Downs, J. L.; Wise, P. M. The role of the brain in female reproductive aging. Mol. Cell. Endocrinol. 2009, 299, 32-38.
29. Meites, J.; Lu, J. K. H. Reproductive aging and neuroendocrine function. In Oxford Review of Reproductive Biology; Charlton, H. M., Ed.; Oxford Press: New York, NY, USA, 1994.
30. Newman, M.; Kasznaik, A. Spatial memory and aging: performance on a human analog of the Morris water maze. Aging. Neuropsychol. Cogn. 2000, 7, 86-93.
31. Wilkniss, S. M.; Jones, M. G.; Korol, D. L.; Gold, P. E.; Manning, C. A. Age-related differences in an ecologically based study of route learning. Psychol. Aging 1997, 12, 372-375.
32. 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.
33. Head, E.; Mehta, R.; Hartley, J.; Kameka, M.; Cummings, B. J.; Cotman, C. W.; Ruehl, W. W.; Milgram, N. W. Spatial learning and memory as a function of age in the dog. Behav. Neurosci 1995, 109, 851-858.
34. Barnes, C. A.; Nadel, L.; Honig, W. K. Spatial memory deficit in senescent rats. Can. J. Psychol. 1980, 34, 29-39.
35. Bimonte, H. A.; Nelson, M. E.; Granholm, A. C. Age-related deficits as working memory load increases: relationships with growth factors. Neurobiol. Aging 2003, 24, 37-48.
36. Markowska, A. L. Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J. Neurosci. 1999, 19, 8122-8133.
37. Arendash, G. W.; Sanberg, P. R.; Sengstock, G. J. Nicotine enhances the learning and memory of aged rats. Pharmacol. Biochem. Behav. 1995, 52, 517-523.
38. Beatty, W. W.; Bierley, R. A.; Boyd, J. G. Preservation of accurate spatial memory in aged rats. Neurobiol. Aging 1985, 6, 219-225.
39. Bond, N. W.; Everitt, A. V.; Walton, J. Effects of dietary restriction on radial-arm maze performance and flavor memory in aged rats. Neurobiol. Aging 1989, 10, 27-30.
40. Chrobak, J. J.; Hanin, I.; Lorens, S. A.; Napier, T. C. Within-subject decline in delayed-non-matchto-sample radial arm maze performance in aging Sprague-Dawley rats. Behav. Neurosci. 1995, 109, 241-245.
41. Frick, K. M.; Baxter, M. G.; Markowska, A. L.; Olton, D. S.; Price, D. L. Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol. Aging 1995, 16, 149-160.
42. Kadar, T.; Arbel, I.; Silbermann, M.; Levy, A., Morphological hippocampal changes during normal aging and their relation to cognitive deterioration. J. Neural Transm. 1994, 44, 133-143.
43. Lebrun, C.; Durkin, T. P.; Marighetto, A.; Jaffard, R. A comparison of the working memory performances of young and aged mice combined with parallel measures of testing and druginduced activations of septo-hippocampal and nbm-cortical cholingergic neurones. Neurobiol. Aging 1990, 11, 515-521.
44. Lindner, M. D.; Balch, A. H.; Vander Maelen, C. P. Short forms of the "reference-" and "workingmemory" Morris water maze for assessing age-related deficits. Behav. Neural Biol. 1992, 58, 94-102.
45. Noda, Y.; Yamada, K.; Nabeshima, T. Role of nitric oxide in the effect of aging on spatial memory in rats. Behav. Brain Res. 1997, 83, 153-158.
46. Pitsikas, N.; Algeri, S. Deterioration of spatial and nonspatial reference and working memory in aged rats: Protective effect of life-long calorie restriction. Neurobiol. Aging 1992, 13, 369-373.
47. Rapp, P. R.; Rosenberg, R. A.; Gallagher, M. An evaluation of spatial information processing in aged rats. Behav. Neurosci. 1987, 101, 3-12.
48. Shukitt-Hale, B.; McEwen, J. J.; Szrengiel, A.; Joseph, J. A. Effect of age on the radial arm water maze-a test of spatial learning and memory. Neurobiol. Aging 2004, 25, 223-229.
49. Stewart, J.; Mitchell, J.; Kalant, N. The effects of life-long food restriction on spatial memory in young and aged Fischer 344 rats measured in the eight-arm radial and the Morris water mazes. Neurobiol. Aging 1989, 10, 669-675.
50. Wallace, J. E.; Krauter, E. E.; Campbell, B. A. Animal models of declining memory in the aged: short-term and spatial memory in the aged rat. J. Gerontol. 1980, 35, 355-363.
51. Wellman, C. L.; Pelleymounter, M. A. Differential effects of nucleus basalis lesions in young adult and aging rats. Neurobiol. Aging 1999, 20, 381-393.
52. Wyss, J. M.; Chambless, B. D.; Kadish, I.; van Groen, T. Age-related decline in water maze learning and memory in rats: strain differences. Neurobiol. Aging 2000, 21, 671-681.
53. 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. Memory 2008, 90, 155-163.
54. Ikegami, S. Behavioral impairment in radial-arm maze learning and acetylcholine content of the hippocampus and cerebral cortex in aged mice. Behav. Brain Res. 1994, 65, 103-111.
55. Salthouse, T. A.; Mitchell, D. R.; Palmon, R. Memory and age differences in spatial manipulation ability. Psychol. Aging 1989, 4, 480-486.
56. Aggleton, J. P.; Blindt, H. S.; Candy, J. M. Working memory in aged rats. Behav. Neurosci. 1989, 103, 975-983.
57. Bimonte-Nelson, H. A.; Singleton, R. S.; Hunter, C. L.; Price, K. L.; Moore, A. B.; Granholm, A. C. Ovarian hormones and cognition in the aged female rat: I. Long-term, but not short-term, ovariectomy enhances spatial performance. Behav. Neurosci. 2003, 117, 1395-406.
58. Bimonte-Nelson, H. A.; Singleton, R. S.; Williams, B. J.; Granholm, A. C. Ovarian hormones and cognition in the aged female rat: II. progesterone supplementation reverses the cognitive enhancing effects of ovariectomy. Behav. Neurosci. 2004, 118, 707-714.
59. Dunnett, S. B.; Evenden, J. L.; Iversen, S. D. Delay-dependent short-term memory deficits in aged rats. Psychopharmacology 1988, 96, 174-180.
60. Winocur, G. Memory decline in aged rats: a neuropsychological interpretation. J. Gerontol. 1986, 41, 758-763.
61. Zornetzer, S. F.; Thompson, R.; Rogers, J. Rapid forgetting in aged rats. Behav. Neural Biol. 1982, 36, 49-60.
62. Willig, F.; Palacios, A.; Monmaur, P.; M'Harzi, M.; Laurent, J.; Delacour, J. Short-term memory, exploration and locomotor activity in aged rats. Neurobiol. Aging 1987, 8, 393-402.
63. Adler, N. T. Neuroendocrinology of Reproduction: Physiology and Behavior; Plenum Press: New York, NY, USA, 1981.
64. Beach, F. A. Hormones and mating behaviora in vertebrates. In Recent Progress in Hormone Research; Academic Press: New York, NY, USA, 1947.
65. Luetters, C.; Huang, M. H.; Seeman, T.; Buckwalter, G.; Meyer, P. M.; Avis, N. E.; Sternfeld, B.; Johnston, J. M.; Greendale, G. A. Menopause transition stage and endogenous estradiol and follicle-stimulating hormone levels are not related to cognitive performance: cross-sectional results from the study of women's health across the nation (SWAN). J. Women's Health 2007, 16, 331-344.
66. Gomez-Gil, E.; Canizares, S.; Torres, A.; De La Torre, F.; Halperin, I.; Salamero, M. Androgen treatment effects on memory in female-to-male transsexuals. Psychoneuroendocrinology 2009, 34, 110-117.
67. Sherwin, B. B. Estrogen and cognitive aging in women. Neuroscience 2006, 138, 1021-1026.
68. Yaffe, K.; Sawaya, G.; Lieberburg, I.; Grady, D. Estrogen therapy in postmenopausal women: effects on cognitive function and dementia. J. Am. Med. Assoc. 1998, 279, 688-695.
