Impact of estrogen receptor alpha and beta agonists on delayed alternation in middle-aged rats

Hormones and Behavior

Volumn 58, Issue 5, 2010, Pages 878-890

  Neese, Steven L ^a   Korol, Donna L ^a   Katzenellenbogen, John A ^a   Schantz, Susan L ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Aging; Cognition; DSA; Estrogen receptor agonists; Working memory

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; DIARYLPROPIONITRILE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DELAYED SPATIAL ALTERATION; FEMALE; HORMONAL REGULATION; LONG EVANS RAT; MENTAL TASK; NONHUMAN; PRIORITY JOURNAL; RAT; TASK PERFORMANCE; WORKING MEMORY;

AGING; ANIMALS; BEHAVIOR, ANIMAL; COGNITION; CONDITIONING, OPERANT; DRUG EVALUATION, PRECLINICAL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; MEMORY, SHORT-TERM; NITRILES; PROPIONATES; PYRAZOLES; RATS; RATS, LONG-EVANS; SELECTIVE ESTROGEN RECEPTOR MODULATORS; TASK PERFORMANCE AND ANALYSIS;

EID: 78349307271     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2010.08.017     Document Type: Article

References (117)

1. Abrari K., Rashidy-Pour A., Semnanian S., Fathollahi Y. Post-training administration of corticosterone enhances consolidation of contextual fear memory and hippocampal long-term potentiation in rats. Neurobiol. Learn. Mem. 2009, 91:260-265.
2. Boccia M.M., Kopf S.R., Baratti C.M. Effects of a single administration of oxytocin or vasopressin and their interactions with two selective receptor antagonists on memory storage in mice. Neurbiol. Learn. Mem. 1998, 69:136-146.
3. Brailoiu E., Dun S.L., Brailoiu G.C., Mizuo K., Sklar L.A., Oprea T.I., Prossnitz E.R., Dun N.J. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 2007, 193:311-321.
4. Bubser M., Schmidt W.J. 6-Hydroxydopamine lesion of the rat prefrontal cortex increases locomotor activity, impairs acquisition of delayed alternation tasks, but does not affect uninterrupted tasks in the radial maze. Behav. Brain. Res. 1990, 37(2):157-168.
5. Chudasama Y., Robbins T.W. Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys, and humans. Biol. Psychol. 2006, 73(1):19-38.
6. Chung W.C.J., Pak T.R., Suzuki S., Pouliot W.A., Andersen M.E., Handa R.J. Estrogen receptor beta splice variant protein (ERβ2) in the adult female rat forebrain and midbrain regions. J. Comp. Neurol. 2007, 505:249-267.
7. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. Rev. 2001, 36:60-90.
8. 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(3):217-225.
9. Daniel J.M., Dohanich G.P. Acetylcholine mediated the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J. Neurosci. 2001, 21(17):6949-6956.
10. 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(1):607-614.
11. Davis D.M., Jacobson T.K., Aliakbair S., Mizumori S.J.Y. Differential effects of estrogen on hippocampal- and striatal-dependent learning. Neurobiol. Learn. Mem. 2005, 84:132-137.
12. Dohanich, G.P.; Korol, D.L.; Shors, T.J., 2009. Steroids, learning and memory. In: Pfaff, D.; Arnold, A.; Rubin, R.; Fahrbach, S.; Etgen, A., eds. Hormones, Brain and Behavior, 2nd ed. New York: Academic Press, pp. 265-327.
13. Dudchenko P.A. An overview of the tasks used to test working memory in rodents. Neurosci. Biobehav. Rev. 2004, 28(7):699-709.
14. Dupont A., DiPaolo T., Gagne B., Barden N. Effects of chronic estrogen treatment on dopamine concentrations and turnover in discrete brain nuclei of ovariectomized rats. Neurosci. Lett. 1981, 22:69-74.
