Building a scientific framework for studying hormonal effects on behavior and on the development of the sexually dimorphic nervous system

NeuroToxicology

Volumn 29, Issue 3, 2008, Pages 504-519

  Li, Abby A ^a   Baum, Michael J ^b   McIntosh, Laura J ^a   Day, Mark ^c   Liu, Feng ^c   Gray Jr , L Earl ^d  

^a EXPONENT INC   (United States)

^b Boston University   (United States)

^c PFIZER INC   (United States)

^d U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Androgens; Animal model; Behavior; Brain; Cognition; Developmental neurotoxicology; Developmental toxicology; Endocrine disruptor; Estrogen receptor alpha agonist; Estrogen receptor beta agonist; Estrogens; Ferret; Gender identity; Hippocampus; Hormone; Hormone therapy; Methoxychlor; Neuroprotection; Ovareictomized; Rat; Sexual differentiation; Sexual orientation; Sexually dimorphic; Synaptic plasticity; Two generation reproduction study

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ANDROGEN; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ENDOCRINE DISRUPTOR; HORMONE; PHENOL DERIVATIVE;

ARTICLE; BEHAVIOR CHANGE; BRAIN DEVELOPMENT; CENTRAL NERVOUS SYSTEM; COGNITION; DECISION MAKING; HORMONAL THERAPY; IMPULSIVENESS; LEARNING DISORDER; NERVE CELL PLASTICITY; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PSYCHOSEXUAL DEVELOPMENT; RISK ASSESSMENT; SEX DIFFERENTIATION; ANIMAL; ANIMAL BEHAVIOR; BEHAVIOR; DRUG EFFECT; DRUG POTENTIATION; FEMALE; GROWTH, DEVELOPMENT AND AGING; HUMAN; MALE; NERVOUS SYSTEM; PHYSIOLOGY; REVIEW; SEXUAL DEVELOPMENT; SYNAPSE;

ANIMALIA; MUSTELA; RATTUS;

ANIMALS; BEHAVIOR; BEHAVIOR, ANIMAL; ENDOCRINE DISRUPTORS; ESTROGEN RECEPTOR BETA; FEMALE; HORMONES; HUMANS; MALE; NERVOUS SYSTEM; PHENOLS; SEX CHARACTERISTICS; SYNAPSES;

EID: 44649098815     PISSN: 0161813X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuro.2008.02.015     Document Type: Article

References (129)

1. Adams M.M., Fink S.E., Janssen W.G., Shah R.A., and Morrison J.H. Estrogen modulates synaptic N-methyl-d-aspartate receptor subunit distribution in the aged hippocampus. J Comp Neurol 474 (2004) 419-426
2. Adriani W., Seta D.D., Dessi-Fulgheri F., Farabollini F., and Laviola G. Altered profiles of spontaneous novelty seeking, impulsive behavior, and response to d-amphetamine in rats perinatally exposed to bisphenol A. Environ Health Perspect 111 4 (2003) 395-401
3. Alexseyenko O.V., Waters P., Zhou H., and Baum M.J. Bilateral damage to the sexually dimorphic medial preoptic area/anterior hypothalamus of male ferrets causes a female-typical preference for and a hypothalamic Fos response to male body odors. Physiol Behav 90 (2007) 438-449
4. Allen L.S., Hines M., Shryne J.E., and Gorski R.A. Two sexually dimorphic cell groups in the human brain. J Neurosci 9 (1989) 497-506
5. Aloisi A.M., Della Seta D., Rendo C., Ceccarelli I., Scaramuzzino A., and Farabollini F. Exposure to the estrogenic pollutant bisphenol A affects pain behavior induced by subcutaneous formalin injection in male and female rats. Brain Res 937 1-2 (2002) 1-7
