ERβ-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks

Neurobiology of Learning and Memory

Volumn 85, Issue 2, 2006, Pages 183-191

  Rhodes, Madeline E ^a   Frye, Cheryl A ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Affect; Emotional learning; Estradiol; Learning; Mnemonic; Spatial

Indexed keywords

COUMESTROL; ESTRADIOL; NICOTINAMIDE ADENINE DINUCLEOTIDE; OIL; PROPYL PYRAZOLE TRIOL; SELECTIVE ESTROGEN RECEPTOR MODULATOR; UNCLASSIFIED DRUG; WATER; DIARYLPROPIONITRILE; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR RELATED RECEPTOR BETA; ESTROGEN RECEPTOR-RELATED RECEPTOR BETA; NITRILE; PROPIONIC ACID DERIVATIVE; PYRAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; DOSE RESPONSE; EMOTION; FEMALE; HORMONE ACTION; LORDOSIS; MAZE TEST; MEMORY; NONHUMAN; RAT; SEXUAL BEHAVIOR; SPATIAL MEMORY; ANIMAL; AROUSAL; BRAIN; COMPARATIVE STUDY; DRUG EFFECT; ESCAPE BEHAVIOR; FEAR; INHIBITION (PSYCHOLOGY); LONG EVANS RAT; ORIENTATION; REACTION TIME; RECALL;

ANIMALS; AROUSAL; AVOIDANCE LEARNING; BRAIN; COUMESTROL; DOSE-RESPONSE RELATIONSHIP, DRUG; EMOTIONS; ESCAPE REACTION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR MODULATORS; FEAR; FEMALE; INHIBITION (PSYCHOLOGY); MAZE LEARNING; MENTAL RECALL; NITRILES; ORIENTATION; PROPIONATES; PYRAZOLES; RATS; RATS, LONG-EVANS; REACTION TIME; RECEPTORS, ESTROGEN; SEXUAL BEHAVIOR, ANIMAL;

EID: 32644457649     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2005.10.003     Document Type: Article

References (76)