15. Elsner J. Testing strategies in behavioral teratology. III. Microanalysis of behavior. Neurobehav. Toxicol. Teratol. 1986, 8(5):573-584.
16. Elsner J., Alder S., Zbinden G. Interaction between ethanol and caffeine in operant behavior of rats. Psychopharmacology 1988, 96:194-205.
17. Ennaceur A., Neave N., Aggleton J.P. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulated cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp. Brain Res. 1997, 113:509-519.
18. Fentie I.H., Greenwood M.M., Wyss J.M., Clark J.T. Age-related changes in gonadal hormones in Long-Evans rats. Endocrine 2004, 25(1):15-22.
19. Floresco S.B., Magyar O. Mesocortical dopamine modulation of executive functions: beyond working memory. Psychopharmacology 2006, 188:567-585.
20. Floresco S.B., Seamans J.K., Phillips A.G. Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without delay. J. Neurosci. 1997, 17(5):1880-1890.
21. Foster T.C., Sharrow K.M., Kumar A., Masse J. Interaction of age and chronic estradiol replacement on memory markers of brain aging. Neurobiol. Aging 2003, 24:839-852.
22. Foy M.R., Baudry M., Foy J.G., Thompson R.F. 17β-estradiol modifies stress-induced and age-related changes in hippocampal synaptic plasticity. Behav. Neurosci. 2008, 122(2):301-309.
23. 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.
24. Frye C.A., Duffy C.K., Walf A.A. Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol. Learn. Mem. 2007, 88:208-216.
25. 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(1-2):115-126.
26. Gendle M.H., Strawderman M.S., Mactutus C.F., Booze R.M., Levitsky D.A., Strupp B.J. Prenatal cocaine exposure does not alter working memory in adult rats. Neurotoxicol. Teratol. 2004, 26(2):319-329.
27. Gibbs R.B., Edwards D., Lazar N., Nelson D., Talameh J. Effects of long-term hormone treatment and of tibolone on monoamines and monoamine metabolites in the brains of ovariectomised. Cynomologous monkeys. J. Neuroendocrinol. 2006, 18(9):643-654.
28. Goldman-Rakic P.S. Architecture of the prefrontal cortex and the central executive. Ann. N.Y. Acad. Sci. 1995, 15(769):71-83.
29. Grady D., Herrington D., Bittner V., Blumenthal R., Davidson M., Hlatky M., Hsia J., Hully S., Herd A., Khan S., Newby L.K., Waters D., Vittinghoff E., Wenger N. Cardiovascular disease outcomes during 6.8years of hormone therapy: heart and estrogen/progestin replacement study follow-up (HERS II). J.A.M.A. 2002, 288:49-57.
30. Gresack J.E., Frick K.M. Effects of continuous and intermittent estrogen treatments on memory in aging female mice. Brain Res. 2006, 1115(1):135-147.
31. Gruber C.J., Tschuggel W., Schneeberger C., Huber J.C. Production and actions of estrogens. N. Engl. J. Med. 2002, 346(5):340-352.
32. 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.
33. Harris H.A., Katzenellenbogen J.A., Katzenellenbogen B.S. Characterization of the biological roles of the estrogen receptors, ERα and ERβ, in the estrogen target tissues in vivo through the use of an ERα-selective ligand. Endocrinology 2002, 143(11):4172-4177.
34. Hodges H. Maze procedures: the radial-arm and water maze compared. Brain Res. Cogn. Brain Res. 1996, 3(3-4):167-181.
35. Holmes A., Wellman C.L. Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci. Biobehav. Rev. 2009, 33:773-783.
36. Hu M., Becker J.B. Acquisition of cocaine self-administration in ovariectomized female rats: effect of estradiol dose or chronic estradiol administration. Drug Alcohol Depen. 2008, 94:56-62.
37. 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(5):1855-1859.
38. Hubscher C.H., Brooks D.L., Johnson J.R. A quantitative method for assessing stages of the rat estrous cycle. Biotech. Histochem. 2005, 80(2):79-87.
