Estrogen, cholinergic system and cognition

Neuroactive Steroids in Brain Function, Behavior and Neuropsychiatric Disorders: Novel Strategies for Research and Treatment

Volumn , Issue , 2008, Pages 123-141

  De Lacalle, Sonsoles ^a   Hyler, Bryan ^a   Borowski, Thomas ^b  

^a CHARLES R DREW UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b PITZER COLLEGE   (United States)

Author keywords

basal forebrain; cholinergic system; estrogen; memory; Plasticity; regeneration

Indexed keywords

EID: 78650000084     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4020-6854-6_6     Document Type: Chapter

References (122)

1. Sherwin BB. Estrogen and cognitive functioning in women. Endocr Rev 2003;24:133-151.
2. Speck O, Ernst T, Braun J, et al. Gender differences in the functional organization of the brain for working memory. Neuroreport 2000;11:2581-2585.
3. Rosenberg L, Park S. Verbal and spatial functions across the menstrual cycle in healthy young women. Psychoneuroendocrinology 2002;27:835-841.
4. Phillips SM, Sherwin BB. Variations in memory function and sex steroid hormones across the menstrual cycle. Psychoneuroendocrinology 1992;17:497-506.
5. Hampson E. Variations in sex-related cognitive abilities across the menstrual cycle. Brain Cogn 1990;14:26-43.
6. Hampson E, Kimura D. Reciprocal effects of hormonal fluctuations on human motor and perceptual-spatial skills. Behav Neurosci 1988;102:456-459.
7. Hampson E. Estrogen-related variations in human spatial and articulatory motor skills. Psychoneuroendocrinology 1990;15:97-111.
8. Zec RF, Trivedi MA. The effects of estrogen replacement therapy on neuropsychological functioning in postmenopausal women with and without dementia: a critical and theoretical review. Neuropsychol Rev 2002;12:65-109.
9. Rice MM, Graves AB, McCurry SM, et al. Estrogen replacement therapy and cognitive function in postmenopausal women without dementia. Am J Med 1997;103:26S-35S.
10. Kampen DL, Sherwin BB. Estrogen use and verbal memory in healthy postmenopausal women. Obstet Gynecol 1994;110:979-983.
11. Robinson D, Friedman L, Marcus R, et al. Estrogen replacement therapy and memory in older women. J Am Geriat Soc 1994;42:919-922.
12. Jacobs DM, Tang MX, Stern Y, et al. Cognitive function in nondemented older women who took estrogen after menopause. Neurology 1998;50:368-373.
13. Smith YR, Giordani B, Lajiness-O'Neill R, et al. Long-term estrogen replacement is associated with improved nonverbal memory and attentional measures in postmenopausal women. Fertil Steril 2001;76:1101-1107.
14. Carlson LE, Sherwin BB. Steroid hormones, memory and mood in a healthy elderly population. Psychoneuroendocrinology 1998;23:583-603.
15. Resnick SM, Metter EJ, Zonderman AB. Estrogen replacement therapy and longitudinal decline in visual memory - A possible protective effect? Neurology 1997;49:1491-1497.
16. Yaffe K, Sawaya G, Lieberburg I, et al. Estrogen therapy in postmenopausal women: Effects on cognitive function and dementia. J Am Med Assoc 1998;279:688-695.
17. Sherwin BB. Estrogenic effects on memory in women. Ann NY Acad Sci 1994;743:213-230.
18. Krug R, Born J, Rasch B. A 3-day estrogen treatment improves prefrontal cortex-dependent cognitive function in postmenopausal women. Psychoneuroendocrinology 2006;31:965-975.
19. Matthews K, Cauley J, Yaffe K, et al. Estrogen replacement therapy and cognitive decline in older community women. J Am Geriatr Soc 1999;47:518-523.
20. Sherwin BB. Estrogen and cognitive aging in women. Neuroscience 2006;138:1021-1026.
21. Henderson VW. Estrogen-containing hormone therapy and Alzheimer's disease risk: Understanding discrepant inferences from observational and experimental research. Neuroscience 2006;138:1031-1039.
22. Pinkerton JV, Henderson VW. Estrogen and cognition, with a focus on Alzheimer's disease. Semin Reprod Med 2005;23:172-179.
23. Almeida OP, Lautenschlager NT, Vasikaran S, et al. A 20-week randomized controlled trial of estradiol replacement therapy for women aged 70 years and older: effect on mood, cognition and quality of life. Neurobiol Aging 2006;27:141-149.
