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Cited by 236Sexual Differentiation and DisordersGenetic and Clinical Aspects of Sex Determination and Chromosomal AbnormalitiesNeuroendocrine regulation and behavior

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The role of androgen receptors in the masculinization of brain and behavior: What we've learned from the testicular feminization mutation

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Zuloaga, Damian G., Puts, David A., Jordan, Cynthia L., Breedlove, S. Marc·2008·Hormones and Behavior
DOI 10.1016/j.yhbeh.2008.01.013PMC PMC2706155
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Abstract

Many studies demonstrate that exposure to testicular steroids such as testosterone early in life masculinizes the developing brain, leading to permanent changes in behavior. Traditionally, masculinization of the rodent brain is believed to depend on estrogen receptors (ERs) and not androgen receptors (ARs). According to the aromatization hypothesis, circulating testosterone from the testes is converted locally in the brain by aromatase to estrogens, which then activate ERs to masculinize the brain. However, an emerging body of evidence indicates that the aromatization hypothesis cannot fully account for sex differences in brain morphology and behavior, and that androgens acting on ARs also play a role. The testicular feminization mutation (Tfm) in rodents, which produces a nonfunctional AR protein, provides an excellent model to probe the role of ARs in the development of brain and behavior. Tfm rodent models indicate that ARs are normally involved in the masculinization of many sexually dimorphic brain regions and a variety of behaviors, including sexual behaviors, stress response and cognitive processing. We review the role of ARs in the development of the brain and behavior, with an emphasis on what has been learned from Tfm rodents as well as from related mutations in humans causing complete androgen insensitivity.

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Research works printed but not linked: 121

  1. Almeida, 2004, One year follow-up study of the association between chemical castration, sex hormones, beta-amyloid, memory and depression in men, Psychoneuroendocrinology, 29, 1071, 10.1016/j.psyneuen.2003.11.002 · DOI
  2. Astur, 1998, A characterization of performance by men and women in a virtual Morris water task: A large and reliable sex difference, Behav. Brain Res., 93, 185, 10.1016/S0166-4328(98)00019-9 · DOI
  3. Attardi, 1976, Androgen and estrogen receptors in brain cytosol from male, female, and testicular feminized (Tfm/y hermaphrodite) mice, Endocrinology, 98, 864, 10.1210/endo-98-4-864 · DOI
  4. Ayub, 1987, Inhibition of rat testicular 17 alpha-hydroxylase and 17,20-lyase activities by anti-androgens (flutamide, hydroxyflutamide, RU23908, cyproterone acetate) in vitro, J. Steroid Biochem., 28, 43, 10.1016/0022-4731(87)90122-1 · DOI
  5. Beach, 1977, Male rats with inherited insensitivity to androgen show reduced sexual behavior, Endocrinology, 100, 197, 10.1210/endo-100-1-197 · DOI
  6. Bing, 1998, High doses of testosterone increase anticonflict behaviour in rat, Eur. Neuropsychopharmacol., 8, 321, 10.1016/S0924-977X(97)00095-3 · DOI
  7. Bloch, 1988, Estrogen/progesterone treatment in adulthood affects the size of several components of the medial preoptic area in the male rat, J. Comp. Neurol., 275, 613, 10.1002/cne.902750409 · DOI
  8. Bodo, 2007, Androgen receptor is essential for sexual differentiation of responses to olfactory cues in mice, Eur. J. Neurosci., 25, 2182, 10.1111/j.1460-9568.2007.05484.x · DOI
  9. Breedlove, 1980, Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord, Science, 210, 564, 10.1126/science.7423210 · DOI
  10. Breedlove, 1981, Sexually dimorphic motor nucleus in the rat lumbar spinal cord: response to adult hormone manipulation, absence in androgen-insensitive rats, Brain Res., 225, 297, 10.1016/0006-8993(81)90837-4 · DOI
  11. Bridges, 2004, Sex differences in Mongolian gerbils in four tests of anxiety, Physiol. Behav., 83, 119, 10.1016/j.physbeh.2004.08.002 · DOI
  12. Burge, 1971, The adrenal gland and the pre and post castrational aggressive behavior of male mice, Physiol. Behav., 7, 885, 10.1016/0031-9384(71)90058-8 · DOI
  13. Charest, 1991, A frameshift mutation destabilizes androgen receptor messenger RNA in the Tfm mouse, Mol. Endocrinol., 5, 573, 10.1210/mend-5-4-573 · DOI