39. Inagaki T., Gautreaux C., Luine V. Acute estrogen treatment facilitates recognition memory consolidation and alters monoamine levels in memory-related brain areas. Horm. Behav. 2010, 58(3):415-426.
40. Isaacson R.L., Varner J.A., Baars J.M., de Wied D. The effects of pregnenolone sulfate and ethylestrenol on retention of a passive avoidance task. Brain Res. 1995, 689:79-84.
41. Izaki Y., Takita M., Akema T. Specific role of the posterior dorsal hippocampus-prefrontal cortex in short-term working memory. Eur. J. Neurosci. 2008, 27(11):3029-3034.
42. Janowsky J.S., Chavez B., Orwoll E. Sex steroids modify working memory. J. Cogn. Neurosci. 2000, 12(3):407-414.
43. Jones M.W. A comparative review of rodent prefrontal cortex and working memory. Curr. Mol. Med. 2002, 2:639-647.
44. Khan M.M., Hadman M., Wakade C., De Sevilla L., Dhanapani K.M., Mahesh V.B., Vadlamudi R.K., Brann D.W. Cloning, expression, and localization of MNAR/PELP1 in rodent brain: colocalization in estrogen receptor-α- but not in gonadotropin-releasing hormone-positive neurons. Endocrinology 2005, 146(12):5215-5227.
45. Kopp C., Ressel V., Wigger E., Tobler I. Influence of estrus cycle and ageing on activity patterns in two inbred mouse strains. Behav. Brain Res. 2006, 167(1):165-174.
46. Korol D.L. Role of estrogen in balancing contributions from multiple memory systems. Neurobiol. Learn. Mem. 2004, 82:309-323.
47. Korol D.L., Kolo L.L. Estrogen-induced changes in place and response learning in young adult female rats. Behav. Neurosci. 2002, 116(3):411-420.
48. Korol D.L., Gold P.E. Hormones and behavior. Neurobiology of Learning and Memory 2007, 243-268. Elsevier, New York. 2nd ed. R. Kesner, J. Martinez (Eds.).
49. Kozlov A.P., Druzin M.Y., Kurzina N.P. The role of D1-dependent dopaminergic mechanisms of the frontal cortex in delayed responding in rats. Neurosci. Behav. Physiol. 2001, 31(4):405-411.
50. Kritzer M.F. Regional, laminar, and cellular distribution of immunoreactivity for ER alpha and ER beta in the cerebral cortex of hormonally intact, adult male and female rats. Cereb. Cortex 2002, 12(2):116-128.
51. Kritzer M.F. Ovarian hormone influences on the density of immunoreactivity for tyrosine hydroxylase and serotonin in the primate corpus striatum. Neuroscience 2003, 122(3):757-772.
52. Kritzer M.F., Kohama S.G. Ovarian hormones influence the morphology, distribution, and density of tyrosine hydroxylase immunoreactive axons in the dorsolateral prefrontal cortex of adult rhesus monkeys. J. Comp. Neurol. 1998, 395(1):1-17.
53. LeFevre J., McClintock M.K. Reproductive senescence in female rats: a longitudinal study of individual differences in estrous cycles and behavior. Biol. Reprod. 1988, 38(4):780-789.
54. Lee I., Kesner R.P. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J. Neurosci. 2003, 23:1517-1523.
55. LeSaux M., DiPaolo T. Chronic estrogenic drug treatment increases preproenkephalin mRNA levels in the rat striatum and nucleus accumbens. Psychoneuroendocrinology 2005, 30(3):251-260.
56. LeSaux M., DiPaolo T. Influence of oestrogenic compounds on monoamine transporters in rat striatum. J. Neuroendocrinol. 2006, 18:25-32.
