Estrogen and basal forebrain cholinergic neurons: Implications for brain aging and Alzheimer's disease-related cognitive decline

Hormones and Behavior

Volumn 34, Issue 2, 1998, Pages 98-111

  Gibbs, Robert B ^a   Aggarwal, Payal ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Acetylcholine; Cortex; Dementia; Gonadal hormones; Hippocampus; Learning and memory

Indexed keywords

ACETYLCHOLINE; BENZODIAZEPINE DERIVATIVE; BRAIN DERIVED NEUROTROPHIC FACTOR; CHOLINE ACETYLTRANSFERASE; ESTRADIOL; ESTROGEN; LORAZEPAM; MESSENGER RNA; MUSCARINIC RECEPTOR BLOCKING AGENT; NERVE GROWTH FACTOR; PROGESTERONE; SCOPOLAMINE; TYROSINE KINASE RECEPTOR;

AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ARTICLE; CHOLINERGIC NERVE CELL; COGNITIVE DEFECT; CONTROLLED STUDY; DEGENERATIVE DISEASE; DEMENTIA; ESTROGEN THERAPY; FEMALE; HIPPOCAMPUS; LEARNING; MALE; MEMORY; NEUROLOGIC DISEASE; NONHUMAN; OVARY FUNCTION; POSTMENOPAUSE; PRIORITY JOURNAL;

EID: 0032192013     PISSN: 0018506X     EISSN: None     Source Type: Journal    
DOI: 10.1006/hbeh.1998.1451     Document Type: Article

References (118)

1. Alkayed N. J., Harukuni I., Kimes A. S., London E. D., Traystman R. J., Hurn P. D. Gender-linked brain injury in experimental stroke. Stroke. 29:1998;159-166.
2. Applebaum-Bowden D., McLean P., Steinmetz A. Lipoprotein, apolipoprotein, and lipolytic enzyme changes following estrogen administration in postmenopausal women. J. Lipid Res. 30:1989;1895-1906.
3. Bartus R. T., Dean R. L., Beer B. An evaluation of drugs for improving memory in aged monkeys: Implications for clinical trials in humans. Psychopharmacol. Bull. 10:1983;168-184.
4. Bauer J., Ganter U., Strauss S. The participation of interleukin-6 in the pathogenesis of Alzheimer's disease. Res. Immunol. 143:1992;650-657.
5. Behl C., Skutella T., Lezoualch F., Post A., Widmann M., Newton C. J., Holsboer F. Neuroprotection against oxidative stress by estrogens - Structure-activity relationship. Mol. Pharmacol. 51:1997;535-541.
6. Belfort M. A., Saade G. R., Snabes M. Hormonal status affects the reactivity of the cerebral vasculature. Am. J. Obstet. Gynecol. 172:1995;1273-1278.
7. Benedetti M., Levi A., Chao M. V. Differential expression of nerve growth factor receptors leads to altered binding affinity and neurotrophin responsiveness. Proc. Natl. Acad. Sci. USA. 90:1993;7859-7863.
8. Bishop J., Simpkins J. W. Role of estrogens in peripheral and cerebral glucose utilization. Rev. Neurosci. 3:1992;121-137.
9. Chao M. V., Hempstead B. L. p75 and Trk: A two-receptor system. Trends Neurosci. 18:1995;321-326.
10. Chapman B. S. A region of the 75 kDa neurotrophin receptor homologous to the death domains of TNFR-I and Fas. FEBS Lett. 374:1995;216-220.
11. Chrobak J. J., Hanin I., Schmechel D. E., Walsh T. J. AF64A-induced working memory impairment: Behavioral, neurochemical and histological correlates. Brain Res. 463:1988;107-117.
12. Courtney M. J., Åkerman K. E. O., Coffey E. T. Neurotrophins protect cultured cerebellar granule neurons against the early phase of cell death by a two-component mechanism. J. Neurosci. 17:1997;4201-4211.
13. 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. 32:1998;217-225.