6. Amateau S.K., and McCarthy M.M. Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior. Nat Neurosci 7 (2004) 643-650
7. Arnold A.P., and Breedlove S.M. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 19 (1985) 469-498
8. Bakker J., Brand T., van Ophemert J., and Slob A.K. Hormonal regulation of adult partner preference behavior in neonatally ATD-treated male rats. Behav Neurosci 107 (1993) 480-487
9. Bakker J., Honda S., Harada N., and Balthazart J. Restoration of male sexual behavior by adult exogenous estrogens in male aromatase knockout mice. Horm Behav 46 (2004) 1-10
10. Barkhem T., Nilsson S., and Gustafsson J.A. Molecular mechanisms, physiological consequences and pharmacological implications of estrogen receptor action. Am J Pharmacogenom 4 (2004) 19-28
11. Baum M.J., Carroll R.S., Cherry J.A., and Tobet S.A. Steroidal control of behavioural, neuroendocrine, and brain sexual differentiation: studies on a carnivore, the ferret. J Neuroendocrinol 2 (1990) 401-418
12. Baum M.J., Erskine M.S., Kornberg E., and Weaver C.E. Prenatal and neonatal testosterone exposure interacts to affect differentiation of sexual behavior and partner preference in female ferrets. Behav Neurosci 104 (1990) 183-198
13. Baum M.J. Mammalian animal models of psychosexual differentiation: when is "translation" to the human situation possible?. Horm Behav 50 (2006) 579-588
14. Berglund H., Lindstrom P., and Savic I. Brain response to putative pheromones in lesbian women. Proc Natl Acad Sci USA 103 (2006) 8269-8274
15. Berman K.F., Schmidt P.J., Rubinow D.R., Danaceau M.A., Van Horn J.D., Esposito G., Ostrem J.L., and Weinberger D.R. Modulation of cognition-specific cortical activity by gonadal steroids: a positron-emission tomography study in women. Proc Natl Acad Sci USA 94 (1997) 8836-8841
16. Bliss T.V., and Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361 (1993) 31-39
17. Bodo C., and Rissman E.F. Androgen receptor is essential for sexual differentiation of responses to olfactory cues in mice. Eur J Neurosci 25 (2007) 2182-2190
18. Breedlove S.M., Cooke B.M., and Jordan C.L. The orthodox view of brain sexual differentiation. Brain Behav Evol 54 (1999) 8-14
19. Brinton R.D., and Nilsen J. Effects of estrogen plus progestin on risk of dementia. JAMA 290 (2003) 1706 [author reply 1707-8]
20. Carlson L.E., and Sherwin B.B. Steroid hormones, memory and mood in a healthy elderly population. Psychoneuroendocrinology 23 (1998) 583-603
21. Carr R., Bertasi F., Betancourt A., Bowers S., Gandy B.S., Ryan P., and Willard S. Effect of neonatal rat bisphenol a exposure on performance in the Morris water maze. J Toxicol Environ Health A 66 21 (2003) 2077-2088
22. CERHR. National Toxicology Program Center for the Evaluation of Risks to Human Reproduction. (CERHR) Expert Panel report on the reproductive and developmental toxicity of bisphenol A. 2007. Available at http://cerhr.niehs.nih.gov/chemicals/bisphenol/BPAFinalEPVF112607.pdf.