24. Thal LJ, Thomas RG, Mulnard R, et al. Estrogen levels do not correlate with improvement in cognition. Arch Neurol 2003;60:209-212.
25. Turgeon JL, McDonnell DP, Martin KA, et al. Hormone therapy: physiological complexity belies therapeutic simplicity. Science 2004;304:1269-1273.
26. Rapp PR, Morrison JH, Roberts JA. Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J Neurosci 2003;23:5708-5714.
27. Tinkler GP, Voytko ML. Estrogen modulates cognitive and cholinergic processes in surgically menopausal monkeys. Prog Neuropsychopharmacol Biol Psychiatry 2005;29:423-431.
28. Lacreuse A. Effects of ovarian hormones on cognitive function in nonhuman primates. Neuroscience 2006;138:859-867.
29. Voytko ML. Estrogen and the cholinergic system modulate visuospatial attention in monkeys (macaca fascicularis). Behav Neurosci 2002;116:187-197.
30. Daniel JM, Fader AJ, Spencer AL, et al. Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm Behav 1997;32:217-225.
31. Fader AJ, Hendricson AW, Dohanich GP. Estrogen improves performance of reinforced T-maze alternation and prevents the amnestic effects of scopolamine administered systemically or intrahippocampally. Neurobiol Learn Mem 1998;69:225-240.
32. Sandstrom NJ, Williams CL. Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 2001;115:384-393.
33. Luine VN, Richards ST, Wu VY, et al. Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm Behav 1998;34:149-162.
34. O'Neal MF, Means LW, Poole MC, et al. Estrogen affects performance of ovariectomized rats in a two-choice water-escape working memory task. Psychoneuroendocrinology 1996;21:51-65.
35. Bimonte-Nelson HA, Francis KR, Umphlet CD, et al. 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.
36. Rhodes ME, Frye CA. ERâ-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks. Neurobiol Learn Mem 2006;85:183-191.
37. Dohanich GP, Fader AJ, Javorsky DJ. Estrogen and estrogen-progesterone treatments counteract the effect of scopolamine on reinforced T-maze alternation in female rats. Behav Neurosci 1994;108:988-992.
38. Singh M, Meyer EM, Millard WJ, et al. Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res 1994;644:305-312.
39. Williams CL. Short-term but not long-term estradiol replacement improves radial-arm maze performance of young and aging rats. Soc Neurosci Abstr 1996;22:1164.
40. Daniel JM, Dohanich GP. Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 2001;21:6949-6956.
41. Markowska AL, Savonenko AV. Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J Neurosci 2002;22:10985-10995.
42. Daniel JM, Hulst JL, Berbling JL. 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.
43. Packard MG, Kohlmaier JR, Alexander GM. Post-training intra-hippocampal estradiol injections enhance spatial memory in male rats: interaction with cholinergic systems. Behav Neurosci 1996;110:626-632.
44. Packard MG, Teather LA. Posttraining estradiol injections enhance memory in ovariectomized rats: Cholinergic blockade and synergism. Neurobiol Learn Mem 1997;68:172-188.
45. Luine VN, Rodriguez M. Effects of estradiol on radial arm maze performance of young and aged rats. Beha Neural Biol 1994;62:230-236.
46. Hasselmo ME. The role of acetylcholine in learning and memory. Curr Opin Neurobiol 2006;16:710-715.
47. Brann DW, Dhandapani K, Wakade C, et al. Neurotrophic and neuroprotective actions of estrogen: Basic mechanisms and clinical implications. Steroids 2007;72:381-405.
48. Luine VN. Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exper Neurol 1985;89:484-490.
49. Dumas J, Hancur-Bucci C, Naylor M, et al. Estrogen treatment effects on anticholinergicinduced cognitive dysfunction in normal postmenopausal women. Neuropsychopharmacology 2006;31:2065-2078.
50. Gibbs RB. Estrogen and nerve growth factor-related systems in brain. In: Hormonal Restructuring of the Adult Brain. Annals of the New York Academy of Sciences, Vol. 743. November 14, 1994. Edited by New York Academy of Sciences, 1994:165-199.