57. LeSaux M., Morrissette M., DiPaolo T. ERbeta mediated the estradiol increase of D2 receptors in rat striatum and nucleus accumbens. Neuropharmacology 2006, 50:451-457.
58. Luine V.N. Sex steroids and cognitive function. J. Neuroendocrinol. 2008, 20(6):866-872.
59. Luine V.N., Richards S.T., Wu V.Y., Beck K.D. Estradiol enhances learning and memory in a spatial task and effects levels of monoaminergic neurotransmitters. Horm. Beh. 1998, 34:149-162.
60. Lund T.D., Rovis T., Chung W.C.J., Handa R.J. Novel actions of estrogen receptor-β on anxiety-related behaviors. Endocrinology 2005, 142(2):797-807.
61. Lupien S.J., Lepage M. Stress, memory, and the hippocampus: can't live with it, can't live without it. Behav. Brain Res. 2001, 127:137-158.
62. Maki P.M., Gast M.J., Vieweg A.J., Burriss S.W., Yaffe K. Hormone therapy in menopausal women with cognitive complaints. Neurology 2007, 69:1322-1330.
63. Mannino C.A., South S.M., Inturrisi C.E., Quinones-Jenab V. Pharmacokinetics and effects of 17beta-estradiol and progesterone implants in ovariectomized rats. J. Pain. 2005, 6(12):809-816.
64. 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(3):284-293.
65. 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(18):8122-8133.
66. Maruki K., Izaki Y., Hori K., Nomura M., Yamauchi T. Effects of rat ventral and dorsal hippocampus temporal inactivation on delayed alternation task. Brain Res. 2001, 895(1-2):273-276.
67. McEwen B.S. Estrogen actions throughout the brain. Recent Prog. Horm. Res. 2002, 57:357-384.
68. McEwen B.S., Alves S.E. Estrogen actions in the central nervous system. Endocr. Rev. 1999, 20(3):279-307.
69. Meyers M.J., Sun J., Carlson K.E., Marriner G.A., Katzenellenbogen B.S., Katzenellenbogen J.A. Estrogen receptor-β potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J. Med. Chem. 2001, 44:4230-4251.
70. Mitra S.W., Hoskin E., Yudkovitz J., Pear L., Wilknison H.A., Hayashi S., Pfaff D.W., Ogawa S., Rohrer S.P., Schaeffer J.M., McEwen B.S., Alves S.E. Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 2003, 144(5):2055-2067.
71. Mizoguchi K., Shoji H., Tanaka Y., Maruyama W., Tabira T. Age-related spatial working memory impairment is caused by prefrontal cortical dopaminergic dysfunction in rats. Neuroscience 2009, 162(4):1192-1201.
72. National Institutes of Health Public Health Service Policy on Humane Care and Use of Laboratory Animals 2002, NIH/Office of Laboratory Animal Welfare, Rockville, MD.
73. National Research Council Institute for Laboratory Animals Research Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research 2003, National Academy Press, Washington, D. C.
74. Newland M.C., Ng W.W., Baggs R.B., Gentry G.D., Weiss B., Miller R.K. Operant behavior in transition reflects neonatal exposure to cadmium. Teratology 1986, 34(3):231-241.
75. Overpeck J.G., Colson S.H., Hohmann J.R., Applestine M.S., Reilly J.F. Concentrations of circulating steroids in normal prepubertal and adult male and female humans, chimpanzees, rhesus monkeys, rats, mice, and hamsters: a literature survey. J. Toxicol. Environ. Health 1978, 4(5-6):785-803.
76. Pandaranandaka J., Poonyachoti S., Kalandakanond-Thongsons S. Anxiolytic property of estrogen related to the changes of the monoamine levels in various brain regions of ovariectomized rats. Physiol. Beh. 2006, 87:828-835.
77. Prokai L., Simpkins J.W. Structure-nongenomic neuroprotection relationship of estrogens and estrogen-derived compounds. Pharmacol. Therapeut. 2007, 114:1-12.