23. Cherry J.A., and Baum M.J. Effects of lesions of a sexually dimorphic nucleus in the preoptic/anterior hypothalamic area on the expression of androgen- and estrogen-dependent sexual behaviors in male ferrets. Brain Res 522 (1990) 191-203
24. Cooke B., Hegstrom C.D., Villeneuve L.S., and Breedlove S.M. Sexual differentiation of the vertebrate brain: principles and mechanisms. Front Neuroendocrinol 19 (1998) 323-362
25. Cyr M., Thibault C., Morissette M., Landry M., and Di Paolo T. Estrogen-like activity of tamoxifen and raloxifene on NMDA receptor binding and expression of its subunits in rat brain. Neuropsychopharmacology 25 (2001) 242-257
26. Day M., Sung A., Logue S., Bowlby M., and Arias R. Beta estrogen receptor knockout (BERKO) mice present attenuated hippocampal CA1 long-term potentiation and related memory deficits in contextual fear conditioning. Behav Brain Res 164 (2005) 128-131
27. Della Seta D., Minder I., Dessi-Fulgheri F., and Farabollini F. Bisphenol-A exposure during pregnancy and lactation affects maternal behavior in rats. Brain Res Bull 65 3 (2005) 255-260
28. Della Seta D., Minder I., Belloni V., Aloisi A.M., Dessì-Fulgheri F., and Farabollini F. Pubertal exposure to estrogenic chemicals affects behavior in juvenile and adult male rats. Horm Behav 50 2 (2006) 301-307
29. Dessi-Fulgheri F., Porrini S., and Farabollini F. Effects of perinatal exposure to bisphenol A on play behavior of female and male juvenile rats. Environ Health Perspect 110 Suppl. 3 (2002) 403-407
30. Dominguez-Salazar E., Portillo W., Baum M.J., Bakker J., and Paredes R.G. Effect of prenatal androgen receptor antagonist or aromatase inhibitor on sexual behavior, partner preference and neuronal Fos responses to estrous female odors in the rat accessory olfactory system. Physiol Behav 75 (2002) 337-346
31. Ema M., Fujii S., Furukawa M., Kiguchi M., Ikka T., and Harazono A. Rat two-generation reproductive toxicity study of bisphenol A. Reprod Toxicol 15 5 (2001) 505-523
32. EPA. Guidelines for developmental toxicity risk assessment (EPA/600/FR-91/001). Published on December 5, 1991, Federal Register 1991;56(234):63798-63826 www.epa.gov/NCEA/raf/pdfs/devtox.pdf.
33. EPA. Guidelines for neurotoxicity risk assessment (EPA/630/R-95/001F). Published on May 14, 1998, Federal Register 1998;63(93):26926-26954 www.epa.gov/ncea/raf/pdfs/neurotox.pdf.
34. Forger N.G., and Breedlove S.M. Sexual dimorphism in human and canine spinal cord: role of early androgen. Proc Natl Acad Sci 19 (1986) 7527-7531
35. Farabollini F., Porrini S., Della SetaD, Bianchi F., and Dessi-Fulgheri F. Effects of perinatal exposure to bisphenol A on sociosexual behavior of female and male rats. Environ Health Perspect 110 Suppl. 3 (2002) 409-414
36. Farabollini F., Porrini S., and Dessi-Fulgheri F. Perinatal exposure to the estrogenic pollutant bisphenol A affects behavior in male and female rats. Pharmacol Biochem Behav 64 4 (1999) 687-694
37. Fujimoto T., Kubo K., and Aou S. Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats. Brain Res 1068 1 (2006) 49-55
38. Goldstein J.M., and Link B.G. Gender and the expression of schizophrenia. J Psychiatr Res 22 (1988) 141-155
39. Gorski R.A. Sexual differentiation of the brain: a model for drug-induced alterations of the reproductive system. Environ Health Perspect 70 (1986) 163-175