14. Davies A. M., Lee K.-F., Jaenisch R. p75-deficient trigeminal sensory neurons have an altered response to NGF but not to other neurotrophins. Neuron. 11:1993;565-574.
15. Dekker J. A. M., Connor D. J., Thal L. J. The role of cholinergic projections from the nucleus basalis in memory. Neurosci. Biobehav. Rev. 15:1991;299-317.
16. 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. 108:1994;988-992.
17. Dornan W. A., McCampbell A. R., Tinkler G. P., Hickman L. J., Bannon A. W., Decker M. W., Gunther K. L. Comparison of site-specific injections into the basal forebrain on water maze and radial arm maze performance in the male rat after immunolesioning with 192 IgG saporin. Behav. Brain Res. 82:1996;93-101.
18. Dunnett S. B., Low W. C., Iversen S. D., Stenevi U., Björklund A. Septal transplants restore maze learning in rats with fimbria-fornix lesions. Brain Res. 251:1982;335-348.
19. Dunnett S. B., Whishaw I. Q., Jones G. H., Gunch S. T. Behavioral, biochemical and histochemical effects of different neurotoxic amino acids injected into the nucleus basalis magnocellularis of rats. Neuroscience. 20:1987;653-669.
20. Etherington R., Mittleman G., Robbins T. W. Comparative effects of nucleus basalis and fimbria-fornix lesions on delayed matching and alternation tests of memory. Neurosci. Res. Commun. 1:1987;135-143.
21. Fader A. J., Hendricson A. W., Dohanich G. P. Estrogen improves performance of reinforced T-maze alternation and prevents the amnestic effects of scopolamine administered systemically or intrahippocampally. Neurobiol. Learning Mem. 1998.
22. Fibiger H. C. Cholinergic mechanisms in learning, memory and dementia: A review of recent evidence. Trends Neurosci. 14:1991;220-223.
23. Fine A., Dunnett S. B., Björklund A., Iversen S. D. Cholinergic ventral forebrain grafts into the neocortex improve passive avoidance memory in a rat model of Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 82:1985;5227-5230.
24. Gibbs R. B. Estrogen and nerve growth factor-related systems in brain: Effects on basal forebrain cholinergic neurons and implications for learning and memory processes and aging. Hormonal Restructuring of the Adult Brain: Basic and Clinical Perspectives. 1994;New York Academy of Sciences, New York. p. 165-199.
25. Gibbs R. B. Expression of estrogen receptor-like immunoreactivity by different subgroups of basal forebrain cholinergic neurons in gonadectomized male and female rats. Brain Res. 720:1996a;61-68.
26. Gibbs R. B. Fluctuations in relative levels of choline acetyltransferase mRNA in different regions of the rat basal forebrain across the estrus cycle: Effects of estrogen and progesterone. J. Neurosci. 16:1996b;1049-1055.
27. Gibbs R. B. Effects of estrogen on basal forebrain cholinergic neurons vary as a function of dose and duration of treatment. Brain Res. 757:1997;10-16.
28. Gibbs R. B. Impairment of basal forebrain cholinergic neurons associated with aging and long-term loss of ovarian function. Exp. Neurol. 151:1998a;289-302.
29. 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. 787:1998b;259-268.
30. Gibbs R. B., Burke A. M., Johnson D. A. Estrogen replacement attenuates effects of scopolamin and lorazepam on memory acquisition and retention. Horm. Behav. 1998.
31. Gibbs R. B., Hashash A., Johnson D. A. Effects of estrogen on potassium-evoked acetylcholine release in the hippocampus and overlying cortex of adult rats. Brain Res. 749:1997;143-146.
32. NGFR. Exp. Neurol. 116:1992;23-39.
33. Gibbs R. B., Wu D.-H., Hersh L., Pfaff D. W. Effects of estrogen replacement on relative levels of ChAT, TrkA and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Exp. Neurol. 129:1994;70-80.
34. Gould E., Woolley C. S., Frankfurt M., McEwen B. S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. Neuroscience. 10:1990;1286-1291.