1. E.M. Apostolakis, J. Garai, J.E. Lohmann, J.H. Clark, and B.W. O'Malley Epidermal growth factor activates reproductive behavior independent of ovarian steroids in female rodents Molecular Endocrinology 14 2000 1086 1098
2. B. Berry, R. McMahan, and M. Gallagher Spatial learning and memory at defined points of the estrous cycle: Effects on performance of a hippocampal-dependent task Behavioral Neuroscience 111 1997 267 274
3. H.A. Bimonte, and V.H. Denenberg Estradiol facilitates performance as working memory load increases Psychoneuroendocrinology 24 1999 161 173
4. E.J. Chesler, and J.M. Juraska Acute administration of estrogen and progesterone impairs the acquisition of the spatial morris water maze in ovariectomized rats Hormones and Behavior 38 2000 234 242
5. J.M. Daniel, A.J. Fader, A.L. Spencer, and G.P. Dohanich Estrogen enhances performance of female rats during acquisition of a radial arm maze Hormones and Behavior 32 1997 217 225
6. G. Diaz-Veliz, V. Soto, N. Dussaubat, and S. Mora Influence of the estrous cycle, ovariectomy and estradiol replacement upon the acquisition of conditioned avoidance responses in rats Physiology and Behavior 46 1989 397 401
7. G. Diaz-Veliz, F. Urresta, N. Dussaubat, and S. Mora Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors Physiology and Behavior 50 1991 61 65
8. H. Eichenbaum, T. Otto, and N.J. Cohen The hippocampus-what does it do? Behavioral and Neural Biology 57 1992 2 36
9. N.K. El-Bakri, A. Islam, S. Zhu, A. Elhassan, A. Mohammed, and B. Winblad Effects of estrogen and progesterone treatment on rat hippocampal NMDA receptors: Relationship to Morris water maze performance Journal of Cellular and Molecular Medicine 8 2004 537 544
10. Espeland, M. A., Rapp, S. R., Shumaker, S. A., Brunner, R., Manson, J. E., & Sherwin, B. B., et al.: Women's Health Initiative Memory Study (2004). Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. Journal of the American Medical Association, 291, 2959-2968.
11. A.J. Fader, P.E. Johnson, and G.P. Dohanich Estrogen improves working but not reference memory and prevents amnestic effects of scopolamine of a radial-arm maze Pharmacology, Biochemistry and Behavior 62 1999 711 717
12. T.C. Foster, K.M. Sharrow, A. Kumar, and J. Masse Interaction of age and chronic estradiol replacement on memory and markers of brain aging Neurobiology of Aging 24 2003 839 852
13. K.M. Frick, S.M. Fernandez, and S.C. Bulinski Estrogen replacement improves spatial reference memory and increases hippocampal synaptophysin in aged female mice Neuroscience 115 2002 547 558
14. C.A. Frye Estrus-associated decrements in a water maze task are limited to acquisition Physiology and Behavio 57 1995 5 14
15. C.A. Frye, L.E. Bayon, N.K. Pursnani, and R.H. Purdy The neurosteroids, progesterone and 3α,5α-THP, enhance sexual motivation, receptivity, and proceptivity in female rats Brain Research 808 1998 72 83
16. C.A. Frye, and E.H. Lacey The neurosteroids DHEA and DHEAS may influence cognitive performance by altering affective state Physiology and Behavior 66 1999 85 92
17. C.A. Frye, S.M. Petralia, and M.E. Rhodes Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3α,5α-THP Pharmacology, Biochemistry, and Behavior 67 2000 587 596
18. C.A. Frye, and M.E. Rhodes Enhancing effects of estrogen on inhibitory avoidance performance may be in part independent of intracellular estrogen receptors in the hippocampus Brain Research 956 2002 285 293
19. C.A. Frye, M.E. Rhodes, and B. Dudek Estradiol to aged female or male mice improves learning in inhibitory avoidance and water maze tasks Brain Research 1036 2005 101 108
20. H.N. Fugger, T.C. Foster, J. Gustafsson, and E.F. Rissman Novel effects of estradiol and estrogen receptor α and β on cognitive function Brain Research 883 2000 258 264
21. L.A. Galea, M. Kavaliers, K.P. Ossenkopp, and E. Hampson Gonadal hormone levels and spatial learning performance in the Morris water maze in male and female meadow voles, Microtus pennsylvanicus Hormones and Behavior 29 1995 106 125
22. J. Garey, M.A. Morgan, J. Frohlich, B.S. McEwen, and D.W. Pfaff Effects of the phytoestrogen coumestrol on locomotor and fear-related behaviors in female mice Hormones and Behavior 40 2001 65 76
23. R.B. Gibbs Estrogen replacement enhances acquisition of a spatial memory task and reduces deficits associated with hippocampal muscarinic receptor inhibition Hormones and Behavior 36 1999 222 233
24. R.B. Gibbs Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats Neurobiology of Aging 21 2000 107 116
25. R.B. Gibbs, R. Gabor, T. Cox, and D.A. Johnson Effects of raloxifene and estradiol on hippocampal acetylcholine release and spatial learning in the rat Psychoneuroendocrinology 29 2004 741 748
26. D.F. Hardy, and J.F. Debold Effects of mounts without intromission upon the behavior of female rats during the onset of estrogen-induced heat Physiology and Behavior 7 1971 643 645