40. Gorski R.A., Gordon J.H., Shryne J.E., and Southam A.M. Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res 148 (1978) 333-346
41. Gould E., Woolley C.S., Frankfurt M., and McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10 (1990) 1286-1291
42. Gray Jr. L.E., Ferrell J.M., and Ostby J.S. Alteration of behavioral sex differentiation by exposure to estrogenic compounds during a critical neonatal period: effects of zearalenone, methoxychlor, and estradiol in hamsters. Toxicol Appl Pharmacol 80 (1985) 127-136
43. Gray Jr. L.E., Ostby J., Ferrell J., Rehnberg G., Linder R., Cooper R., Goldman J., Slott V., and Laskey J. A dose-response analysis of methoxychlor-induced alterations of reproductive development and function in the rat. Fundam Appl Toxicol 12 (1989) 92-108
44. Gray Jr. L.E., and Ostby J. Effects of pesticides and toxic substances on behavioral and morphological reproductive development: endocrine versus nonendocrine mechanisms. Toxicol Ind Health 14 (1998) 159-184
45. Gray Jr. L.E., Ostby J.S., Ferrell J.M., Sigmon E.R., and Goldman J.M. Methoxychlor induces estrogen-like alterations of behavior and the reproductive tract in the female rat and hamster: effects on sex behavior, running wheel activity, and uterine morphology. Toxicol Appl Pharmacol 96 (1988) 525-540
46. Gray Jr. L.E., Wilson V.S., Stoker T., Lambright C., Furr J., Noriega N., Howdeshell K., Ankley G.T., and Guillette L. Adverse effects of environmental antiandrogens and androgens on reproductive development in mammals. Int J Androl 29 (2006) 96-104
47. Gray Jr. L.E. Neonatal chlordecone exposure alters behavioral sex differentiation in female hamsters. Neurotoxicology 3 (1982) 67-79
48. Gruber C.J., Tschugguel W., Schneeberger C., and Huber J.C. Production and actions of estrogens. N Engl J Med 346 (2002) 340-352
49. Hotchkiss A.K., Ostby J.S., Vandenbergh J.G., and Gray Jr. L.E. An environmental antiandrogen, vinclozolin, alters the organization of play behavior. Physiol Behav 79 (2003) 151-156
50. Hotchkiss A.K., Ostby J.S., Vandenburgh J.G., and Gray Jr. L.E. Androgens and environmental antiandrogens affect reproductive development and play behavior in the Sprague-Dawley rat. Environ Health Perspect 110 Suppl. 3 (2002) 435-439
51. Ishido M., Masuo Y., Kunimoto M., Oka S., Morita M., and Bisphenol. A causes hyperactivity in the rat concomitantly with impairment of tyrosine hydroxylase immunoreactivity. J Neurosci Res 76 3 (2004) 423-433
52. Ishido M., Morita M., Oka S., and Masuo Y. Alteration of gene expression of G protein-coupled receptors in endocrine disruptors-caused hyperactive rats. Regul Pept 126 1-2 (2005) 145-153
53. Kawai K., Nozaki T., Nishikata H., Aou S., Takii M., and Kubo C. Aggressive behavior and serum testosterone concentration during the maturation process of male mice: the effects of fetal exposure to bisphenol A. Environ Health Perspect 111 2 (2003) 175-178
54. Kelliher K.R., and Baum M.J. Nares occlusion eliminates heterosexual partner selection without disrupting coitus in ferrets of both sexes. J Neurosci 21 (2001) 5832-5840
55. Kelliher K.R., Chang Y.M., Wersinger S.R., and Baum M.J. Sex difference and testosterone modulation of pheromone-induced Neuronal Fos in the Ferret's main olfactory bulb and hypothalamus. Biol Reprod 59 (1998) 1454-1463