  14. Cooke, 1999, A brain sexual dimorphism controlled by adult circulating androgens, Proc. Natl. Acad. Sci. U. S. A., 96, 7538, 10.1073/pnas.96.13.7538 · DOI
  15. Cooke, 2003, Both estrogen receptors and androgen receptors contribute to testosterone-induced changes in the morphology of the medial amygdala and sexual arousal in male rats, Horm. Behav., 43, 336, 10.1016/S0018-506X(02)00047-8 · DOI
  16. Clos, 1988, Microsomal effects of cyproterone acetate and flutamide in rat testis, Gen. Pharmacol., 19, 393, 10.1016/0306-3623(88)90035-3 · DOI
  17. De Blas, 1990, Effect of postpuberal gonadectomy on cell population of the locus coeruleus in the rat, Med. Sci. Res., 18, 355
  18. De Blas, 1995, Feminization of the rat locus coeruleus: the role of estradiol, Conf. Reprod. Behav., 27
  19. Dohler, 1986, Pre- and postnatal influence of an estrogen antagonist and an androgen antagonist on differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats, Neuroendocrinology, 42, 443, 10.1159/000124484 · DOI
  20. Domínguez-Salazar, 2002, 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, 337, 10.1016/S0031-9384(01)00674-6 · DOI
  21. Drews, 1998, Direct and mediated effects of testosterone: analysis of sex reversed mosaic mice heterozygous for testicular feminization, Cytogenet. Cell Genet., 80, 68, 10.1159/000014959 · DOI
  22. Dugger, 2007, Androgen receptors are required for full masculinization of the ventromedial hypothalamus (VMH) in rats, Horm. Behav., 51, 195, 10.1016/j.yhbeh.2006.10.001 · DOI
  23. Durazzo, 2007, Effects of the testicular feminization mutation (Tfm) of the androgen receptor gene on BSTMPM volume and morphology in rats, Neurosci. Lett., 419, 168, 10.1016/j.neulet.2007.04.033 · DOI
  24. Edinger, 2004, Testosterone's analgesic, anxiolytic, and cognitive-enhancing effects may be due in part to actions of its 5alpha-reduced metabolites in the hippocampus, Behav. Neurosci., 118, 1352, 10.1037/0735-7044.118.6.1352 · DOI
  25. Finney, 1976, Synergistic effect of estradiol benzoate and dihydrotestosterone on aggression in mice, Horm. Behav., 7, 391, 10.1016/0018-506X(76)90010-6 · DOI
  26. Frye, 2001, Posttraining androgens' enhancement of cognitive performance is temporally distinct from androgens' increases in affective behavior, Cogn. Affect. Behav. Neurosci., 1, 172, 10.3758/CABN.1.2.172 · DOI
  27. Frye, 2004, Testosterone's metabolism in the hippocampus may mediate its anti-anxiety effects in male rats, Pharmacol. Biochem. Behav., 78, 473, 10.1016/j.pbb.2004.04.019 · DOI
  28. Frye, C.A., Edinger, K., Sumida, K., in press. Androgen Administration to Aged Male Mice Increases Anti-Anxiety Behavior and Enhances Cognitive Performance. Neuropsychopharmacology.
  29. Gandelman, 1980, Gonadal hormones and the induction of intraspecific fighting in mice, Neurosci. Biobehav. Rev., 4, 133, 10.1016/0149-7634(80)90011-1 · DOI
  30. Garcia-Falgueras, 2005, The role of the androgen receptor in CNS masculinization, Brain Res., 1035, 13, 10.1016/j.brainres.2004.11.060 · DOI
  31. Gibbs, 2005, Testosterone and estradiol produce different effects on cognitive performance in male rats, Horm. Behav., 48, 268, 10.1016/j.yhbeh.2005.03.005 · DOI
  32. Goldstein, 1972, Studies on the pathogenesis of the pseudohermaphroditism in the mouse with testicular feminization, J. Clin. Invest., 51, 1647, 10.1172/JCI106966 · DOI
  33. Gorski, 1978, Evidence for a morphological sex difference within the medial preoptic area of the rat brain, Brain Res., 148, 333, 10.1016/0006-8993(78)90723-0 · DOI
  34. Gorski, 1980, Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat, J. Comp. Neurol., 193, 529, 10.1002/cne.901930214 · DOI
  35. Grumbach, 1999, Estrogen: consequences and implications of human mutations in synthesis and action, J. Clin. Endocrinol. Metab., 84, 4677, 10.1210/jc.84.12.4677 · DOI
  36. Guillamon, 1988, Effects of sex steroids on the development of the locus coeruleus in the rat, Brain Res., 468, 306, 10.1016/0165-3806(88)90143-5 · DOI
  37. Guillamon, 1988, Early effects of gonadal steroids on the neuron number in the medial posterior region and the lateral division of the bed nucleus of the stria terminalis in the rat, Brain Res. Dev. Brain Res., 44, 281, 10.1016/0165-3806(88)90226-X · DOI
  38. Hajszan, T., MacLusky, N.J., Leranth, C., 2008. Role of Androgens and the Androgen Receptor in Remodeling of Spine Synapses in Limbic Brain Areas. Horm. Behav. (this issue). · DOI
  39. Hamson, 2005, Mating behavior and CNS morphology in rats carrying the testicular feminization mutation, Soc. Neurosci.