27. S.A. Hart, J.D. Patton, and C.S. Woolley Quantitative analysis of ERα and GAD colocalization in the hippocampus of the adult female rat Journal of Comparative Neurology 440 2001 144 155
28. T. Heikkinen, J. Puolivali, L. Liu, A. Rissanen, and H. Tanila Effects of ovariectomy and estrogen treatment on learning and hippocampal neurotransmitters in mice Hormones and Behavior 41 2002 22 32
29. T. Heikkinen, J. Puolivali, and H. Tanila Effects of long-term ovariectomy and estrogen treatment on maze learning in aged mice Experimental Gerontology 39 2004 1277 1283
30. S.C. Hewitt, and K.S. Korach Oestrogen receptor knockout mice: roles for oestrogen receptors alpha and beta in reproductive tissues Reproduction 125 2003 143 149
31. E. Hogervorst, J. Williams, M. Budge, W. Riedel, and J. Jolles The nature of the effect of female gonadal hormone replacement therapy on cognitive function in post-menopausal women: a meta-analysis Neuroscience 101 2000 485 512
32. I. Izquierdo, and J.H. Medina Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures Neurobiology of Learning and Memory 68 1997 285 316
33. A.M. Jasnow, J. Schulkin, and D.W. Pfaff Estrogen facilitates fear conditioning and increases corticotropin-releasing hormone mRNA expression in the central amygdala in female mice Hormones and Behavior 2005 [Epub ahead of print]
34. D.L. Korol, and L.L. Kolo Estrogen-induced changes in place and response learning in young adult female rats Behavioral Neuroscience 116 2002 411 420
35. D.L. Korol, E.L. Malin, K.A. Borden, R.A. Busby, and J. Couper-Leo Shifts in preferred learning strategy across the estrous cycle in female rats Hormones and Behavior 45 2004 330 338
36. L.M. Kow, and D.W. Pfaff The membrane actions of estrogens can potentiate their lordosis behavior-facilitating genomic actions Proceedings of the National Academy of Sciences of the United States of America 101 2004 12354 12357
37. G.G. Kuiper, B. Carlsson, K. Grandien, E. Enmark, J. Haggblad, and S. Nilsson Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β Endocrinology 138 1997 863 870
38. G.G. Kuiper, J.G. Lemmen, B. Carlsson, J.C. Corton, S.H. Safe, and P.T. van der Saag Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta Endocrinology 139 1998 4252 4263
39. A. Lacreuse, and J.G. Herndon Estradiol selectively affects processing of conspecifics' faces in female rhesus monkeys Psychoneuroendocrinology 28 2003 885 905
40. H. Lannert, P. Wirtz, V. Schuhmann, and R. Galmbacher Effects of Estradiol (-17β) on learning, memory and cerebral energy metabolism in male rats after intracerebroventricular administration of streptozotocin Journal of Neural Transmission 105 1998 1045 1063
41. E.D. Lephart, T.W. West, K.S. Weber, R.W. Rhees, K.D. Setchell, and H. Adlercreutz Neurobehavioral effects of dietary soy phytoestrogens Neurotoxicology and Teratology 24 2002 5 16
42. M.K. Lindberg, S. Moverare, S. Skrtic, H. Gao, K. Dahlman-Wright, and J.A. Gustafsson Estrogen receptor (ER)-β reduces ERα-regulated gene transcription, supporting a "ying yang" relationship between ERα and ERβ in mice Molecular Endocrinology 17 2003 203 208
43. L. Linzmayer, H.V. Semlitsch, B. Saletu, G. Bock, G. Saletu-Zyhlarz, and A. Zoghlami Double-blind, placebo-controlled psychometric studies on the effects of a combined estrogen-progestin regimen versus estrogen alone on performance, mood and personality of menopausal syndrome patients Arzneimittelforschung 51 2001 238 245
44. V.N. Luine, L.F. Jacome, and N.J. Maclusky Rapid enhancement of visual and place memory by estrogens in rats Endocrinology 144 2003 2836 2844
45. V.N. Luine, S.T. Richards, V.Y. Wu, and K.D. Beck Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters Hormones and Behavior 34 1998 149 162
46. L.K. Marriott, B. Hauss-Wegrzyniak, R.S. Benton, P.D. Vraniak, and G.L. Wenk Long-term estrogen therapy worsens the behavioral and neuropathological consequences of chronic brain inflammation Behavioral Neuroscience 116 2002 902 911
47. L.K. Marriott, and D.L. Korol Short-term estrogen treatment in ovariectomized rats augments hippocampal acetylcholine release during place learning Neurobiology of Learning and Memory 80 2003 315 322
48. M.J. Meyers, J. Sun, K.E. Carlson, G.A. Marriner, B.S. Katzenellenbogen, and J.A. Katzenellenbogen Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues Journal of Medicinal Chemistry 44 2001 4230 4251
49. T.A. Milner, B.S. McEwen, S. Hayashi, C.J. Li, L.P. Reagan, and S.E. Alves Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites Journal of Comparative Neurology 429 2001 355 371
50. S. Mora, N. Dussaubat, and G. Diaz-Veliz Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats Psychoneuroendocrinology 21 1996 609 620