56. Kindon H.A., Baum M.J., and Paredes R.J. Medial preoptic/anterior hypothalamic lesions induce a female-typical profile of sexual partner preference in male ferrets. Horm Behav 30 (1996) 514-527
57. Kubo K., Arai O., Ogata R., Omura M., Hori T., and Aou S. Exposure to bisphenol A during the fetal and suckling periods disrupts sexual differentiation of the locus coeruleus and of behavior in the rat. Neurosci Lett 304 1-2 (2001) 73-76
58. Kubo K., Arai O., Omura M., Watanabe R., Ogata R., and Aou S. Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neurosci Res 45 3 (2003) 345-356
59. Kurebayashi H., Nagatsuka S.I., Nemoto H., Noguchi H., and Ohno Y. Disposition of low doses of 14C-bisphenol A in male, female, pregnant, fetal, and neonatal rats. Arch Toxicol 79 (2005) 243-252
60. Kwon S., Stedman D.B., Elswick B.A., Cattley R.C., and Welsch F. Pubertal development and reproductive functions of Crl:CD BR Sprague-Dawley rats exposed to bisphenol A during prenatal and postnatal development. Toxicol Sci 55 2 (2000) 399-406
61. Laviola G., Gioiosa L., Adriani W., and Palanza P. D-amphetamine-related reinforcing effects are reduced in mice exposed prenatally to estrogenic endocrine disruptors. Brain Res Bull 65 3 (2005) 235-240
62. Lee S.J., Campomanes C.R., Sikat P.T., Greenfield A.T., Allen P.B., and McEwen B.S. Estrogen induces phosphorylation of cyclic AMP response element binding (pCREB) in primary hippocampal cells in a time-dependent manner. Neuroscience 124 (2004) 549-560
63. LeVay S. A difference in hypothalamic structure between heterosexual and homosexual men. Science 253 (1991) 1034-1037
64. Li C., Brake W.G., Romeo R.D., Dunlop J.C., Gordon M., Buzescu R., Magarinos A.M., Allen P.B., Greengard P., Luine V., and McEwen B.S. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. Proc Natl Acad Sci USA 101 (2004) 2185-2190
65. Maggi A., Ciana P., Belcredito S., and Vegeto E. Estrogens in the nervous system: mechanisms and nonreproductive functions. Ann Rev Physiol 66 (2004) 291-313
66. Maki P.M., Rich J.B., and Rosenbaum R.S. Implicit memory varies across the menstrual cycle: estrogen effects in young women. Neuropsychologia 40 (2002) 518-529
67. Masuo Y., Ishido M., Morita M., and Oka S. Effects of neonatal treatment with 6-hydroxydopamine and endocrine disruptors on motor activity and gene expression in rats. Neural Plast 11 1-2 (2004) 59-76
68. Masuo Y., Morita M., Oka S., and Ishido M. Motor hyperactivity caused by a deficit in dopaminergic neurons and the effects of endocrine disruptors: a study inspired by the physiological roles of PACAP in the brain. Regul Pept 123 1-3 (2004) 225-234
69. McEwen B. Estrogen actions throughout the brain. Recent Prog Horm Res 57 (2002) 357-384
70. Milner T.A., Ayoola K., Drake C.T., Herrick S.P., Tabori N.E., McEwen B.S., Warrier S., and Alves S.E. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol 491 (2005) 81-95
71. Mizuo K., Narita M., Miyagawa K., Okuno E., and Suzuki T. Prenatal and neonatal exposure to bisphenol-A affects the morphine-induced rewarding effect and hyperlocomotion in mice. Neurosci Lett 356 2 (2004) 95-98
72. Munn SJ, Allanou R, Aschberger K, Berthault F, De Bruijn J, Musset C, O'Connor S, Pakalin S, Pellegrini G, Scheer S, Vegra S. Bisphenol-A. European Union Risk Assessment Report. vol. 37, 2003.