  40. Hamson, 2006, Patterns of ultrasonic vocalization in androgen-insensitive XY rats compared with normal males and females, Soc. Neurosci.
  41. Handa, 1994, Gonadal steroid hormone receptors and sex differences in the hypothalamo–pituitary–adrenal axis, Horm. Behav., 28, 464, 10.1006/hbeh.1994.1044 · DOI · Paper page
  42. Harding, 2003, Effects of testosterone in the VMN on copulation, partner preference, and vocalizations in male rats, Horm. Behav., 43, 327, 10.1016/S0018-506X(02)00049-1 · DOI
  43. Harding, 2004, Androgen receptor blockade in the MPOA or VMN: effects on male sociosexual behaviors, Physiol. Behav., 81, 671, 10.1016/j.physbeh.2004.03.008 · DOI
  44. He, 1991, A frame-shift mutation in the androgen receptor gene causes complete androgen insensitivity in the testicular-feminized mouse, Nucleic Acids Res., 19, 2373, 10.1093/nar/19.9.2373 · DOI
  45. Hines, 1992, Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat, Brain Res., 579, 321, 10.1016/0006-8993(92)90068-K · DOI · Paper page
  46. Holman, 1991, Differential effects of neonatal castration on the development of sexually dimorphic brain areas in the gerbil, Brain Res. Dev. Brain Res., 61, 147, 10.1016/0165-3806(91)90125-3 · DOI
  47. Imperato-McGinley, 1982, Hormonal evaluation of a large kindred with complete androgen insensitivity: evidence for secondary 5 alpha-reductase deficiency, J. Clin. Endocrinol. Metab., 54, 931, 10.1210/jcem-54-5-931 · DOI
  48. Imperato-McGinley, 1991, Cognitive abilities in androgen-insensitive subjects: comparison with control males and females from the same kindred, Clin. Endocrinol., 34, 341, 10.1111/j.1365-2265.1991.tb00303.x · DOI
  49. Imwalle, 2005, Lack of functional estrogen receptor beta influences anxiety behavior and serotonin content in female mice, Physiol. Behav., 84, 157, 10.1016/j.physbeh.2004.11.002 · DOI
  50. Isgor, 1998, Prenatal gonadal steroids affect adult spatial behavior, CA1 and CA3 pyramidal cell morphology in rats, Horm. Behav., 34, 183, 10.1006/hbeh.1998.1477 · DOI
  51. Isgor, 2003, Effects of neonatal gonadal steroids on adult CA3 pyramidal neuron dendritic morphology and spatial memory in rats, J. Neurobiol., 55, 179, 10.1002/neu.10200 · DOI
  52. Jones, 2003, Altered circulating hormone levels, endothelial function and vascular reactivity in the testicular feminised mouse, Eur. J. Endocrinol., 148, 111, 10.1530/eje.0.1480111 · DOI
  53. Joseph, 1978, Effects of hormone manipulations and exploration on sex differences in maze learning, Behav. Biol., 24, 364, 10.1016/S0091-6773(79)90223-2 · DOI
  54. Juntti, S.A., Coats, J.K., Shah, N.M., 2008. A genetic approach to dissect sexually dimorphic behaviours. Horm. Behav. (this issue). · DOI
  55. Kessler, 1994, Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Results from the National Comorbidity Survey, Arch. Gen. Psychiatry, 51, 8, 10.1001/archpsyc.1994.03950010008002 · DOI · Paper page
  56. Kuiper, 1998, Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta, Endocrinology, 139, 4252, 10.1210/en.139.10.4252 · DOI · Paper page
  57. Leranth, 2003, Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats, J. Neurosci., 23, 1588, 10.1523/JNEUROSCI.23-05-01588.2003 · DOI
  58. Leranth, 2004, Androgens increase spine synapse density in the CA1 hippocampal subfield of ovariectomized female rats, J. Neurosci., 24, 495, 10.1523/JNEUROSCI.4516-03.2004 · DOI