69. Asthana, S.; Craft, S.; Baker, L. D.; Raskind, M. A.; Birnbaum, R. S.; Lofgreen, C. P.; Veith, R. C.; Plymate, S. R. Cognitive and neuroendocrine response to transdermal estrogen in postmenopausal women with Alzheimer's disease: results of a placebo-controlled, double-blind, pilot study. Psychoneuroendocrinology 1999, 24, 657-677.
70. Asthana, S.; Baker, L. D.; Craft, S.; Stanczyk, F. Z.; Veith, R. C.; Raskind, M. A.; Plymate, S. R. High-dose estradiol improves cognition for women with AD: results of a randomized study. Neurology 2001, 57, 605-612.
71. Ohkura, T.; Isse, K.; Akazawa, K.; Hamamoto, M.; Yaoi, Y.; Hagino, N. Evaluation of estrogen treatment in female patients with dementia of the Alzheimer type. Endocr. J. 1994, 41, 361-371.
72. Ohkura, T.; Isse, K.; Akazawa, K.; Hamamoto, M.; Yaoi, Y.; Hagino, N. Long-term estrogen replacement therapy in female patients with dementia of the Alzheimer type: 7 case reports. Dementia 1995, 6, 99-107.
73. Halbreich, U.; Lumley, L. A.; Palter, S.; Manning, C.; Gengo, F.; Joe, S. H. Possible acceleration of age effects on cognition following menopause. J. Psychiat. Res. 1995, 29, 153-163.
74. 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.
75. Singh, G. K.; Kochanek, K. D.; MacDorman, M. F. Advance report of final mortality statistics, 1994. Mon. Vital Stat. Rep. 1996, 45, 1-80.
76. Amundsen, D. W.; Diers, C. J. The age of menopause in classical Greece and Rome. Hum. Biol. 1970, 42, 79-86.
77. Amundsen, D. W.; Diers, C. J. The age of menopause in medieval Europe. Hum. Biol. 1973, 45, 605-612.
78. Sherwin, B. B. Estrogen and cognitive functioning in women. Endocr. Rev. 2003, 24, 133-151.
79. Sherwin, B. B. Estrogen and cognitive functioning in women. Proc. Soc. Exp. Biol. Med. 1998, 217, 17-22.
80. Nyberg, L.; McIntosh, A. R.; Cabeza, R.; Habib, R.; Houle, S.; Tulving, E. General and specific brain regions involved in encoding and retrieval of events: what, where, and when. Proc. Nat. Acad. Sci. USA 1996, 93, 11280-11285.
81. Schacter, D. L.; Curran, T.; Reiman, E. M.; Chen, K.; Bandy, D. J.; Frost, J. T. Medial temporal lobe activation during episodic encoding and retrieval: a PET study. Hippocampus 1999, 9, 575-581.
82. Schacter, D. L.; Wagner, A. D. Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus 1999, 9, 7-24.
83. Grunwald, T.; Lehnertz, K.; Heinze, H. J.; Helmstaedter, C.; Elger, C. E. Verbal novelty detection within the human hippocampus proper. Proc. Nat. Acad. Sci. USA 1998, 95, 3193-3197.
84. Grunwald, T.; Kurthen, M. Novelty detection and encoding for declarative memory within the human hippocampus. Clin. EEG Neurosci. 2006, 37, 309-314.
85. Resnick, S. M.; Maki, P. M.; Golski, S.; Kraut, M. A.; Zonderman, A. B. Effects of estrogen replacement therapy on PET cerebral blood flow and neuropsychological performance. Horm. Behav. 1998, 34, 171-182.
86. Maki, P. M.; Resnick, S. M. Longitudinal effects of estrogen replacement therapy on PET cerebral blood flow and cognition. Neurobiol. Aging 2000, 21, 373-383.
87. Acosta, J. I.; Mayer, L.; Talboom, J. S.; Tsang, C. W.; Smith, C. J.; Enders, C. K.; Bimonte-Nelson, H. A. Transitional versus surgical menopause in a rodent model: etiology of ovarian hormone loss impacts memory and the acetylcholine system. Endocrinology 2009, 150, 4248-4259.
88. Aenlle, K. K.; Kumar, A.; Cui, L.; Jackson, T. C.; Foster, T. C., Estrogen effects on cognition and hippocampal transcription in middle-aged mice. Neurobiol. Aging 2009, 30, 932-945.
89. Markham, J. A.; Pych, J. C.; Juraska, J. M. Ovarian hormone replacement to aged ovariectomized female rats benefits acquisition of the morris water maze. Horm. Behav. 2002, 42, 284-293.
90. 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 2010, In Press.
91. Braden, B. B.; Talboom, J. S.; Crain, I. D.; Simard, A. R.; Lukas, R. J.; Prokai, L.; Scheldrup, M. R.; Bowman, B. L.; Bimonte-Nelson, H. A. Medroxyprogesterone acetate impairs memory and alters the GABAergic system in aged surgically menopausal rats. Neurobiol. Learn. Memory 2010, 93, 444-453.
92. Acosta, J. I.; Mayer, L.; Braden, B. B.; Nonnenmacher, S.; Mennenga, S.; Bimonte, H. A. The cognitive effects of CEE depend on whether menopause is transitional or surgical. Endocrinology 2010, in press.
93. 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.
94. Frick, K. M.; Fernandez, S. M.; Bulinski, S. C. Estrogen replacement improves spatial reference memory and increases hippocampal synaptophysin in aged female mice. Neuroscience 2002, 115, 547-558.
95. 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.
96. Foster, T. C.; Sharrow, K. M.; Kumar, A.; Masse, J. Interaction of age and chronic estradiol replacement on memory and markers of brain aging. Neurobiol. Aging 2003, 24, 839-852.
97. Bimonte-Nelson, H. A.; Francis, K. R.; Umphlet, C. D.; Granholm, A. C. Progesterone reverses the spatial memory enhancements initiated by tonic and cyclic oestrogen therapy in middle-aged ovariectomized female rats. Eur. J. Neurosci. 2006, 24, 229-242.
98. Markowska, A. L.; Savonenko, A. V. Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen replacement withdrawal in aging rats. J. Neurosci. 2002, 22, 10985-10995.
99. Savonenko, A. V.; Markowska, A. L. The cognitive effects of ovariectomy and estrogen replacement are modulated by aging. Neuroscience 2003, 119, 821-830.
100. McDonald, R. J.; White, N. M. A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav. Neurosci. 1993, 107, 3-22.
101. Morris, R. G.; Garrud, P.; Rawlins, J. N.; O'Keefe, J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297, 681-683.
102. Squire, L. R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 1992, 99, 195-231.
103. 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.
104. Greendale, G. A.; Wight, R. G.; Huang, M. H.; Avis, N.; Gold, E. B.; Joffe, H.; Seeman, T.; Vuge, M.; Karlamangla, A. S. Menopause-associated symptoms and cognitive performance: Results from the study of Women's Health Across the Nation. Am. J. Epidemiol. 2010, 171, 1214-1224.
105. Thilers, P. P.; Macdonald, S. W.; Nilsson, L. G.; Herlitz, A. Accelerated postmenopausal cognitive decline is restricted to women with normal BMI: longitudinal evidence from the Betula project. Psychoneuroendocrinology 2010, 35, 516-524.
106. Weber, M.; Mapstone, M. Memory complaints and memory performance in the menopausal transition. Menopause 2009, 16, 694-700.
107. Farrag, A. K.; Khedr, E. M.; Abdel-Aleem, H.; Rageh, T. A. Effect of surgical menopause on cognitive functions. Dement. Geriat. Cogn. Disorder. 2002, 13, 193-198.
108. Phillips, S. M.; Sherwin, B. B. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology 1992, 17, 485-495.
109. Sherwin, B. B. Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology 1988, 13, 345-357.
110. 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.
111. Bimonte, H. A.; Denenberg, V. H. Estradiol facilitates performance as working memory load increases. Psychoneuroendocrinology 1999, 24, 161-173.
112. El-Bakri, N. K.; Islam, A.; Zhu, S.; Elhassan, A.; Mohammed, A.; Winblad, B.; Adem, A. Effects of estrogen and progesterone treatment on rat hippocampal NMDA receptors: relationship to Morris water maze performance. J. Cell. Mol. Med. 2004, 8, 537-544.