51. Beninger RJ, Wirsching BA, Jhamandas K, et al. Animal studies of brain acetylcholine and memory. Arch Gerontol Geriatr Suppl 1989;1:71-89.
52. Tanabe F, Miyasaka N, Kubota T, et al. Estrogen and progesterone improve scopolamineinduced impairment of spatial memory. J Med Dent Sci 2004;51:89-98.
53. Gibbs RB, Wu DH, Hersh LB, et al. 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. Exper Neurol 1994;129:70-80.
54. McGaughy J, Sarter M. Effects of ovariectomy, 192 IgG-saporin-induced cortical cholinergic deafferentation, and administration of estradiol on sustained attention performance in rats. Behav Neurosci 1999;113:1216-1232.
55. Miller MM, Hyder SM, Assayag R, et al. Estrogen modulates spontaneous alternation and the cholinergic phenotype in the basal forebrain. Neuroscience 1999;91:1143-1153.
56. Farr SA, Banks WA, Morley JE. Estradiol potentiates acetylcholine and glutamate-mediated post-trial memory processing in the hippocampus. Brain Res 2000;864:263-269.
57. Rudick CN, Gibbs RB, Woolley CS. A role for the basal forebrain cholinergic system in estrogeninduced disinhibition of hippocampal pyramidal cells. J Neurosci 2003;23:4479-4490.
58. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 1st ed. Sydney: Academic, 1982.
59. De Lacalle S, Kulkarni S, Wiley RG. Lesion induced transneuronal plasticity of the cholinergic innervation in the adult rat entorhinal cortex. Eur J Neurosci 1998;10:1054-1062.
60. Saenz C, Dominguez R, De Lacalle S. Estrogen contributes to structural recovery after a lesion. Neurosci Lett 2006;392:198-201.
61. Hartonian I, Mufson EJ, De Lacalle S. Long-term plastic changes in galanin innervation in the rat basal forebrain. Neuroscience 2002;115:787-795.
62. Frye CA. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol Behav 1995;57:5-14.
63. Warren SG, Juraska JM. Spatial and non spatial learning across the rat estrous cycle. Behav Neurosci 1997;111:259-265.
64. Gibbs RB. Estrogen replacement enhances acquisition of a spatial memory task and reduces deficits associated with hippocampal muscarinic receptor inhibition. Horm Behav 1999;36:222-233.
65. Gibbs RB. 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.
66. Heikkinen T, Puolivali J, Liu L, et al. Effects of ovariectomy and estrogen treatment on learning and hippocampal neurotransmitters in mice. Horm Behav 2002;41:22-32.
67. Holmes MM, Wide JK, Galea LA. 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.
68. Galea LA, Wide JK, Paine TA, et al. 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.
69. Ferrini M, Bisagno V, Piroli G, et al. Effects of estrogens on choline-acetyltransferase immunoreactivity and GAP-43 mRNA in the forebrain of young and aging male rats. Cell Mol Neurobiol 2002;22:289-301.
70. Aggarwal P, Gibbs RB. Estrogen replacement does not prevent the loss of choline acetyltransferasepositive cells in the basal forebrain following either neurochemical or mechanical lesions. Brain Res 2000;882:75-85.
71. Gibbs RB. Effects of estrogen on basal forebrain cholinergic neurons vary as a function of dose and duration of treatment. Brain Res 1997;757:10-16.
72. NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp Neurol 1992;116:23-39.
73. McGaughy J, Dalley JW, Morrison CH, et al. Selective behavioral and neurochemical effects of cholinergic lesions produced by intrabasalis infusions of 192 IgG-saporin on attentional performance in a five-choice serial reaction time task. J Neurosci 2002;22:1905-1913.
74. Horvath KM, Hartig W, Van Der Veen R, et al. 17beta-Estradiol enhances cortical cholinergic innervation and preserves synaptic density following excitotoxic lesions to the rat nucleus basalis magnocellularis. Neuroscience 2002;110:489-504.
75. 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.
76. Gibbs RB, Nelson D, Anthony MS, et al. Effects of long term hormone replacement and of tibolone on choline acetyltransferase and acetylcholinesterase activities in the brains of ovariectomized, cynomologous monkeys. Neuroscience 2002;113:907-914.