35. Green P. S., Bishop J., Simpkins J. W. 17-α-Estradiol exerts neuroprotective effects on SK-N-SH cells. J. Neurosci. 17:1997a;511-515.
36. Green P. S., Gordon K., Simpkins J. W. Phenolic a ring requirement for the neuroprotective effects of steroids. J. Steroid Biochem. Mol. Biol. 63:1997b;229-235.
37. Gridley K. E., Green P. S., Simpkins J. W. Low concentrations of estradiol reduce β-amyloid (25-35)-induced toxicity, lipid peroxidation and glucose utilization in human SK-N-SH neuroblastoma cells. Brain Res. 778:1997;158-165.
38. Häfner H. Epidemiology of Alzheimer's disease. Maurer K., Riederer P., Beckmann H. Alzheimer's Disease, Epidemiology, Neuropathology, Neurochemistry, and Clinics. 1990;23-39 Spring-Verlag, Berlin.
39. Hantzopoulos P. A., Suri C., Glass D. J., Goldfarb M. P., Yancopoulos G. D. The low affinity NGF receptor, p75, can collaborate with each of the Trks to potentiate functional responses to the neurotrophins. Neuron. 13:1994;187-201.
40. Henderson V. W. The epidemiology of estrogen replacement therapy and Alzheimer's disease. Neurology. 48:1997;S27-S35.
41. Henderson V. W., Watt L., Buckwalter J. G. Cognitive skills associated with estrogen replacement in women with Alzheimer's disease. Psychoneuroendocrinology. 21:1996;421-430.
42. Honjo H., Ogino Y., Tanaka K. An effect of conjugated estrogen to cognitive impairment in women with senile dementia-Alzheimer's type: A placebo-controlled double blind study. J. Jpn. Menopause Soc. 1:1993;167-171.
43. Honjo H., Tanaka K., Kashiwagi T., Urabe M., Hayashi O. M., Hayashi K. Senile dementia-Alzheimer's type and estrogen. Horm. Metab. Res. 27:1994;204-207.
44. Jaffe A. B., Toran-Allerand C. D., Greengard P., Gandy S. E. Estrogen regulates metabolism of Alzheimer amyloid β precursor protein. J. Biol. Chem. 269:1994;13065-13068.
45. Jorm A. F., Korten A. E., Henderson A. S. The prevalence of dementia: A quantitative integration of the literature. Acta Psychiatr. Scand. 76:1987;465-479.
46. Kasa P., Rakonczay Z., Gulya K. The cholinergic system in Alzheimer's disease. Prog. Neurobiol. 52:1997;511-535.
47. Kawas C., Resnick S., Morrison A., Brookmeyer R., Corrada M., Zonderman A., Bacal C., Lingle D. L., Metter E. A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: The Baltimore Longitudinal Study of Aging. Neurology. 48:1997;1517-1521.
48. ++. J. Neurosci. Res. 50:1997;522-530.
49. Koh S., Chang P., Collier T. J., Loy R. Loss of NGF receptor immunoreactivity in basal forebrain neurons of aged rats: Correlation with spatial memory impairment. Brain Res. 498:1989;397-404.
50. Koh S., Loy R. Age-related loss of nerve growth factor sensitivity in rat basal forebrain neurons. Brain Res. 440:1988;396-401.
51. Kumar V., Calache M. Treatment of Alzheimer's disease with cholinergic drugs. Int. J. Clin. Pharmacol. Ther. Toxicol. 29:1991;23-37.
52. Kushwaha R. S., Foster D. M., Barrett P. H. R., Carey K. D., Bernard M. G. Metabolic regulation of plasma apolipoprotein E by estrogen and progesterone in the baboon (Papio. Metabolism. 40:1991;93-100.
53. Lawrence A. D., Sahakian B. J. Alzheimer disease, attention, and the cholinergic system. Alzheimer Dis. Assoc. Disorders. 9:1995;43-49.