113. 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. Physiol. Behav. 1999, 66, 11-20.
114. Feng, Z.; Cheng, Y.; Zhang, J. T. Long-term effects of melatonin or 17 beta-estradiol on improving spatial memory performance in cognitively impaired, ovariectomized adult rats. J. Pineal Res. 2004, 37, 198-206.
115. Gibbs, R. B.; Johnson, D. A. Sex-specific effects of gonadectomy and hormone treatment on acquisition of a 12-arm radial maze task by Sprague Dawley rats. Endocrinology 2008, 149, 3176-3183.
116. Wallace, M.; Luine, V.; Arellanos, A.; Frankfurt, M. Ovariectomized rats show decreased recognition memory and spine density in the hippocampus and prefrontal cortex. Brain Res. 2006, 1126, 176-182. (Pubitemid 44880922)
117. Springer, L. N.; McAsey, M. E.; Flaws, J. A.; Tilly, J. L.; Sipes, I. G.; Hoyer, P. B. Involvement of apoptosis in 4-vinylcyclohexene diepoxide-induced ovotoxicity in rats. Toxicol. Appl. Pharmacol. 1996, 139, 394-401.
118. Mayer, L. P.; Devine, P. J.; Dyer, C. A.; Hoyer, P. B. The follicle-deplete mouse ovary produces androgen. Biol. Reprod. 2004, 71, 130-138.
119. Rocca, W. A.; Bower, J. H.; Maraganore, D. M.; Ahlskog, J. E.; Grossardt, B. R.; de Andrade, M.; Melton, L. J., 3rd. Increased risk of cognitive impairment or dementia in women who underwent oophorectomy before menopause. Neurology 2007, 69, 1074-1083.
120. Kuhl, H. Pharmacology of estrogens and progestogens: influence of different routes of administration. Climacteric 2005, 8, 3-63.
121. Sitruk-Ware, R. Hormonal replacement therapy. Rev. Endocr. Metab. Disorder. 2002, 3, 243-256.
122. Daniel, J. M.; Fader, A. J.; Spencer, A. L.; Dohanich, G. P. Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm. Behav. 1997, 32, 217-225.
123. Dohanich, G. P.; Fader, A. J.; Javorsky, D. J. Estrogen and estrogen-progesterone treatments counteract the effect of scopolamine on reinforced T-maze alternation in female rats. Behav. Neurosci. 1994, 108, 988-992.
124. 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. Behav. Brain Res. 2001, 126, 115-126.
125. Holmes, M. C.; Wide, J. K.; Galea, L. A. M. Low levels of estradiol facilitate, whereas high levels of estradiol impair, working memory performance on the radial arm maze. Behav. Neurosci. 2002, 116, 928-934.
126. Luine, V. N.; Richards, S. T.; Wu, V. Y.; Beck, K. D. Estradiol enhances learning and memory in a spatial memory task and effects of monoaminergic neurotransmitters. Horm. Behav. 1998, 34, 149-162.
127. Luine, V. N.; Jacome, L. F.; Maclusky, N. J. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 2003, 144, 2836-2844.
128. Marriott, L. K.; Korol, D. L. Short-term estrogen treatment in ovariectomized rats augments hippocampal acetylcholine release during place learning. Neurobiol. Learn. Memory 2003, 80, 315-322.
129. McLaughlin, K. J.; Bimonte-Nelson, H. A.; Neisewander, J. L.; Conrad, C. D. Assessment of estradiol influence on spatial tasks and hippocampal CA1 spines: Evidence that the duration of hormone deprivation after ovariectomy compromises 17β-estradiol effectiveness in altering CA1 spines. Horm. Behav. 2008, 54, 386-395.
130. Packard, M. G.; Teather, L. A. Posttraining estradiol injections enhance memory in ovariectomized rats: cholinergic blockade and synergism. Neurobiol. Learn. Memory 1997, 68, 172-188.
131. Sandstrom, N. J.; Williams, C. L. Memory retention is modulated by acute estradiol and progesterone replacement. Behav. Neurosci. 2001, 115, 384-393.
132. Singh, M.; Meyer, E. M.; Millard, W. J.; Simpkins, J. W. Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res. 1994, 644, 305-312.
133. Fernandez, S. M.; Frick, K. M. Chronic oral estrogen affects memory and neurochemistry in middle-aged female mice. Behav. Neurosci. 2004, 118, 1340-1351.
134. Lewis, M. C.; Kerr, K. M.; Orr, P. T.; Frick, K. M. Estradiol-induced enhancement of object memory consolidation involves NMDA receptors and protein kinase A in the dorsal hippocampus of female C57BL/6 mice. Behav. Neurosci. 2008, 122, 716-721.
135. Broadbent, N. J.; Squire, L. R.; Clark, R. E. Spatial memory, recognition memory, and the hippocampus. Proc. Nat. Acad. Sci. USA 2004, 101, 14515-14520.
136. Forwood, S. E.; Winters, B. D.; Bussey, T. J. Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours. Hippocampus 2005, 15, 347-355.
137. Hammond, R. S.; Tull, L. E.; Stackman, R. W. On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiol. Learn. Memory 2004, 82, 26-34.
138. Fernandez, S. M.; Lewis, M. C.; Pechenino, A. S.; Harburger, L. L.; Orr, P. T.; Gresack, J. E.; Schafe, G. E.; Frick, K. M. Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J. Neurosci. 2008, 28, 8660-8667.
139. Voytko, M. L. Estrogen and the cholinergic system modulate visuospatial attention in monkeys (Macaca fascicularis). Behav. Neurosci. 2002, 116, 187-197.
140. Voytko, M. L. The effects of long-term ovariectomy and estrogen replacement therapy on learning and memory in monkeys (Macaca fascicularis). Behav. Neurosci. 2000, 114, 1078-1187.
141. Lacreuse, A.; Herndon, J. G. Estradiol selectively affects processing of conspecifics' faces in female rhesus monkeys. Psychoneuroendocrinology 2003, 28, 885-905.
142. Blaustein, J. D. An estrogen by any other name. Endocrinology 2008, 149, 2697-2698.
143. Daniel, J. M. Effects of oestrogen on cognition: What have we learned from basic research? J. Neuroendocr. 2006, 18, 787-795.
144. Caldwell, B. M.; Watson, R. I. An evaluation of psychologic effects of sex hormone administration in aged women. I. Results of therapy after six months. J. Gerontol. 1952, 7, 228-244.
145. Hersh, A. L.; Stefanick, M. L.; Stafford, R. S. National use of postmenopausal hormone therapy: annual trends and response to recent evidence. J. Am. Med. Assoc. 2004, 291, 47-53.
146. Bhavnani, B. R. Estrogens and menopause: pharmacology of conjugated equine estrogens and their potential role in the prevention of neurodegenerative diseases such as Alzheimer's. J. Steroid Biochem. Mol. Biol. 2003, 85, 473-482.
147. Campbell, S.; Whitehead, M. Oestrogen therapy and the menopausal syndrome. Clin. Obstet. Gynaecol. 1977, 4, 31-47.
148. Kantor, H. I.; Michael, C. M.; Shore, H. Estrogen for older women. Am. J. Obstet. Gynecol. 1973, 116, 115-158.
149. Shumaker, S. A.; Legault, C.; Rapp, S. R.; Thal, L.; Wallace, R. B.; Ockene, J. K.; Hendrix, S. L.; Jones, B. N., 3rd; 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. J. Am. Med. Assoc. 2003, 289, 2651-2662.
150. 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. J. Am. Med. Assoc. 2004, 291, 2959-2968.
151. 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. J. Am. Med. Assoc. 2004, 291, 2947-2958.
152. Resnick, S. M.; Maki, P. M.; Rapp, S. R.; Espeland, M. A.; Brunner, R.; Coker, L. H.; Granek, I. A.; Hogan, P.; Ockene, J. K.; Shumaker, S. A. Effects of combination estrogen plus progestin hormone treatment on cognition and affect. J. Clin. Endocrinol. Metab. 2006, 91, 1802-1810.
153. 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.
154. Shumaker, S. A.; Reboussin, B. A.; Espeland, M. A.; Rapp, S. R.; McBee, W. L.; Dailey, M.; Bowen, D.; Terrell, T.; Jones, B. N. The Women's Health Initiative Memory Study (WHIMS): a trial of the effect of estrogen therapy in preventing and slowing the progression of dementia. Control Clin. Trials 1998, 19, 604-621.