77. Tinkler GP, Tobin JR, Voytko ML. 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.
78. Kritzer MF, Kohama SG. Ovarian hormones differentially influence immunoreactivity for dopamine â-hydroxylase, choline acetyltransferase, and serotonin in the dorsolateral prefrontal cortex of adult rhesus monkeys. J Comp Neurol 1999;409:438-451.
79. Singer CA, Pang PA, Dobie DJ, et al. Estrogen increases GAP-43 (Neuromodulin) mRNA in the preoptic area of aged rats. Neurobiol aging 1996;17:661-663.
80. Brinton RD, Tran J, Proffitt P, et al. 17 β-estradiol enhances the outgrowth and survival of neocortical neurons in culture. Neurochem Res 1997;22:1339-1351.
81. Ferreira A, Caceres A. Estrogen-enhanced neurite growth: evidence for a selective induction of tau and stable microtubules. J Neurosci 1991;11:392-400.
82. Dominguez R, Jalali C, De Lacalle S. Morphological effects of estrogen on cholinergic neurons in vitro involves activation of extracellular signal-regulated kinases. J Neurosci 2004;24:982-990.
83. Segal M, Murphy D. Estradiol induces formation of dendritic spines in hippocampal neurons: functional correlates. Horm Behav 2001;40:156-159.
84. Garcia-Segura LM, Azcoitia I, Don Carlos LL. Neuroprotection by estradiol. Prog Neurobiol 2001;63:29-60.
85. Desjardins GC, Beaudet A, Meaney MJ, et al. Estrogen-induced hypothalamic β-endorphin neuron loss: a possible model for hypothalamic aging. Exp Gerontol 1995;30:253-267.
86. Sudo S, Wen TC, Desaki J, et al. β-Estradiol protects hippocampal CA1 neurons against transient forebrain ischemia in gerbil. Neurosci Res 1997;29:345-354.
87. Luine VN, Khylchevskaya RI, McEwen BS. Effect of gonadal steroids on activities of monoamine oxidase and choline acetylase in rat brain. Brain Res 1975;86:293-306.
88. McEwen BS, Biegon A, Davis PG, et al. Steroid hormones: humoral signals which alter brain cell properties and functions. Recent Prog Horm Res 1982;38:41-92.
89. Gibbs RB, Aggarwal P. Estrogen and basal forebrain cholinergic neurons: Implications for brain aging and Alzheimer's disease-related cognitive decline. Horm Behav 1998;34:98-111.
90. Gibbs RB. Effects of gonadal hormone replacement on measures of basal forebrain cholinergic function. Neuroscience 2000;101:931-938.
91. Gibbs RB. Effects of ageing and long-term hormone replacement on cholinergic neurones in the medial septum and nucleus basalis magnocellularis of ovariectomized rats. J Neuroendocrinol 2003;15:477-485.
92. Lam TT, Leranth C. Role of the medial septum diagonal band of Broca cholinergic neurons in oestrogen-induced spine synapse formation on hippocampal CA1 pyramidal cells of female rats. Eur J Neurosci 2003;17:1997-2005.
93. Bora SH, Liu Z, Kecojevic A, et al. Direct, complex effects of estrogens on basal forebrain cholinergic neurons. Exp Neurol 2005;194:506-522.
94. Grandholm A-C E, Ford KA, Hyde LA, et al. Estrogen restores cognition and cholinergic phenotype in an animal model of Down syndrome. Physiol Behav 2002;77:371-385.
95. McMillan PJ, Singer CA, Dorsa DM. 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.
96. Pongrac JL, Gibbs RB, De Franco DB. Estrogen-mediated regulation of cholinergic expression in basal forebrain neurons requires extracellular-signal- regulated kinase activity. Neuroscience 2004;124:809-816.
97. Szego EM, Barabas K, Balog J, et al. Estrogen induces estrogen receptor alpha-dependent cAMP response element-binding protein phosphorylation via mitogen activated protein kinase pathway in basal forebrain cholinergic neurons in vivo. J Neurosci 2006;26:4104-4110.
98. Pan Y, Anthony M, Clarkson TB. 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.
99. Watters JJ, Dorsa DM. Transcriptional effects of estrogen on neuronal neurotensin gene expression involve cAMP/protein kinase A-dependent signaling mechanisms. J Neurosci 1998;18:6672-6680.
100. Gabor R, Nagle R, Johnson DA, et al. Estrogen enhances potassium-stimulated acetylcholine release in the rat hippocampus. Brain Res 2003;962:244-247.