78. 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. Ann. Rev. Physiol. 2008, 70:165-190.
79. 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(5):1802-1810.
80. Robbins T.W., Arnsten A.F.T. The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Ann. Rev. Neurosci. 2009, 32:267-287.
81. Roegge C.S., Widholm J.J., Engeseth N.J., Wang X., Brosch K.O., Seegal R.F., Schantz S.L. Delayed spatial alternation impairments in adult rats following dietary n-6 deficiency during development. Neurotoxicol. Teratol. 2005, 27(3):485-495.
82. Roesch D.M. Effects of selective receptor agonists on food intake and body weight gain in rats. Physiol. Behav. 2006, 87:39-44.
83. Rhodes M.E., Frye C.A. ERβ-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks. Neurobiol. Learn. Mem. 2006, 85:183-191.
84. Rodgers S.P., Bohacek J., Daniel J.M. Transient estradiol exposure during middle age in ovariectomized rats exerts lasting effects on cognitive function and the hippocampus. Endocrinology 2010, 151(3):1194-1203.
85. Roozendaal B. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 2000, 25:213-238.
86. Santollo J., Wiley M.D., Eckel L.A. Acute activation of ERα decreases food intake, meal size, and body weight in ovariectomized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293(6):R2194-R2201.
87. Savonenko A.V., Markowska A.L. The cognitive effects of ovariectomy and estrogen replacement are modulated by aging. Neuroscience 2003, 119(3):821-830.
88. Shughrue P.J., Merchenthaler I. Distribution of estrogen receptor beta immunoreactivity in the rat central nervous system. J. Comp. Neurol. 2001, 436(1):64-81.
89. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 1997, 388(4):507-525.
90. Sloan H.L., Good M., Dunnett S.B. Double dissociation between hippocampal and prefrontal lesions on an operant delayed matching task and a water maze reference memory task. Behav. Brain Res. 2006, 171(1):116-126.
91. Stauffer S.R., Coletta C.J., Tedesco R., Nishiguchi G., Carlson K., Sun J., Katzenellenbogen B.S., Katzenellenbogen J.A. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-α-selective relationships. J. Med. Chem. 2000, 43:4934-4947.
92. Strupp B.J., Beaudin S.A. Assessing the neurobehavioral effects of early toxicant exposure: a perspective from animal research. Human Developmental Neurotoxicology 2006, 415-445. Taylor & Francis Group, New York. D. Bellinger (Ed.).
93. 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. Mem. 2008, 90:155-163.
94. Toran-Allerand C.D. Estrogen and the brain: beyond ER-alpha, ER-beta, and 17beta-estradiol. Ann. N.Y. Acad. Sci. 2005, 1052:136-144.
95. Verma A., Moghaddam B. NMDA receptor antagonists impair prefrontal cortex function as assessed via spatial delayed alternation performance in rats: modulation by dopamine. J. Neurosci. 1996, 16(1):373-379.
96. Vijayraghavan S., Wang M., Birnbaum S.G., Williams G.V., Arnsten A.F. Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nat. Neurosci. 2007, 10(3):376-384.
97. Walf A.A., Rhodes M.E., Frye C.A. Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats. Neurobiol. Learn. Mem. 2006, 86:35-46.
98. Walf A.A., Koonce C.J., Frye C.A. Estradiol or diarylpropionitrile decrease anxiety-like behavior of wildtype, but not estrogen receptor beta knockout, mice. Beh. Neurosci. 2008, 122:974-981.
99. Walf A.A., Koonce C.J., Frye C.A. Estradiol or diarylpropionitrile administration to wild type, but not estrogen receptor beta knockout, mice enhances performance in the object recognition and object placement tasks. Neurobiol. Learn. Mem. 2008, 89(4):513-521.
100. Walf A.A., Paris J.J., Frye C.A. Chronic estradiol replacement to aged female rats reduces anxiety-like and depression-like behavior and enhances cognitive performance. Psychoneuroendocrinology 2009, 34:909-916.