155. Bohacek, J.; Bearl, A. M.; Daniel, J. M. Long-term ovarian hormone deprivation alters the ability of subsequent oestradiol replacement to regulate choline acetyltransferase protein levels in the hippocampus and prefrontal cortex of middle-aged rats. J. Neuroendocrinol. 2008, 20, 1023-1027.
156. Woolley, C. S. Effects of oestradiol on hippocampal circuitry. Novart. Fdn. Symp. 2000, 230, 173-180; discussion 181-187.
157. 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.
158. Voytko, M. L.; Higgs, C. J.; Murray, R. Differential effects on visual and spatial recognition memory of a novel hormone therapy regimen of estrogen alone or combined with progesterone in older surgically menopausal monkeys. Neuroscience 2008, 154, 1205-1217.
159. 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.
160. Lacreuse, A.; Wilson, M. E.; Herndon, J. G. Estradiol, but not raloxifene, improves aspects of spatial working memory in aged ovariectomized rhesus monkeys. Neurobiol. Aging 2002, 23, 589-600.
161. Luine, V.; Rodriguez, M. Effects of estradiol on radial arm maze performance of young and aged rats. Behav. Neural Biol. 1994, 62, 230-236.
162. Ziegler, D. R.; Gallagher, M. Spatial memory in middle-aged female rats: Assessment of estrogen replacement after ovariectomy. Brain Res. 2005, 1052, 163-173.
163. Beason-Held, L. L.; Rosene, D. L.; Killiany, R. J.; Moss, M. B. Hippocampal formation lesions produce memory impairment in the rhesus monkey. Hippocampus 1999, 9, 562-574.
164. 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, 18, 13-19.
165. 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.
166. 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.
167. Frick, K. M.; Fernandez, S. M.; Bennett, J. C.; Prange-Kiel, J.; MacLusky, N. J.; Leranth, C. Behavioral training interferes with the ability of gonadal hormones to increase CA1 spine synapse density in ovariectomized female rats. Eur. J. Neurosci. 2004, 19, 3026-3032. (Pubitemid 38822593)
168. Bagger, Y. Z.; Tanko, L. B.; Alexandersen, P.; Qin, G.; Christiansen, C. Early postmenopausal hormone therapy may prevent cognitive impairment later in life. Menopause 2005, 12, 12-17.
169. North American Menopause Society. Estrogen and progestogen use in postmenopausal women: 2010. position statement of The North American Menopause Society. Menopause. 2010, 17, 242-255.
170. Stovall, D. W.; Beard, M. K.; Barbier, S.; Chen, E.; Rosenberg, E.; De Papp, A. E. Response to oral bisphosphonates in subgroups of younger and older postmenopausal women. J. Womens Health (Larchmt) 2010, 19, 491-497.
171. Gibbs, R. B. Estrogen therapy and cognition: a review of the cholinergic hypothesis. Endocr. Rev. 2010, 31, 224-53.
172. Smith, D. C.; Prentice, R.; Thompson, D. J.; Herrmann, W. L. Association of exogenous estrogen and endometrial carcinoma. N. Engl. J. Med. 1975, 293, 1164-1167.
173. Chesler, E. J.; Juraska, J. M. Acute administration of estrogen and progesterone impairs the acquisition of the spatial Morris water maze in ovariectomized rats. Horm. Behav. 2000, 38, 234-242.
174. Brett, M.; Baxendale, S. Motherhood and memory: A review. Psychoneuroendocrinology 2001, 26, 339-362.
175. Freeman, E. W.; Weinstock, L.; Rickels, K.; Sondheimer, S. J.; Coutifaris, C. A placebocontrolled study of effects of oral progesterone on performance and mood. Br. J. Clin. Pharmacol. 1992, 33, 293-298.
176. Lu, K. H.; Hopper, B. R.; Vargo, T. M.; Yen, S. S. Chronological changes in sex steroid, gonadotropin and prolactin secretions in aging female rats displaying different reproductive states. Biol. Reprod. 1979, 21, 193-203.
177. Huang, H. H.; Steger, R. W.; Bruni, J. F.; Meites, J. Patterns of sex steroid and gonadotropin secretion in aging female rats. Endocrinology 1978, 103, 1855-1859.
178. Wise, P. M.; Ratner, A. Effect of ovariectomy on plasma LH, FSH, estradiol, and progesterone and medial basal hypothalamic LHRH concentrations old and young rats. Neuroendocrinology 1980, 30, 15-19.
179. Warren, S. G.; Juraska, J. M. Sex differences and estropausal phase effects on water maze performance in aged rats. Neurobiol. Learn. Memory 2000, 74, 229-240.
180. Warren, S. G.; Juraska, J. M. Spatial and nonspatial learning across the rat estrous cycle. Behav. Neurosci. 1997, 111, 259-266.
181. Berry, B.; McMahan, R.; Gallagher, M. Spatial learning and memory at defined points of the estrous cycle: Effects on performance of a hippocampal-dependent task. Behav. Neurosci. 1997, 111, 267-274.
182. Stackman, R. W.; Blasberg, M. E.; Langan, C. J.; Clark, A. S. Stability of spatial working memory across the estrous cycle of Long-Evans rats. Neurobiol. Learn. Memory 1997, 67, 167-171.
183. Harburger, L. L.; Bennett, J. C.; Frick, K. M. Effects of estrogen and progesterone on spatial memory consolidation in aged females. Neurobiol. Aging 2007, 28, 602-610.
184. Bimonte-Nelson, H. A.; Nelson, M. E.; Granholm, A. C. Progesterone counteracts estrogeninduced increases in neurotrophins in the aged female rat brain. Neuroreport 2004, 15, 2659-2663.
185. Aguirre, C. C.; Baudry, M. Progesterone reverses 17beta-estradiol- mediated neuroprotection and BDNF induction in cultured hippocampal slices. Eur. J. Neurosci. 2009, 29, 447-454.
186. Nilsen, J.; Brinton, R. D. Impact of progestins on estrogen-induced neuroprotection: synergy by progesterone and 19-norprogesterone and antagonism by medroxyprogesterone acetate. Endocrinology 2002, 143, 205-212.
187. Gabriel, A.; Fahim, G. Do Depot Medroxyprogesterone Acetate Contraceptive Injections Cause Mood Changes and Memory Impairment? Prim. Psychiatr. 2005, 12, 59-60.
188. Ziel, H. K.; Finkle, W. D. Increased risk of endometrial carcinoma among users of conjugated estrogens. N. Engl. J. Med. 1975, 293, 1167-1170.
189. Prokai, L.; Prokai-Tatrai, K.; Perjesi, P.; Zharikova, A. D.; Perez, E. J.; Liu, R.; Simpkins, J. W. Quinol-based cyclic antioxidant mechanism in estrogen neuroprotection. Proc. Nat. Acad. Sci. USA 2003, 100, 11741-11746.
190. Tan, R. S. Memory loss as a reported symptom of andropause. Arch. Androl. 2001, 47, 185-189.
191. Davidson, J. M.; Chen, J. J.; Crapo, L.; Gray, G. D.; Greenleaf, W. J.; Catania, J. A. Hormonal changes and sexual function in aging men. J. Clin. Endocrinol. Metab. 1983, 57, 71-77.
192. Hijazi, R. A.; Cunningham, G. R. Andropause: is androgen replacement therapy indicated for the aging male? Annu. Rev. Med. 2005, 56, 117-137.
193. Hogervorst, E.; Williams, J.; Budge, M.; Barnetson, L.; Combrinck, M.; Smith, A. D. Serum total testosterone is lower in men with Alzheimer's disease. Neurol. Endocrinol. Lett. 2001, 22, 163-168.
194. Moffat, S. D.; Zonderman, A. B.; Metter, E. J.; Blackman, M. R.; Harman, S. M.; Resnick, S. M. Longitudinal assessment of serum free testosterone concentration predicts memory performance and cognitive status in elderly men. J. Clin. Endocrinol. Metab. 2002, 87, 5001-5007.
195. Moffat, S. D.; Zonderman, A. B.; Metter, E. J.; Kawas, C.; Blackman, M. R.; Harman, S. M.; Resnick, S. M. Free testosterone and risk for Alzheimer disease in older men. Neurology 2004, 62, 188-193.