  59. Lisciotto, 1994, Sex differences in the distribution and projections of testosterone target neurons in the medial preoptic area and the bed nucleus of the stria terminalis of rats, Horm. Behav., 28, 492, 10.1006/hbeh.1994.1047 · DOI
  60. Lund, 2004, Dihydrotestosterone may inhibit hypothalamo–pituitary–adrenal activity by acting through estrogen receptor in the male mouse, Neurosci. Lett., 365, 43, 10.1016/j.neulet.2004.04.035 · DOI
  61. Lund, 2006, The androgen 5alpha-dihydrotestosterone and its metabolite 5alpha-androstan-3beta, 17beta-diol inhibit the hypothalamo–pituitary–adrenal response to stress by acting through estrogen receptor beta-expressing neurons in the hypothalamus, J. Neurosci., 26, 1448, 10.1523/JNEUROSCI.3777-05.2006 · DOI · Paper page
  62. Luttge, 1973, Androgen-induced agonistic behavior in castrate male Swiss–Webster mice: comparison of four naturally occurring androgens, Behav. Biol., 8, 725, 10.1016/S0091-6773(73)80114-2 · DOI
  63. MacLusky, 2004, Effects of dehydroepiandrosterone and flutamide on hippocampal CA1 spine synapse density in male and female rats: implications for the role of androgens in maintenance of hippocampal structure, Endocrinology, 145, 4154, 10.1210/en.2004-0477 · DOI
  64. MacLusky, 2005, The 17alpha and 17beta isomers of estradiol both induce rapid spine synapse formation in the CA1 hippocampal subfield of ovariectomized female rats, Endocrinology, 146, 287, 10.1210/en.2004-0730 · DOI
  65. MacLusky, 2006, Androgen effects on hippocampal CA1 spine synapse numbers are retained in Tfm male rats with defective androgen receptors, Endocrinology, 147, 2392, 10.1210/en.2005-0673 · DOI
  66. Madeira, 1995, Age and sex do not affect the volume, cell numbers, or cell size of the suprachiasmatic nucleus of the rat: an unbiased stereological study, J. Comp. Neurol., 361, 585, 10.1002/cne.903610404 · DOI
  67. Madeira, 2001, Influence of sex and estrus cycle on the sexual dimorphisms of the hypothalamic ventromedial nucleus: stereological evaluation and Golgi study, J. Comp. Neurol., 432, 329, 10.1002/cne.1106 · DOI
  68. Malsbury, 1994, Neurotrophic effects of testosterone on the medial nucleus of the amygdala in adult male rats, J. Neuroendocrinol., 6, 57, 10.1111/j.1365-2826.1994.tb00555.x · DOI
  69. Matsumoto, 1983, Sex difference in volume of the ventromedial nucleus of the hypothalamus in the rat, Endocrinol. Jpn., 30, 277, 10.1507/endocrj1954.30.277 · DOI
  70. Matsumoto, 2003, Alteration in sex-specific behaviors in male mice lacking the aromatase gene, Neuroendocrinology, 77, 416, 10.1159/000071313 · DOI
  71. Matochik, 1994, Intracranial androgenic activation of male-typical behaviors in house mice: motivation versus performance, Behav. Brain Res., 60, 141, 10.1016/0166-4328(94)90141-4 · DOI
  72. McAbee, 1999, Estrogen, but not androgens, regulates androgen receptor messenger ribonucleic acid expression in the developing male rat forebrain, Endocrinology, 140, 3674, 10.1210/en.140.8.3674 · DOI
  73. McAbee, 1999, Regulation of androgen receptor messenger ribonucleic acid expression in the developing rat forebrain, Endocrinology, 140, 1807, 10.1210/en.140.4.1807 · DOI
  74. McClellan, 2006, Development of the ventromedial nucleus of the hypothalamus, Front. Neuroendocrinol., 27, 193, 10.1016/j.yfrne.2006.02.002 · DOI
  75. Meaney, 1988, The sexual differentiation of social play, Trends Neurosci., 11, 54, 10.1016/0166-2236(88)90164-6 · DOI · Paper page
  76. Meaney, 1983, Sexual differentiation of social play in rat pups is mediated by the neonatal androgen-receptor system, Neuroendocrinology, 37, 85, 10.1159/000123524 · DOI · Paper page