73. Nagao T., Saito Y., Usumi K., Kuwagata M., and Imai K. Reproductive function in rats exposed neonatally to bisphenol A and estradiol benzoate. Reprod Toxicol 13 4 (1999) 303-311
74. Narita M., Miyagawa K., Mizuo K., Yoshida T., and Suzuki T. Prenatal and neonatal exposure to low-dose of bisphenol-A enhance the morphine-induced hyperlocomotion and rewarding effect. Neurosci Lett (2006)
75. Negishi T., Kawasaki K., Suzaki S., Maeda H., Ishii Y., Kyuwa S., Kuroda Y., and Yoshikawa Y. Behavioral alterations in response to fear-provoking stimuli and tranylcypromine induced by perinatal exposure to bisphenol A and nonylphenol in male rats. Environ Health Perspect 112 11 (2004) 1159-1164
76. Negishi T., Kawasaki K., Takatori A., Ishii Y., Kyuwa S., Kuroda Y., and Yoshikawa Y. Effects of perinatal exposure to bisphenol A on the behavior of offspring in F344 rats. Environ Toxicol Pharmacol 14 (2003) 99-108
77. Palanza P.L., Howdeshell K.L., Parmigiani S., and vom Saal F.S. Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice. Environ Health Perspect 110 Suppl. 3 (2002) 415-422
78. Paredes R.G., and Baum M.J. Altered sexual partner preference in male ferrets given excitotoxic lesions of thepreoptic area/anterior hypothalamus. J Neurosci 15 (1995) 6619-6630
79. Paredes R.G., Tzschentke T., and Nakach N. Lesions of the medial preoptic area/anterior hypothalamus (MPOA/AH) modify partner preference in male rats. Brain Res 813 (1998) 1-8
80. Patisaul H.B., Fortino A.E., and Polston E.K. Neonatal genistein or bisphenol-A exposure alters sexual differentiation of the AVPV. Neurotoxicol Teratol 28 1 (2006) 111-118
81. Pellis S.M., and Pellis V.C. The prejuvenile onset of play fighting in laboratory rats (Rattus norvegicus). Dev Psychobiol 31 (1997) 193-205
82. Pfaff D.W., Vasudevan N., Kia H.K., Zhu Y.S., Chan J., Garey J., Morgan M., and Ogawa S. Estrogens, brain and behavior: studies in fundamental neurobiology and observations related to women's health. J Steroid Biochem Mol Biol 74 (2000) 365-373
83. Phillips S.M., and Sherwin B.B. Variations in memory function and sex steroid hormones across the menstrual cycle. Psychoneuroendocrinology 17 (1992) 497-506
84. Phillips S.M., and Sherwin B.B. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology 17 (1992) 485-495
85. Porrini S., Belloni V., Della SetaD, Farabollini F., Giannelli G., and Dessi-Fulgheri F. Early exposure to a low dose of bisphenol A affects socio-sexual behavior of juvenile female rats. Brain Res Bull 65 3 (2005) 261-266
86. Pottenger L.H., Domoradzki J.Y., Markham D.A., Hansen S.C., Cagen S.Z., and Waechter Jr. J.M. The relative bioavailability and metabolism of bisphenol A in rats is dependent upon the route of administration. Toxicol Sci 54 1 (2000) 3-18
87. Rao M.L., and Kolsch H. Effects of estrogen on brain development and neuroprotection-implications for negative symptoms in schizophrenia. Psychoneuroendocrinology 28 Suppl. 2 (2003) 83-96
88. Razzoli M., Valsecchi P., and Palanza P. Chronic exposure to low doses bisphenol A interferes with pair-bonding and exploration in female Mongolian gerbils. Brain Res Bull 65 3 (2005) 249-254
89. Rissman E.F., Heck A.L., Leonard J.E., Shupnik M.A., and Gustafsson J.A. Disruption of estrogen receptor beta gene impairs spatial learning in female mice. Proc Natl Acad Sci USA 99 (2002) 3996-4001
90. Rissman E.F., Wersinger S.R., Taylor J.A., and Lubahn D.B. Estrogen receptor function as revealed by knockout studies: neuroendocrine and behavioral aspects. Horm Behav 31 (1997) 232-243
91. Robarts D.W., and Baum M.J. Ventromedial hypothalamic nucleus lesions disrupt olfactory mate recognition and receptivity in female ferrets. Horm Behav 51 (2007) 104-113