196. Rosario, E. R.; Chang, L.; Stanczyk, F. Z.; Pike, C. J. Age-related testosterone depletion and the development of Alzheimer disease. J. Am. Med. Assoc. 2004, 292, 1431-1432.
197. Kimura, D.; Hampson, E. Cognitive pattern in men and women is influenced by fluctuations in sex hormones. Curr. Dir. Psychol. Sci. 1994, 3, 57-61.
198. Neave, N.; Menaged, M.; Weightman, D. R. Sex differences in cognition: the role of testosterone and sexual orientation. Brain Cogn. 1999, 41, 245-262.
199. Silverman, I.; Kastuk, D.; Choi, J.; Phillips, K. Testosterone levels and spatial ability in men. Psychoneuroendocrinology 1999, 24, 813-822.
200. Barrett-Connor, E.; Goodman-Gruen, D.; Patay, B. Endogenous sex hormones and cognitive function in older men. J. Clin. Endocr. Metab. 1999, 84, 3681-3685. (Pubitemid 30645225)
201. Yaffe, K.; Lui, L. Y.; Zmuda, J.; Cauley, J. Sex hormones and cognitive function in older men. J. Am. Geriatr. Soc. 2002, 50, 707-712.
202. Gouchie, C.; Kimura, D. The relationship between testosterone levels and cognitive ability patterns. Psychoneuroendocrinology 1991, 16, 323-334.
203. Cherrier, M. M.; Matsumoto, A. M.; Amory, J. K.; Johnson, M.; Craft, S.; Peskind, E. R.; Raskind, M. A. Characterization of verbal and spatial memory changes from moderate to supraphysiological increases in serum testosterone in healthy older men. Psychoneuroendocrinology 2007, 32, 72-79.
204. Martin, D. M.; Wittert, G.; Burns, N. R.; McPherson, J. Endogenous testosterone levels, mental rotation performance, and constituent abilities in middle-to-older aged men. Horm. Behav. 2008, 53, 431-441.
205. Lacreuse, A.; Chiavetta, M. R.; Shirai, A. A.; Meyer, J. S.; Grow, D. R. Effects of testosterone on cognition in young adult male rhesus monkeys. Physiol. Behav. 2009, 98, 524-531.
206. Cherrier, M. M.; Asthana, S.; Plymate, S.; Baker, L.; Matsumoto, A. M.; Peskind, E.; Raskind, M. A.; Brodkin, K.; Bremner, W.; Petrova, A.; La Tendresse, S.; Craft, S. Testosterone supplementation improves spatial and verbal memory in healthy older men. Neurology 2001, 57, 80-88.
207. Gray, P. B.; Singh, A. B.; Woodhouse, L. J.; Storer, T. W.; Casaburi, R.; Dzekov, J.; Dzekov, C.; Sinha-Hikim, I.; Bhasin, S. Dose-dependent effects of testosterone on sexual function, mood, and visuospatial cognition in older men. J. Clin. Endocrinol. Metab. 2005, 90, 3838-3846.
208. Janowsky, J. S.; Oviatt, S. K.; Orwoll, E. S. Testosterone influences spatial cognition in older men. Behav. Neurosci. 1994, 108, 325-332.
209. Bhasin, S.; Woodhouse, L.; Casaburi, R.; Singh, A. B.; Bhasin, D.; Berman, N.; Chen, X.; Yarasheski, K. E.; Magliano, L.; Dzekov, C.; Dzekov, J.; Bross, R.; Phillips, J.; Sinha-Hikim, I.; Shen, R.; Storer, T. W. Testosterone dose-response relationships in healthy young men. Amer. J. Physiol., Endocrinol. Metab. 2001, 281, E1172-E1181.
210. Cherrier, M. M.; Matsumoto, A. M.; Amory, J. K.; Ahmed, S.; Bremner, W.; Peskind, E. R.; Raskind, M. A.; Johnson, M.; Craft, S. The role of aromatization in testosterone supplementation: effects on cognition in older men. Neurology 2005, 64, 290-296.
211. Tan, R. S.; Pu, S. J., A pilot study on the effects of testosterone in hypogonadal aging male patients with Alzheimer's disease. Aging Male 2003, 6, 13-17.
212. Kenny, A. M.; Fabregas, G.; Song, C.; Biskup, B.; Bellantonio, S. Effects of testosterone on behavior, depression, and cognitive function in older men with mild cognitive loss. J. Gerontol. Biol. Sci. Med. Sci. 2004, 59, 75-78.
213. Becker, K. Principles and Practice of Endocrinology and Metabolism; J. B. Lippincott Co.,: Philadelphia, PA, USA, 1995.
214. Naftolin, F. Brain aromatization of androgens. J. Reprod. Med. 1994, 39, 257-261.
215. Bimonte-Nelson, H. A.; Singleton, R. S.; Nelson, M. E.; Eckman, C. B.; Barber, J.; Scott, T. Y.; Granholm, A. C. Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Exp. Neurol. 2003, 181, 301-312.
216. Benice, T. S.; Raber, J. Testosterone and dihydrotestosterone differentially improve cognition in aged female mice. Learn. Memory 2009, 16, 479-485.
217. Lukacs, H.; Hiatt, E. S.; Lei, Z. M.; Rao, C. V. Peripheral and intracerebroventricular administration of human chorionic gonadotropin alters several hippocampus-associated behaviors in cycling female rats. Horm. Behav. 1995, 29, 42-58.
218. Chu, C.; Gao, G.; Huang, W. A study on co-localization of FSH and its receptor in rat hippocampus. J. Mol. Histol. 2008, 39, 49-55.
219. Webber, K. M.; Casadesus, G.; Bowen, R. L.; Perry, G.; Smith, M. A. Evidence for the role of luteinizing hormone in Alzheimer disease. Endocr. Metab. Immun. Disord. Drug Target. 2007, 7, 300-303.
220. Hyde, Z.; Flicker, L.; Almeida, O. P.; McCaul, K. A.; Jamrozik, K.; Hankey, G. J.; Chubb, S. A.; Yeap, B. B. Higher luteinizing hormone is associated with poor memory recall: the health in men study. J. Alzheimers Dis. 2010, 19, 943-951.
221. Webber, K. M.; Perry, G.; Smith, M. A.; Casadesus, G. The contribution of luteinizing hormone to Alzheimer disease pathogenesis. Clin. Med. Res. 2007, 5, 177-183.
222. Lei, Z. M.; Rao, C. V.; Kornyei, J. L.; Licht, P.; Hiatt, E. S. Novel expression of human chorionic gonadotropin/luteinizing hormone receptor gene in brain. Endocrinology 1993, 132, 2262-2270.
223. Zhang, W.; Lei, Z. M.; Rao, C. V. Immortalized hippocampal cells contain functional luteinizing hormone/human chorionic gonadotropin receptors. Life Sci. 1999, 65, 2083-2098.
224. Martinez-Morales, J. R.; Lopez-Coviella, I.; Hernandez-Jimenez, J. G.; Reyes, R.; Bello, A. R.; Hernandez, G.; Blusztajn, J. K.; Alonso, R. Sex steroids modulate luteinizing hormone-releasing hormone secretion in a cholinergic cell line from the basal forebrain. Neuroscience 2001, 103, 1025-1031.
225. Nauton, P.; Giry, N.; Bruhat, M. A.; Alliot, J. Effect of administration of an analog of LHRH on appetitive learning in young and middle-aged female rats. Pharmacol. Biochem. Behav. 1992, 43, 1005-1013.
226. Alliot, J.; Nauton, P.; Bruhat, M. A. Administration of LHRH analog can improve working memory in aged female rats. Psychoneuroendocrinology 1993, 18, 543-550.
227. Bowen, R. L.; Verdile, G.; Liu, T.; Parlow, A. F.; Perry, G.; Smith, M. A.; Martins, R. N.; Atwood, C. S. Luteinizing hormone, a reproductive regulator that modulates the processing of amyloidbeta precursor protein and amyloid-beta deposition. J. Biol. Chem. 2004, 279, 20539-20545.