54. Leanza G., Nilsson O. G., Nikkhah G., Wiley R. G., Björklund A. Effects of neonatal lesions of the basal forebrain cholinergic system by 192 immunoglobulin G-saporin: Biochemical, behavioral and morphological characterization. Neuroscience. 74:1996;119-141.
55. Lee K.-F., Davies A. M., Jaenisch R. p75-deficient embryonic dorsal root sensory and neonatal sympathetic neurons display a decreased sensitivity to NGF. Development. 120:1994a;1027-1033.
56. Lee T. H., Abe K., Nakamura M., Kogure K., Itoyama Y. Reduction of nerve growth factor receptor immunoreactivity in ischaemic gerbil hippocampal CA1 neurons after treatment withL. Neurol. Res. 16:1994b;201-204.
57. 3. Endocrinology. 100:1977;903-910.
58. Luine V., Rodriguez M. Effects of estradiol on radial arm maze performance of young and aged rats. Behav. Neural Biol. 62:1994;230-236.
59. Luine V. N. Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp. Neurol. 89:1985;484-490.
60. Luine V. N. Steroid hormone modulation of hippocampal dependent spatial memory. Stress. 2:1997;21-36.
61. Luine V. N., Khylchevskaya R., McEwen B. S. Effect of gonadal steroids on activities of monoamine oxidase and choline acetylase in rat brain. Brain Res. 86:1975;293-306.
62. Matsuoka N., Maeda N., Ohkubo Y., Yamaguchi I. Differential effects of physostigmine and pilocarpine on the spatial memory deficits produced by two septo-hippocampal deafferentations in rats. Brain Res. 559:1991;233-240.
63. Mattson M. P., Robinson N., Guo Q. Estrogens stabilize mitochondrial function and protect neural cells against the pro-apoptotic action of mutant presenilin-1. NeuroReport. 8:1997;3817-3821.
64. McEntee W. J., Crook T. H. Cholinergic function in the aged brain: Implications for treatment of memory impairments associated with aging. Behav. Pharmacol. 3:1992;327-336.
65. McEwen B. S. Gonadal and adrenal steroids regulate neurochemical and structural plasticity of the hippocampus via cellular mechanisms involving NMDA receptors. Cell. Mol. Neurobiol. 16:1996;103-116.
66. McGurk S. R., Levin E. D., Butcher L. L. Impairment of radial-arm maze performance in rats following lesions involving the cholinergic medial pathway: Reversal by arecoline and differential effects of muscarinic and nicotinic antagonists. Neuroscience. 44:1991;137-147.
67. 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 adult female Sprague-Dawley rat. J. Neurosci. 16:1996;1860-1865.
68. Miranda R. C., Sohrabji F., Toran-Allerand D. Presumptive estrogen target neurons express mRNAs for both the neurotrophins and neurotrophin receptors: A basis for potential developmental interactions of estrogen with the neurotrophins. Mol. Cell. Neurosci. 4:1993;510-525.
69. Mooradian A. D. Antioxidant properties of steroids. J. Steroid Biochem. Mol. Biol. 45:1993;509-511.
70. Muesing R. A., Miller V. T., LaRosa J. C., Stoy D. B., Phillips E. A. Effects of unopposed conjugated equine estrogen on lipoprotein composition and apolipoprotein-E distribution. J. Clin. Endocrinol. Metab. 75:1992;1250-1254.
71. Mufson E. J. NGF, p75NTR and trkA in Alzheimer's disease. Neural Notes. III:1997;16-19.
72. Mufson E. J., Lavine N., Jaffar S., Kordower J. H., Quirion R., Saragovi H. U. Reduction in p140-TrkA receptor protein within the nucleus basalis and cortex in Alzheimer's disease. Exp. Neurol. 146:1997;91-103.
73. Mufson E. J., Li J.-M., Sobreviela T., Kordower J. H. Decreased trkA gene expression within basal forebrain neurons in Alzheimer's disease. NeuroReport. 8:1996;25-29.
74. Murphy D. D., Cole N. B., Greenberger V., Segal M. Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons. J. Neurosci. 18:1998;2550-2559.