92. Rubin B.S., Lenkowski J.R., Schaeberle C.M., Vandenberg L.N., Ronsheim P.M., and Soto A.M. Evidence of altered brain sexual differentiation in mice exposed perinatally to low, environmentally relevant levels of bisphenol A. Endocrinology 147 (2006) 3681-3691
93. Ryan B.C., and Vandenbergh J.G. Developmental exposure to environmental estrogens alters anxiety and spatial memory in female mice. Horm Behav (2006)
94. Sashihara K., Ohgushi A., Ando R., Yamashita T., Takagi R., Nakanishi T., Yoshimatsu T., and Furuse M. Effects of central administration of bisphenol A on behaviors and growth in chicks. J Poult Sci 38 4 (2001) 275-281
95. Sato M., Shimada M., and Sato Y. The effects of prenatal exposure to ethinyl estradiol and bisphenol-A on the developing brain, reproductive organ and behavior of mouse. Congenital Anomalies 41 (2001) 187-193
96. Sato T., Matsumoto T., Kawano H., Watanabe T., Uematsu Y., Sekine K., Fukuda T., Aihara K., Krust A., Yamada T., Nakamichi Y., Yamamoto Y., Nakamura T., Yoshimura K., Yoshizawa T., Metzger D., Chambon P., and Kato S. Brain masculinization requires androgen receptor function. Proc Natl Acad Sci USA 101 (2004) 1673-1678
97. Savic I., Berglund H., Gulyas B., and Roland P. Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans. Neuron 31 (2001) 661-668
98. Savic I., Berglund H., and Lindstrom P. Brain response to putative pheromones in homosexual men. Proc Natl Acad Sci USA 102 (2005) 7356-7361
99. Shima N., Yamaguchi Y., and Yuri K. Distribution of estrogen receptor beta mRNA-containing cells in ovariectomized and estrogen-treated female rat brain. Anat Sci Int 78 (2003) 85-97
100. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388 (1997) 507-525
101. Shughrue P.J., Scrimo P.J., and Merchenthaler I. Estrogen binding and estrogen receptor characterization (ERalpha and ERbeta) in the cholinergic neurons of the rat basal forebrain. Neuroscience 96 (2000) 41-49
102. Smith C.C., and McMahon L.L. Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J Neurosci 26 (2006) 8517-8522
103. Smith C.C., and McMahon L.L. Estrogen-induced increase in the magnitude of long-term potentiation occurs only when the ratio of NMDA transmission to AMPA transmission is increased. J Neurosci 25 (2005) 7780-7791
104. Suzuki T., Mizuo K., Nakazawa H., Funae Y., Fushiki S., Fukushima S., Shirai T., and Narita M. Prenatal and neonatal exposure to bisphenol-A enhances the central dopamine D1 receptor-mediated action in mice: enhancement of the methamphetamine-induced abuse state. Neuroscience 117 3 (2003) 639-644
105. Takagi H., Shibutani M., Masutomi N., Uneyama C., Takahashi N., Mitsumori K., and Hirose M. Lack of maternal dietary exposure effects of bisphenol A and nonylphenol during the critical period for brain sexual differentiation on the reproductive/endocrine systems in later life. Arch Toxicol 78 2 (2004) 97-105
106. Tobet S.A., Zahniser D.J., and Baum M.J. Differentiation in male ferrets of a sexually dimorphic nucleus of the preoptic/anterior hypothalamic area requires prenatal estrogen. Neuroendocrinology 44 (1986) 299-308
107. Toran-Allerand C.D. Estrogen and the brain: beyond ER-alpha and ER-beta. Exp Gerontol 39 (2004) 1579-1586
108. Toran-Allerand C.D. Estrogen and the brain: beyond ER-alpha, ER-beta, and 17beta-estradiol. Ann NY Acad Sci 1052 (2005) 136-144
109. Vega Matuszczyk J.V., and Larsson K. Sexual preference and feminine and masculine sexual behavior of male rats prenatally exposed to antiandrogen or antiestrogen. Horm Behav 29 (1995) 191-206