228. Casadesus, G.; Webber, K. M.; Atwood, C. S.; Pappolla, M. A.; Perry, G.; Bowen, R. L.; Smith, M. A. Luteinizing hormone modulates cognition and amyloid-beta deposition in Alzheimer APP transgenic mice. Biochem. Biophys. Acta 2006, 1762, 447-452.
229. Casadesus, G.; Milliken, E. L.; Webber, K. M.; Bowen, R. L.; Lei, Z.; Rao, C. V.; Perry, G.; Keri, R. A.; Smith, M. A. Increases in luteinizing hormone are associated with declines in cognitive performance. Mol. Cell. Biochem. 2007, 269, 107-111.
230. Short, R. A.; Bowen, R. L.; O'Brien, P. C.; Graff-Radford, N. R. Elevated gonadotropin levels in patients with Alzheimer disease. Mayo Clin. Proc. 2001, 76, 906-909.
231. McEwen, B. S.; Coirini, H.; Westlind-Danielsson, A.; Frankfurt, M.; Gould, E.; Schumacher, M.; Woolley, C. Steroid hormones as mediators of neural plasticity. J. Steroid Biochem. Mol. Biol. 1991, 39, 223-232.
232. McEwen, B. S. Multiple ovarian hormone effects on brain structure and function. J. Gend. Specif. Med. 1998, 1, 33-41.
233. Moffat, S. D. Effects of testosterone on cognitive and brain aging in elderly men. Ann. N Y Acad. Sci. 2005, 1055, 80-92.
234. Genazzani, A. R.; Pluchino, N.; Luisi, S.; Luisi, M. Estrogen, cognition and female ageing. Hum. Reprod. Update 2007, 13, 175-187.
235. Brody, H. Organization of the cerebral cortex. III. A study of aging in the human cerebral cortex. J. Comp. Neurol. 1955, 102, 511-516.
236. Simic, G.; Kostovic, I.; Winblad, B.; Bogdanovic, N. Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J. Comp. Neurol. 1997, 379, 482-494.
237. West, M. J. Regionally specific loss of neurons in the aging human hippocampus. Neurobiol. Aging 1993, 14, 287-293.
238. Smith, D. E.; Rapp, P. R.; McKay, H. M.; Roberts, J. A.; Tuszynski, M. H. Memory impairment in aged primates is associated with focal death of cortical neurons and atrophy of subcortical neurons. J. Neurosci. 2004, 24, 4373-4381.
239. Funahashi, S.; Bruce, C. J.; Goldman-Rakic, P. S. Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas". J. Neurosci. 1993, 13, 1479-1497.
240. Quintana, J.; Fuster, J. M. From perception to action: temporal integrative functions of prefrontal and parietal neurons. Cereb. Cortex 1999, 9, 213-221.
241. Levy, R.; Goldman-Rakic, P. S. Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp. Brain Res. 2000, 133, 23-32.
242. Rowe, J. B.; Toni, I.; Josephs, O.; Frackowiak, R. S.; Passingham, R. E. The prefrontal cortex: response selection or maintenance within working memory? Science 2000, 288, 1656-1660.
243. Fuster, J. M. Frontal lobe and cognitive development. J. Neurocytol. 2002, 31, 373-385.
244. Rapp, P. R.; Deroche, P. S.; Mao, Y.; Burwell, R. D. Neuron number in the parahippocampal region is preserved in aged rats with spatial learning deficits. Cereb. Cortex 2002, 12, 1171-1179.
245. Kaplan, M. S.; Hinds, J. W. Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs. Science 1977, 197, 1092-1094.
246. Eriksson, P. S.; Perfilieva, E.; Bjork-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.
247. Kornack, D. R.; Rakic, P. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Nat. Acad. Sci. USA 1999, 96, 5768-5773.
248. Bertoni-Freddari, C.; Fattoretti, P.; Solazzi, M.; Giorgetti, B.; Di Stefano, G.; Casoli, T.; Meier-Ruge, W. Neuronal death versus synaptic pathology in Alzheimer's disease. Ann. NY Acad. Sci. 2003, 1010, 635-638.
249. Esiri, M. The neuropathology of Alzheimer's disease. In Neurobiology of Alzheimer's Disease, 2nd ed.; Dawbarn, D., Allen, S., Eds.; Oxford University Press: New York, NY, USA, 2001.
250. Poucet, B. A further characterization of the spatial problem-solving deficit induced by lesions of the medial frontal cortex in the rat. Behav. Brain Res. 1990, 41, 229-237.
251. Poucet, B.; Herrmann, T. Septum and medial frontal cortex contribution to spatial problemsolving. Behav. Brain Res. 1990, 37, 269-280.
252. Miotto, E. C.; Bullock, P.; Polkey, C. E.; Morris, R. G. Spatial working memory and strategy formation in patients with frontal lobe excisions. Cortex 1996, 32, 613-630.
253. Ranganath, C.; Johnson, M. K.; D'Esposito, M. Prefrontal activity associated with working memory and episodic long-term memory. Neuropsychologia 2003, 41, 378-389. (Pubitemid 35365964)
254. Woolley, C. S. Acute effects of estrogen on neuronal physiology. Annu. Rev. Pharmacol. Toxicol. 2007, 47, 657-680.
255. McEwen, B. S. Neural gonadal steroid actions. Science 1981, 211, 1303-1311.
256. Parsons, B.; McEwen, B. S.; Pfaff, D. W. A discontinuous schedule of estradiol treatment is sufficient to activate progesterone-facilitated feminine sexual behavior and to increase cytosol receptors for progestins in the hypothalamus of the rat. Endocrinology 1982, 110, 613-619.
257. Pfaff, D. W.; McEwen, B. S. Actions of estrogens and progestins on nerve cells. Science 1983, 219, 808-814.
258. Terasawa, E.; Timiras, P. S. Electrical activity during the estrous cycle of the rat: cyclic changes in limbic structures. Endocrinology 1968, 83, 207-216.
259. Foy, M. R. 17β-estradiol: effect on CA1 hippocampal synaptic plasticity. Neurobiol. Learn. Memory 2001, 76, 239-252.
260. Gould, E.; Woolley, C. S.; Frankfurt, M.; McEwen, B. S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 1990, 10, 1286-1291.
261. Silva, I.; Mello, L. E.; Freymuller, E.; Haidar, M. A.; Baracat, E. C. Estrogen, progestogen and tamoxifen increase synaptic density of the hippocampus of ovariectomized rats. Neurosci. Lett. 2000, 291, 183-186.
262. Woolley, C. S.; McEwen, B. S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 1992, 12, 2549-2554.
263. Woolley, C. S.; McEwen, B. S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 1993, 336, 293-306.
264. MacLusky, N. J.; Hajszan, T.; Prange-Kiel, J.; Leranth, C. Androgen modulation of hippocampal synaptic plasticity. Neuroscience 2006, 138, 957-965.
265. Moser, M. B. Making more synapses: a way to store information? Cell. Mol. Life Sci. 1999, 55, 593-600.
266. Geinisman, Y. Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb. Cortex 2000, 10, 952-962.
267. Sorra, K. E.; Harris, K. M. Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 2000, 10, 501-511.
268. Nimchinsky, E. A.; Sabatini, B. L.; Svoboda, K. Structure and function of dendritic spines. Annu. Rev. Physiol. 2002, 64, 313-353.
269. Kasai, H.; Matsuzaki, M.; Noguchi, J.; Yasumatsu, N.; Nakahara, H. Structure-stability-function relationships of dendritic spines. Trends Neurosci. 2003, 26, 360-368.
270. Sandstrom, N. J.; Williams, C. L. Spatial memory retention is enhanced by acute and continuous estradiol replacement. Horm. Behav. 2004, 45, 128-135.
271. Jones, M. W. A comparative review of rodent prefrontal cortex and working memory. Curr. Mol. Med. 2002, 2, 639-647.
272. Fader, A. J.; Johnson, P. E.; Dohanich, G. P. Estrogen improves working but not reference memory and prevents amnestic effects of scopolamine of a radial-arm maze. Pharmacol. Biochem. Behav. 1999, 62, 711-717.
273. Hruska, Z.; Dohanich, G. P. The effects of chronic estradiol treatment on working memory deficits induced by combined infusion of beta-amyloid (1-42) and ibotenic acid. Horm. Behav 2007, 52, 297-306.