75. Murray C. L., Fibiger H. C. Learning and memory deficits after lesions of the nucleus basalis magnocellularis: Reversal by physostigmine. Neuroscience. 14:1985;1025-1032.
76. Murray C. L., Fibiger H. C. Pilocarpine and physostigmine attenuate spatial memory impairments produced by lesions of the nucleus basalis magnocellularis. Behav. Neurosci. 100:1986;23-32.
77. Alzheimer's Association 1995 National Public Policy Program to Conquer Alzheimer's Disease. 1995;Alzheimer's Association, Washington.
78. Niki E., Nakano M. Estrogens as antioxidants. Methods Enzymol. 186:1990;330-333.
79. Nilsson O. G., Leanza G., Rosenblad C., Lappi D. A., Wiley R. G., Björklund A. Spatial learning impairments in rats with selective immunolesion of the forebrain cholinergic system. NeuroReport. 3:1992;1005-1008.
80. Nilsson O. G., Shapiro M. L., Gage F. H., Olton D. S., Björklund A. Spatial learning and memory following fimbria-fornix transection and grafting of fetal septal neurons to the hippocampus. Exp. Brain Res. 67:1987;195-215.
81. 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. 41:1994a;361-371.
82. Ohkura T., Isse K., Akazawa K., Hamamoto M., Yaoi Y., Hagino N. Low-dose estrogen replacement therapy for Alzheimer disease in women. Menopause. 1:1994b;125-130.
83. 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. 6:1995a;99-107.
84. Ohkura T., Teshima Y., Isse K., Matsuda H., Inoue T., Sakai Y., Iwasaki N., Yaoi Y. Estrogen increases cerebral and cerebellar blood flows in postmenopausal women. Menopause. 2:1995b;13-18.
85. Olton D. S. Dementia: Animal models of the cognitive impairments following damage to the basal forebrain cholinergic system. Brain Res. Bull. 25:1990;499-502.
86. 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. 403:1987;389-392.
87. Packard M. G., Kohlmaier J. R., Alexander G. M. Posttraining intrahippocampal estradiol injections enhance spatial memory in male rats: Interaction with cholinergic systems. Behav. Neurosci. 110:1996;626-632.
88. Paganini-Hill A., Henderson V. W. Estrogen deficiency and risk of Alzheimer's disease in women. Am. J. Epidemiol. 140:1994;256-261.
89. Paganini-Hill A., Henderson V. W. Estrogen replacement therapy and risk of Alzheimer's disease. Arch. Intern. Med. 156:1996;2213-2217.
90. Perry E. K., Perry R. H., Blessed G., Tomlinson B. E. Necropsy evidence of cholinergic deficits in senile dementia. Lancet. 1:1977.
91. Perry E. K., Tomlinson B. E., Blessed G., Bergmann K., Gibson P. H., Perry R. H. Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br. Med. J. 2:1978;1457.
92. Phillips S. M., Sherwin B. B. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology. 17:1992a;485-495.
93. Phillips S. M., Sherwin B. B. Variations in memory function and sex steroid hormones across the menstrual cycle. Psychoneuroendocrinology. 17:1992b;497-506.
94. Ridley R. M., Gribble S., Clark B., Baker H. F., Fine A. Restoration of learning ability in fornix-transected monkeys after fetal basal forebrain but not fetal hippocampal tissue transplantation. Neurosci. 48:1992;779-792.
95. Scoville S. A., Bufton S. M., Liuzzi F. J. Effects of chronic ovariectomy and estrogen replacement on lumbar dorsal root ganglion trkA and PPT mRNA levels. Soc. Neurosci. Abstr. 23:1997.
96. Segal R. A., Greenberg M. E. Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19:1996;463-489.
97. Sherwin B. B., Gelfand M. M. Sex steroids and affect in the surgical menopause: A double-blind, cross-over study. Psychoneuroendocrinol. 10:1985;325-335.