110. Volkel W., Bittner N., and Dekant W. Quantitation of bisphenol A and bisphenol A glucuronide in biological samples by high performance liquid chromatography-tandem mass spectrometry. Drug Metab Dispos 33 11 (2005) 1748-1757
111. Volkel W., Colnot T., Csanady G.A., Filser J.G., and Dekant W. Metabolism and kinetics of bisphenol a in humans at low doses following oral administration. Chem Res Toxicol 15 10 (2002) 1281-1287
112. Walf A.A., and Frye C.A. ERbeta-selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats. Neuropsychopharmacology 30 (2005) 1598-1609
113. Wersinger S.R., and Baum M.J. Sexually dimorphic processing of somatosensory and chemosensory inputs to forebrain luteinizing hormone-releasing hormone neurons in mated ferrets. Endocrinology 138 (1997) 1121-1129
114. Wersinger S.R., and Rissman E.F. Oestrogen receptor alpha is essential for female-directed chemo-investigatory behaviour but is not required for the pheromone-induced luteinizing hormone surge in male mice. J Neuroendocrinol 12 (2000) 103-110
115. Wersinger S.R., Sannen K., Villalba C., Lubahn D.B., Rissman E.F., and De Vries G.J. Masculine sexual behavior is disrupted in male and female mice lacking a functional estrogen receptor alpha gene. Horm Behav 32 (1997) 176-183
116. Whitlock J.R., Heynen A.J., Shuler M.G., and Bear M.F. Learning induces long-term potentiation in the hippocampus. Science 313 (2006) 1093-1097
117. Whitsett J.M., Gray L.E., and Bediz G.M. Differential influence of stereoisomers of estradiol on sexual behavior of female hamsters. J Comp Physiol Psychol 92 (1978) 7-12
118. Willhite C.C., Ball G.L., and McLellan C.J. Derivation of a bisphenol A oral reference dose (RfD) and drinking-water equivalent concentration. J Tox Env Health, Part B 11 (2000) 69-146
119. Wisniewski A.B., Migeon C.J., Meyer-Bahlburg H.F., Gearhart J.P., Berkovitz G.D., Brown T.R., and Money J. Complete androgen insensitivity syndrome: long-term medical, surgical, and psychosexual outcome. J Clin Endocrinol Metab 85 (2000) 2664-2669
120. Woolley C.S., Gould E., Frankfurt M., and McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10 (1990) 4035-4039
121. Woolley C.S., and McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12 (1992) 2549-2554
122. Woolley C.S., and 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 336 (1993) 293-306
123. Woolley C.S. Acute effects of estrogen on neuronal physiology. Ann Rev Pharmacol Toxicol 47 (2007) 657-680
124. Xu J., and Forger N.G. Expression and androgen regulation of the ciliary neurotrophic factor receptor (CNTFRalpha) in muscles and spinal cord. J Neurobiol 35 May (2) (1998) 217-225
125. Xu X., Liu Y., Sadamatsu M., Tsutsumi S., Akaike M., Ushijima H., and Kato N. Perinatal bisphenol A affects the behavior and SRC-1 expression o f male pups but does not influence on the thyroid hormone receptors and its responsive gene. Neurosci Res (2007) 10.1016/j.neures.2007.02.011
126. Yaffe K., Lui L.Y., Grady D., Cauley J., Kramer J., and Cummings S.R. Cognitive decline in women in relation to non-protein-bound oestradiol concentrations. Lancet 356 (2000) 708-712
127. Yue X., Lu M., Lancaster T., Cao P., Honda S., Staufenbiel M., Harada N., Zhong Z., Shen Y., and Li R. Brain estrogen deficiency accelerates Abeta plaque formation in an Alzheimer's disease animal model. Proc Natl Acad Sci USA 102 (2005) 19198-19203
128. Zhou Y., Watters J.J., and Dorsa D.M. Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain. Endocrinology 137 (1996) 2163-2166
129. Zucker K.J., Bradley S.J., Oliver G., Blake J., Fleming S., and Hood J. Psychosexual development of women with congenital adrenal hyperplasia. Horm Behav 30 (1996) 300-318