274. Luine, V. N. Steroid hormone influences on spatial memory. Ann. NY Acad. Sci. 1994, 743, 201-211.
275. Lacreuse, A.; Verreault, M.; Herndon, J. G. Fluctuations in spatial recognition memory across the menstrual cycle in female rhesus monkeys. Psychoneuroendocrinology 2001, 26, 623-639.
276. Hao, J.; Janssen, W. G.; Tang, Y.; 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 increases the number of spinophilin-immunoreactive spines in the hippocampus of young and aged female rhesus monkeys. J. Comp. Neurol. 2003, 465, 540-550.
277. 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.
278. 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.
279. Gibbs, R. B. Basal forebrain cholinergic neurons are necessary for estrogen to enhance acquisition of a delayed matching-to-position T-maze task. Horm. Behav. 2002, 42, 245-257.
280. Gibbs, R. B. Estradiol enhances DMP acquisition via a mechanism not mediated by turning strategy but which requires intact basal forebrain cholinergic projections. Horm. Behav. 2007, 52, 352-359.
281. Singer, C. A.; McMillan, P. J.; Dobie, D. J.; Dorsa, D. M. Effects of estrogen replacement on choline acetyltransferase and trkA mRNA expression in the basal forebrain of aged rats. Brain Res. 1998, 789, 343-346.
282. Kompoliti, K.; Chu, Y.; Polish, A.; Roberts, J.; McKay, H.; Mufson, E. J.; Leurgans, S.; Morrison, J. H.; Kordower, J. H. Effects of estrogen replacement therapy on cholinergic basal forebrain neurons and cortical cholinergic innervation in young and aged ovariectomized rhesus monkeys. J. Comp. Neurol. 2004, 472, 193-207.
283. O'Malley, C. A.; Hautamaki, R. D.; Kelley, M.; Meyer, E. M. Effects of ovariectomy and estradiol benzoate on high affinity choline uptake, ACh synthesis, and release from rat cerebral cortical synaptosomes. Brain Res. 1987, 403, 389-92.
284. Luine, V. N.; McEwen, B. S. Sex differences in cholinergic enzymes of diagonal band nuclei in the rat preoptic area. Neuroendocrinology 1983, 36, 475-482.
285. Luine, V. N. Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp. Neurol. 1985, 89, 484-490.
286. McMillan, P. J.; Singer, C. A.; Dorsa, D. M. The effects of ovariectomy and estrogen replacement on trkA and choline acetyltransferase mRNA expression in the basal forebrain of the adult female Sprague-Dawley rat. J. Neurosci. 1996, 16, 1860-1865.
287. Gibbs, R. B.; Wu, D.; Hersh, L. B.; Pfaff, D. W. Effects of estrogen replacement on the relative levels of choline acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Exp. Neurol. 1994, 129, 70-80.
288. Gibbs, R. B.; Pfaff, D. W. Effects of estrogen and fimbria/fornix transection on p75NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp. Neurol. 1992, 116, 23-39.
289. Gibbs, R. B. Effects of estrogen on basal forebrain cholinergic neurons vary as a function of dose and duration of treatment. Brain Res. 1997, 757, 10-16.
290. Granholm, A. C.; Ford, K. A.; Hyde, L. A.; Bimonte, H. A.; Hunter, C. L.; Nelson, M.; Albeck, D.; Sanders, L. A.; Mufson, E. J.; Crnic, L. S. Estrogen restores cognition and cholinergic phenotype in an animal model of Down syndrome. Physiol. Behav. 2002, 77, 371-385.
291. Gibbs, R. B. Fluctuations in relative levels of choline acetyltransferase mRNA in different regions of the rat basal forebrain across the estrous cycle: effects of estrogen and progesterone. J. Neurosci. 1996, 16, 1049-1055.
292. Gibbs, R. B.; Nelson, D.; Anthony, M. S.; Clarkson, T. B. Effects of long-term hormone replacement and of tibolone on choline acetyltransferase and acetylcholinesterase activities in the brains of ovariectomized, cynomologus monkeys. Neuroscience 2002, 113, 907-914.
293. 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.
294. Tinkler, G. P.; Tobin, J. R.; Voytko, M. L. Effects of two years of estrogen loss or replacement on nucleus basalis cholinergic neurons and cholinergic fibers to the dorsolateral prefrontal and inferior parietal cortex of monkeys. J. Comp. Neurol. 2004, 469, 507-521.
295. Blaustein, J. D. Estrogen receptor immunoreactivity in rat brain: rapid effects of estradiol injection. Endocrinology 1993, 132, 1218-1224.
296. Kassis, J. A.; Gorski, J. Estrogen receptor replenishment. Evidence for receptor recycling. J. Biol. Chem. 1981, 256, 7378-7382. (Pubitemid 11021814)
297. Rosser, M.; Chorich, L.; Howard, E.; Zamorano, P.; Mahesh, V. B. Changes in rat uterine estrogen receptor messenger ribonucleic acid levels during estrogen- and progesterone-induced estrogen receptor depletion and subsequent replenishment. Biol. Reprod. 1993, 48, 89-98.
298. Gibbs, R. B. Effects of gonadal hormone replacement on measures of basal forebrain cholinergic function. Neuroscience 2000, 101, 931-938.
299. Nakamura, N.; Fujita, H.; Kawata, M. Effects of gonadectomy on immunoreactivity for choline acetyltransferase in the cortex, hippocampus, and basal forebrain of adult male rats. Neuroscience 2002, 109, 473-485.
300. Romeo, R. D.; Staub, D.; Jasnow, A. M.; Karatsoreos, I. N.; Thornton, J. E.; McEwen, B. S. Dihydrotestosterone increases hippocampal N-methyl-D-aspartate binding but does not affect choline acetyltransferase cell number in the forebrain or choline transporter levels in the CA1 region of adult male rats. Endocrinology 2005, 146, 2091-2097.
301. Chakraborty, T. R.; Gore, A. C. Aging-related changes in ovarian hormones, their receptors, and neuroendocrine function. Exp. Biol. Med. (Maywood) 2004, 229, 977-987.
302. Beato, M.; Chavez, S.; Truss, M. Transcriptional regulation by steroid hormones. Steroids 1996, 61, 240-251.
303. Toran-Allerand, C. D. Estrogen and the brain: beyond ER-alpha, ER-beta, and 17beta-estradiol. Ann. NY Acad. Sci. 2005, 1052, 136-144.
304. Prossnitz, E. R.; Arterburn, J. B.; Smith, H. O.; Oprea, T. I.; Sklar, L. A.; Hathaway, H. J. Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annu. Rev. Physiol. 2008, 70, 165-190.
305. 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.
306. Prokai, L.; Simpkins, J. W. Structure-nongenomic neuroprotection relationship of estrogens and estrogen-derived compounds. Pharmacol. Ther. 2007, 114, 1-12.
307. Vasudevan, N.; Pfaff, D. W. Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front Neuroendocrinol. 2008, 29, 238-257.
308. Brinton, R. D.; Tran, J.; Proffitt, P.; Montoya, M. 17 beta-Estradiol enhances the outgrowth and survival of neocortical neurons in culture. Neurochem. Res. 1997, 22, 1339-1351.
309. 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.
310. 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, S35-S52.
311. Littleton-Kearney, M. T.; Klaus, J. A.; Hurn, P. D. Effects of combined oral conjugated estrogens and medroxyprogesterone acetate on brain infarction size after experimental stroke in rat. J. Cereb. Blood Flow Metab. 2005, 25, 421-426.
312. 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.
313. Zemlyak, I.; Brooke, S. M.; Sapolsky, R. M. Protection against gp120-induced neurotoxicity by an array of estrogenic steroids. Brain Res. 2002, 958, 272-276.
314. Brinton, R. D.; Proffitt, P.; Tran, J.; Luu, R. Equilin, a principal component of the estrogen replacement therapy premarin, increases the growth of cortical neurons via an NMDA receptordependent mechanism. Exp. Neurol. 1997, 147, 211-220.
315. Nilsen, J.; Morales, A.; Brinton, R. D. Medroxyprogesterone acetate exacerbates glutamate excitotoxicity. Gynecol. Endocrinol. 2006, 22, 355-361.