101. Wang V.C., Sable H.K., Ju Y., Allred C.D., Helferich W.G., Korol D.L., Schantz S.L. Effects of chronic estradiol treatment on delayed spatial alternation and differential reinforcement of low rates of responding. Behav. Neurosci. 2008, 122(4):794-804.
102. Wang V.C., Neese S.L., Korol D.L., Schantz S.L. Chronic estradiol replacement impairs performance on an operant delayed spatial alternation task in young, middle-aged, and old rats. Horm. Behav. 2009, 56:382-390.
103. Warburton E.C., Brown M.W. Findings from animals concerning when interactions between perirhinal cortex, hippocampus, and medial prefrontal cortex are necessary for recognition memory. Neuropsychologia 2010, 48(8):2262-2272.
104. Warren S.G., Juraska J.M. Sex differences and estropausal phase effects on water maze performance in aged rats. Neurbiol. Learn. Mem. 2000, 74(3):229-240.
105. Wegorzewska I.N., Walters K., Weiser M.J., Cruthirds D.F., Ewell E., Larco D.O., Handa R.J., Wu J. Postovariectomy weight gain in female rats is reversed by estrogen receptor α agonist, propylpyrazoletriol. Am. J. Obstet. Gynecol. 2008, 199(1):67.e1-67.e5.
106. Weiser M.J., Foradori C.D., Handa R.J. Estrogen receptor beta in the brain: from form to function. Brain Res. Rev. 2008, 57:309-320.
107. Weiser M.J., Wu J., Handa R.J. Estrogen receptor-β agonist diarylpropionitrile: biological activities of R- and S-enantiomers on behavior and hormonal response to stress. Neuroendocrinology 2009, 150(4):1817-1825.
108. Widholm J.J., Clarkson G.B., Strupp B.J., Crofton K.M., Seegal R.F., Schantz S.L. Spatial reversal learning in Aroclor 1254-exposed rats: sex-specific deficits in associative ability and inhibitory control. Toxicol. Appl. Pharmacol. 2001, 174(2):188-198.
109. Widholm J.J., Seo B.W., Strupp B.J., Seegal R.F., Schantz S.L. Effects of perinatal exposure to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin on spatial and visual reversal learning in rats. Neurotoxicol. Teratol. 2003, 25(4):459-471.
110. Widholm J.J., Villareal S., Seegal R.F., Schantz S.L. Spatial alternation deficits following developmental exposure to Aroclor 1254 and/or methylmercury in rats. Toxicol. Sci. 2004, 82(2):577-589.
111. Williams G.V., Castner S.A. Under the curve: critical issues for elucidating D1 receptor function in working memory. Neuroscience 2006, 139:263-276.
112. Winocur G., Hasher L. Aging and time-of-day effects on cognition in rats. Behav. Neurosci. 1999, 113(5):991-997.
113. Winocur G., Hasher L. Age and time-of-day effects on learning and memory in a non-matching-to-sample test. Neurbiol. Aging 2004, 25(8):1107-1115.
114. Yener T., Tunc A.T., Aslan H., Aytan H., Caliskan A.C. Determination of oestrous cycle of the rats by direct examination: how reliable?. Anat. Histol. Emryol. 2007, 36:75-77.
115. Zahrt J., Taylor J.R., Mathew R.G., Arnsten A.F. Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance. J. Neurosci. 1997, 17(21):8528-8535.
116. Zurkovsky L., Brown S.L., Korol D.L. Estrogen modulates place learning through estrogen receptors in the hippocampus. Neurobiol. Learn. Mem. 2006, 86(3):336-343.
117. Zurkovsky L., Brown S.L., Boyd S.E., Fell J.A., Korol D.L. Estrogen modulates learning in female rats by acting directly at distinct memory systems. Neuroscience 2007, 144(1):26-37.