101. Resnick SM, Henderson VW. Hormone therapy and risk of Alzheimer disease: a critical time. JAMA 2002;288:2170-2172.
102. Maki PM. Hormone therapy and cognitive function: Is there a critical period for benefit? Neuroscience 2006;138:1027-1030.
103. Shughrue PJ, Lane MV, Merchenthaler I. Comparative distribution of estrogen receptoralpha and -β mRNA in the rat central nervous system. J Comp Neurol 1997;388:507-525.
104. Shughrue PJ, Scrimo PJ, Merchenthaler I. Estrogen binding and estrogen receptor characterization (ERα and ERβ) in the cholinergic neurons of the rat basal forebrain. Neuroscience 2000;96:41-49.
105. Shughrue PJ, Lane MV, Merchenthaler I. Biologically active estrogen receptor-β: evidence from in vivo autoradiographic studies with estrogen receptor á-knockout mice. Endocrinology 1999;140:2613-2620.
106. Miettinen RA, Kalesnykas G, Koivisto EH. Estimation of the total number of cholinergic neurons containing estrogen receptor-á in the rat basal forebrain. J Histochem Cytochem 2002;50:891-902.
107. McMillan PJ, Le Master AM, Dorsa DM. Tamoxifen enhances choline acetyltransferase mRNA expression in rat basal forebrain cholinergic neurons. Mol Brain Res 2002;103:140-145.
108. Singer CA, Figueroa-Masot XA, Batchelor RH, et al. The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J Neurosci 1999;19:2455-2463.
109. Singh M, Setalo G, Jr., Guan X, et al. Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J Neurosci 1999;19:1179-1188.
110. Singh M, Setalo G, Jr., Guan X, et al. Estrogen-induced activation of the mitogen-activated protein kinase cascade in the cerebral cortex of estrogen receptor-a knock-out mice. J Neurosci 2000;20:1694-1700.
111. Pedata F, Giovannelli L, Pepeu G. GM1 ganglioside facilitates the recovery of high-affinity choline uptake in the cerebral cortex of rats with a lesion of the nucleus basalis magnocellularis. J Neurosci Res 1984;12:421-427.
112. Sarter M, Parikh V. Choline transporters, cholinergic transmission and cognition. Nat Rev Neurosci 2005;6:48-56.
113. Towart LA, Alves SE, Znamensky V, et al. Subcellular relationships between cholinergic terminals and estrogen receptor-alpha in the dorsal hippocampus. J Comp Neurol 2003;463:390-401.
114. Leranth C, Shanabrough M, Horvath TL. Hormonal regulation of hippocampal spine synapse density involves subcortical mediation. Neuroscience 2000;101:349-356.
115. Mufson EJ, Cai WJ, Jaffar S, et al. Estrogen receptor immunoreactivity within subregions of the rat forebrain: neuronal distribution and association with perikarya containing choline acetyltransferase. Brain Res 1999;849:253-274.
116. Ishunina TA, Swaab DF. Increased neuronal metabolic activity and estrogen receptors in the vertical limb of the diagonal band of Broca in Alzheimer's disease: relation to sex and aging. Exp Neurol 2003;183:159-172.
117. Henke H, Lang W. Cholinergic enzymes in neocortex, hippocampus and basal forebrain of non-neurological and senile dementia of Alzheimer-type patients. Brain Res 1983;267:281-291.
118. Allen SJ, MacGowan SH, Tyler S, et al. Reduced cholinergic function in normal and Alzheimer's disease brain is associated with apolipoprotein E4 genotype. Neurosci Lett 1997;239:33-36.
119. Pappas BA, Bayley PJ, Bui BK, et al. Choline acetyltransferase activity and cognitive domain scores of Alzheimer's patients. Neurobiol Aging 2000;21:11-17.
120. Schonknecht P, Pantel J, Klinga K, et al. Reduced cerebrospinal fluid estradiol levels are associated with increased β-amyloid levels in female patients with Alzheimer's disease. Neurosci Lett 2001;307:122-124.
121. Auld DS, Kornecook TJ, Bastianetto S, et al. Alzheimer's disease and the basal forebrain cholinergic system: relations to β-amyloid peptides, cognition, and treatment strategies. Prog Neurobiol 2002;68:209-245.
122. Wilcock GK, Esiri MM, Bowen DM, et al. Alzheimer's disease: correlation of cortical choline acetyltransferase activity with the severity of dementia and histological abnormalities. J Neurol Sci 1982;57:407-417.