316. Hammond, J.; Le, Q.; Goodyer, C.; Gelfand, M.; Trifiro, M.; Le Blanc, A. Testosterone-mediated neuroprotection through the androgen receptor in human primary neurons. J. Neurochem. 2001, 77, 1319-1326.
317. Zhang, Y.; Champagne, N.; Beitel, L. K.; Goodyer, C. G.; Trifiro, M.; Le Blanc, A. Estrogen and androgen protection of human neurons against intracellular amyloid beta1-42 toxicity through heat shock protein 70. J. Neurosci. 2004, 24, 5315-5321.
318. Nguyen, T. V.; Yao, M.; Pike, C. J. Androgens activate mitogen-activated protein kinase signaling: role in neuroprotection. J. Neurochem. 2005, 94, 1639-1651.
319. Chisu, V.; Manca, P.; Lepore, G.; Gadau, S.; Zedda, M.; Farina, V. Testosterone induces neuroprotection from oxidative stress. Effects on catalase activity and 3-nitro-L-tyrosine incorporation into alpha-tubulin in a mouse neuroblastoma cell line. Arch. Ital. Biol. 2006, 144, 63-73.
320. Azcoitia, I.; Sierra, A.; Veiga, S.; Honda, S.; Harada, N.; Garcia-Segura, L. M. Brain aromatase is neuroprotective. J. Neurobiol. 2001, 47, 318-329.
321. Veiga, S.; Garcia-Segura, L. M.; Azcoitia, I. Neuroprotection by the steroids pregnenolone and dehydroepiandrosterone is mediated by the enzyme aromatase. J. Neurobiol. 2003, 56, 398-406.
322. Bimonte-Nelson, H. A.; Granholm, A. C.; Nelson, M. E.; Moore, A. B. Patterns of neurotrophin protein levels in male and female Fischer 344 rats from adulthood to senescence: how young is "young" and how old is "old"? Exp. Aging Res. 2008, 34, 13-26.
323. Hall, J.; Thomas, K. L.; Everitt, B. J. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat. Neurosci. 2000, 3, 533-535.
324. Granholm, A. C. Oestrogen and nerve growth factor - neuroprotection and repair in Alzheimer's disease. Expert Opin. Investig. Drugs 2000, 9, 685-694.
325. Kesslak, J. P.; So, V.; Choi, J.; Cotman, C. W.; Gomez-Pinilla, F. Learning upregulates brainderived neurotrophic factor messenger ribonucleic acid: a mechanism to facilitate encoding and circuit maintenance? Behav. Neurosci. 1998, 112, 1012-1019.
326. Siegel, G. J.; Chauhan, N. B. Neurotrophic factors in Alzheimer's and Parkinson's disease brain. Brain Res. Brain Res. Rev. 2000, 33, 199-227.
327. Levi-Montalcini, R. The nerve growth factor 35 years later. Science 1987, 237, 1154-1162.
328. Woolf, N. J. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 1991, 37, 475-524.
329. Gibbs, R. B. Levels of trkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement. Brain Res. 1998, 810, 294.
330. Pan, Y.; Anthony, M.; Clarkson, T. B. Effect of estradiol and soy phytoestrogens on choline acetyltransferase and nerve growth factor mRNAs in the frontal cortex and hippocampus of female rats. Proc. Soc. Exp. Biol. Med. 1999, 221, 118-125.
331. Hafting, T.; Fyhn, M.; Molden, S.; Moser, M. B.; Moser, E. I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436, 801-806.
332. Katoh-Semba, R.; Semba, R.; Kato, H.; Ueno, M.; Arakawa, Y.; Kato, K. Regulation by androgen of levels of the beta subunit of nerve growth factor and its mRNA in selected regions of the mouse brain. J. Neurochem. 1994, 62, 2141-2147.
333. Tirassa, P.; Thiblin, I.; Agren, G.; Vigneti, E.; Aloe, L.; Stenfors, C. High-dose anabolic androgenic steroids modulate concentrations of nerve growth factor and expression of its low affinity receptor (p75-NGFr) in male rat brain. J. Neurosci. Res. 1997, 47, 198-207.
334. Ottem, E. N.; Beck, L. A.; Jordan, C. L.; Breedlove, S. M. Androgen-dependent regulation of brainderived neurotrophic factor and tyrosine kinase B in the sexually dimorphic spinal nucleus of the bulbocavernosus. Endocrinology 2007, 148, 3655-3665.
335. Gold, S. M.; Chalifoux, S.; Giesser, B. S.; Voskuhl, R. R. Immune modulation and increased neurotrophic factor production in multiple sclerosis patients treated with testosterone. J. Neuroinflamm. 2008, 5, 32.
336. Li, Z. K.; Shen, L.; Ke, H.; Li, F.; Ni, L. M.; Li, Q. H. Effects of androgen on the expression of brain aromatase cytopigment and nerve growth factor in neonatal rats with hypoxic-ischemic brain damage. Zhongguo Dang Dai Er Ke Za Zhi 2008, 10, 441-446.
337. Eckerman, D. A.; Gordon, W. A.; Edwards, J. D.; MacPhail, R. C.; Gage, M. I. Effects of scopolamine, pentobarbital, and amphetamine on radial arm maze performance in the rat. Pharmacol. Biochem. Behav. 1980, 12, 595-602.
338. Rupniak, N. M.; Field, M. J.; Samson, N. A.; Steventon, M. J.; Iversen, S. D. Direct comparison of cognitive facilitation by physostigmine and tetrahydroaminoacridine in two primate models. Neurobiol. Aging 1990, 11, 609-613.
339. Drachman, D. A.; Leavitt, J. Human memory and the cholinergic system. A relationship to aging? Arch. Neurol. 1974, 30, 113-121.
340. Mufson, E. J.; Conner, J. M.; Kordower, J. H. Nerve growth factor in Alzheimer's disease: defective retrograde transport to nucleus basalis. Neuroreport 1995, 6, 1063-1066.
341. Bimonte-Nelson, H. A.; Hunter, C. L.; Nelson, M. E.; Granholm, A. C. Frontal cortex BDNF levels correlate with working memory in an animal model of Down syndrome. Behav. Brain Res. 2003, 139, 47-57.
342. Almli, C. R.; Levy, T. J.; Han, B. H.; Shah, A. R.; Gidday, J. M.; Holtzman, D. M. BDNF protects against spatial memory deficits following neonatal hypoxia-ischemia. Exp. Neurol. 2000, 166, 99-114.
343. Dixon, C. E.; Flinn, P.; Bao, J.; Venya, R.; Hayes, R. L. Nerve growth factor attenuates cholinergic deficits following traumatic brain injury in rats. Exp. Neurol. 1997, 146, 479-490.
344. Backman, C.; Rose, G. M.; Hoffer, B. J.; Henry, M. A.; Bartus, R. T.; Friden, P.; Granholm, A. C. Systemic administration of a nerve growth factor conjugate reverses age-related cognitive dysfunction and prevents cholinergic neuron atrophy. J. Neurosci. 1996, 16, 5437-5442.
345. Fischer, W.; Wictorin, K.; Bjorklund, A.; Williams, L. R.; Varon, S.; Gage, F. H. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 1987, 329, 65-68.
346. Gustilo, M. C.; Markowska, A. L.; Breckler, S. J.; Fleischman, C. A.; Price, D. L.; Koliatsos, V. E. Evidence that nerve growth factor influences recent memory through structural changes in septohippocampal cholinergic neurons. J. Comp. Neurol. 1999, 405, 491-507.
347. Markowska, A. L.; Koliatsos, V. E.; Breckler, S. J.; Price, D. L.; Olton, D. S. Human nerve growth factor improves spatial memory in aged but not in young rats. J. Neurosci. 1994, 14, 4815-4824.
348. Scali, C.; Casamenti, F.; Pazzagli, M.; Bartolini, L.; Pepeu, G. Nerve growth factor increases extracellular acetylcholine levels in the parietal cortex and hippocampus of aged rats and restores object recognition. Neurosci. Lett. 1994, 170, 117-120.
349. Smith, Y. R.; Love, T.; Persad, C. C.; Tkaczyk, A.; Nichols, T. E.; Zubieta, J. K. Impact of combined estradiol and norethindrone therapy on visuospatial working memory assessed by functional magnetic resonance imaging. J. Clin. Endocrinol. Metab. 2006, 91, 4476-4481.