98. Shi J., Zhang Y. Q., Simpkins J. W. Effects of 17-β-estradiol on glucose transporter 1 expression and endothelial cell survival following focal ischemia in the rats. Exp. Brain Res. 117:1997;200-206.
99. Simpkins J. W., Rajakamar G., Zhang Y. Q., Simpkins C. E., Greenwald D., Yu C. J., Bodor N., Day A. L. Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat. J. Neurosurg. 87:1997;724-730.
100. Singh M., Meyer E. M., Huang F. S., Millard W. J., Simpkins J. W. Ovariectomy reduces ChAT activity and NGF mRNA levels in the frontal cortex and hippocampus of the female Sprague Dawley rat. Program of the 23rd Annual Meeting of the Society for Neuroscience. 1993;. p. 1254.
101. 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. 644:1994;305-312.
102. Singh M., Meyer E. M., Simpkins J. W. The effects of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats. Endocrinology. 136:1995;2320-2324.
103. Sohrabji F., Miranda R. C., Toran-Allerand C. D. Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J. Neurosci. 14:1994;459-471.
104. Tang M.-X., Jacobs D., Stern Y., Marder K., Schofield P., Gurland B., Andrews H., Mayeux R. Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet. 348:1996;429-432.
105. Thoenen H., Bandtlow C., Heumann R. The physiological function of nerve growth factor in the central nervous system: Comparison with the periphery. Rev. Physiol. Biochem. Pharmacol. 109:1987;145-178.
106. Toran-Allerand D., Miranda R. C., Bentham W. D. L., Sohrabji F., Brown T. J., Hochberg R. B., MacLusky N. J. Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain. Proc. Natl. Acad. Sci. 89:1992;4668-4672.
107. Verdi J. M., Birren S. J., Ibáñez C. F., Persson H., Kaplan D. R., Benedetti M., Chao M. V., Anderson D. J. p75LNGFR regulates Trk signal transduction and NGF-induced neuronal differentiation in MAH cells. Neuron. 12:1994;733-745.
108. Voytko M. L. Cognitive functions of the basal forebrain cholinergic system in monkeys: Memory or attention? Behav. Brain Res. 75:1996;13-25.
109. Weinstock M. The pharmacotherapy of Alzheimer's disease based on the cholinergic hypothesis: An update. Neurodegeneration. 4:1995;349-356.
110. Welner S. A., Dunnett S. B., Salamone J. D., MacLean B., Iversen S. D. Transplantation of embryonic ventral forebrain grafts to the neocortex of rats with bilateral lesions of nucleus basalis magnocellularis ameliorates a lesion-induced deficit in spatial memory. Brain Res. 463:1988;192-197.
111. Wenk G. L. The nucleus basalis magnocellularis cholinergic system: One hundred years of progress. Neurobiol. Learning Mem. 67:1997;85-95.
112. Whitehouse P. J., Price D. L., Struble R. G., Clark A. W., Coyle J. T., DeLong M. R. Alzheimer's disease and senile dementia: Loss of neurons in the basal forebrain. Science. 215:1982;1237-1239.
113. Williams C. L. Short-term but not long-term estradiol replacement improves radial arm maze performance of young and aging rats. Soc. Neurosci. Abstr. 22:1996.
114. Williams C. L., Barnett A. M., Meck W. H. Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav. Neurosci. 104:1990;84-97.
115. Williams C. L., Meck W. H. The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology. 16:1991;155-176.
116. Woolf N. J. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37:1991;475-524.
117. Woolley C. S., McEwen B. S. Estradiol mediates fluctuation in hippocampal synapse density during estrus in the adult rat. J. Neurosci. 12:1992;2549-2554.
118. Xu H., Gouras G. K., Greenfield J. P., Vincent B., Maslund J., Mazzarelli L., Fried G., Jovanovic J. N., Seeger M., Relkin N. R., Liao F., Checler F., Buxbaum J. D., Chait B. T., Thinakaran G., Sisodia S. S., Wang R., Greengard P., Gandy S. Estrogen reduces neuronal generation of Alzheimer β-amyloid peptides. Nat. Med. 4:1998;447-451.