51. M.A. Morgan, and D.W. Pfaff Effects of estrogen on activity and fear-related behaviors in mice Hormones and Behavior 40 2001 472 482
52. M.A. Morgan, J. Schulkin, and D.W. Pfaff Estrogens and non-reproductive behaviors related to activity and fear Neuroscience and Biobehavioral Reviews 28 2004 55 63
53. S. Ogawa, J. Chan, J.A. Gustafsson, K.S. Korach, and D.W. Pfaff Estrogen increases locomotor activity in mice through estrogen receptor alpha: specificity for the type of activity Endocrinology 144 2003 230 239
54. S. Ogawa, V. Eng, J. Taylor, D.B. Lubahn, K.S. Korach, and D.W. Pfaff Roles of estrogen receptor-α gene expression in reproduction-related behaviors in female mice Endocrinology 139 1998 5070 5081
55. S. Ogawa, J.D. Gordan, J. Taylor, D. Lubahn, K. Korach, and D.W. Pfaff Reproductive functions illustrating direct and indirect effects of genes on behavior Hormones and Behavior 30 1996 487 494
56. M.F. O'Neal, L.W. Means, M.C. Poole, and R.J. Hamm Estrogen affects performance of ovariectomized rats in a two-choice water-escape working memory task Psychoneuroendocrinology 21 1996 51 65
57. M.G. Packard, and L.A. Teather Posttraining estradiol injections enhance memory in ovariectomized rats: Cholinergic blockade and synergism Neurobiology of Learning and Memory 68 1997 172 188
58. G. Pelletier, and M. El-Alfy Immunocytochemical localization of estrogen receptors alpha and beta in the human reproductive organs The Journal of Clinical Endocrinology and Metabolism 85 2000 4835 4840
59. M.E. Rhodes, and C.A. Frye Estrogen has mnemonic enhancing effects in the inhibitory avoidance task Pharmacology, Biochemistry, and Behavior 78 2004 551 558
60. E.F. Rissman, A.L. Heck, J.E. Leonard, M.A. Shupnik, and J.A. Gustafsson Disruption of estrogen receptor beta gene impairs spatial learning in female mice Proceedings of the National Academy of Sciences of the United States of America 99 2002 3996 4001
61. N.J. Sandstrom, and C.L. Williams Memory retention is modulated by acute estradiol and progesterone replacement Behavioral Neuroscience 115 2001 384 393
62. B.B. Sherwin Oestrogen and cognitive function throughout the female lifespan Novartis Foundation Symposium 230 2000 188 196
63. P.J. Shughrue, M.V. Lane, and I. Merchenthaler Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system Journal of Comparative Neurology 388 1997 507 525
64. P.J. Shughrue, and I. Merchenthaler Distribution of estrogen receptor beta immunoreactivity in the rat central nervous system Journal of Comparative Neurology 436 2001 64 81
65. P.J. Shughrue, and I. Merchenthaler Evidence for novel estrogen binding sites in the rat hippocampus Neuroscience 99 2000 605 612
66. Shumaker, S. A., Legault, C., Kuller, L., Rapp, S. R., Thal, L., & Lane, D. S., et al.; Women's Health Initiative Memory Study. 2004. Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. The Journal of the American Medical Association 291, 2947-2958.
67. Shumaker, S. A., Legault, C., Rapp, S. R., Thal, L., Wallace, R. B., & Ockene, J. K., et al.; WHIMS Investigators 2003. 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. The Journal of the American Medical Association 289, 2651-2662.
68. R.W. Stackman, M.E. Blasberg, C.J. Langan, and A.S. Clark Stability of spatial working memory across the estrous cycle of Long-Evans rats Neurobiology of Learning and Memory 67 1997 167 171
69. S.R. Stauffer, C.J. Coletta, R. Tedesco, G. Nishiguchi, K. Carlson, J. Sun, B.S. Katzenellenbogen, and J.A. Katzenellenbogen Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists Journal of Medicinal Chemistry 43 2000 4934 4947
70. L.A. Towart, S.E. Alves, V. Znamensky, S. Hayashi, B.S. McEwen, and T.A. Milner Subcellular relationships between cholinergic terminals and estrogen receptor-alpha in the dorsal hippocampus Journal of Comparative Neurology 463 2003 390 401
71. H.G. Van Oyen, N.E. Van De Poll, and J.P. De Bruin Sex, age and shock-intensity as factors in passive avoidance Physiology and Behavior 23 1979 915 918
72. N. Vasudevan, L.M. Kow, and D.W. Pfaff Early membrane estrogenic effects required for full expression of slower genomic actions in a nerve cell line Proceedings of the National Academy of Sciences of the United States of America 98 2001 12267 12271
73. J.M. Vongher, and C.A. Frye Progesterone in conjunction with estradiol has neuroprotective effects in an animal model of neurodegeneration Pharmacology Biochemistry and Behavior 64 1999 777 785
74. A.A. Walf, and C.A. Frye ERβ-selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats Neuropsychopharmacology 30 2005 1598 1609
75. A.A. Walf, M.E. Rhodes, and C.A. Frye Antidepressant effects of ERβ-selective estrogen receptor modulators in the forced swim test Pharmacology Biochemistry and Behavior 78 2004 523 529
76. S.G. Warren, and J.M. Juraska Spatial and nonspatial learning across the rat estrous cycle Behavioral Neuroscience 111 1997 259 266