  77. Money, 1968, Fetal feminization induced by androgen insensitivity in the testicular feminizing syndrome: effect on marriage and maternalism, Johns Hopkins Med. J., 123, 105
  78. Monks, 2007, Overexpression of wild-type androgen receptor in muscle recapitulates polyglutamine disease, Proc. Natl. Acad. Sci. U. S. A., 104, 18259, 10.1073/pnas.0705501104 · DOI
  79. Morris, 2005, Partial demasculinization of several brain regions in adult male (XY) rats with a dysfunctional androgen receptor gene, J. Comp. Neurol., 487, 217, 10.1002/cne.20558 · DOI · Paper page
  80. Naftolin, 1975, The formation and metabolism of estrogens in brain tissues, Adv. Biosci.,, 15, 105
  81. Naghdi, 2001, The effects of intrahippocampal testosterone and flutamide on spatial localization in the Morris water maze, Brain Res., 897, 44, 10.1016/S0006-8993(00)03261-3 · DOI
  82. Nomura, 2002, Genotype/age interactions on aggressive behavior in gonadally intact estrogen receptor beta knockout (betaERKO) male mice, Horm. Behav., 41, 288, 10.1006/hbeh.2002.1773 · DOI
  83. Nunez, 2000, Hippocampal anatomy and water maze performance are affected by neonatal cryoanesthesia in rats of both sexes, Horm. Behav., 37, 169, 10.1006/hbeh.2000.1572 · DOI
  84. Ogawa, 1997, Behavioral effects of estrogen receptor gene disruption in male mice, Proc. Natl. Acad. Sci. U. S. A., 94, 1476, 10.1073/pnas.94.4.1476 · DOI
  85. Ogawa, 2000, Abolition of male sexual behaviors in mice lacking estrogen receptors alpha and beta (alpha beta ERKO), Proc. Natl. Acad. Sci. U. S. A., 97, 14737, 10.1073/pnas.250473597 · DOI
  86. Ohno, 1974, Tfm mutation and masculinization versus feminization of the mouse central nervous system, Cell, 3, 235, 10.1016/0092-8674(74)90137-8 · DOI
  87. Olioff, 1978, Sex differences in the play behavior of prepubescent rats, Physiol. Behav., 20, 113, 10.1016/0031-9384(78)90060-4 · DOI · Paper page
  88. Olsen, 1979, Androgen-insensitive rats are defeminised by their testes, Nature, 279, 238, 10.1038/279238a0 · DOI · Paper page
  89. Olsen, 1992, Genetic influences on sexual behavior differentiation, 1, 10.1007/978-1-4899-2453-7_1 · DOI · Paper page
  90. Olsen, 1981, Hormonal control of the development of sexual behavior in androgen-insensitive (Tfm) rats, Physiol. Behav., 27, 883, 10.1016/0031-9384(81)90058-5 · DOI · Paper page
  91. Puts, 2006, Defending the brain from estrogen, Nat. Neurosci., 9, 155, 10.1038/nn0206-155 · DOI
  92. Puts, D.A., McDaniel, M.A., Jordan, C.L., Breedlove, S.M., in press. Spatial ability and prenatal androgens: Meta-analyses of congenital adrenal hyperplasia and digit ratio (2D:4D) studies. Archives of Sexual Behavior (Special Issue).
  93. Rizk, 2005, Behavioral performance of Tfm mice supports the beneficial role of androgen receptors in spatial learning and memory, Brain Res., 1034, 132, 10.1016/j.brainres.2004.12.002 · DOI
  94. Rizk-Jackson, 2006, Effects of sex on object recognition and spatial navigation in humans, Behav. Brain Res., 173, 181, 10.1016/j.bbr.2006.06.029 · DOI
  95. Robinson, 1986, Sex differences in the shape of the sexually dimorphic nucleus of the preoptic area and suprachiasmatic nucleus of the rat: 3-D computer reconstructions and morphometrics, Brain Res., 371, 380, 10.1016/0006-8993(86)90380-X · DOI
  96. Roof, 1993, Neonatal exogenous testosterone modifies sex difference in radial arm and Morris water maze performance in prepubescent and adult rats, Behav. Brain Res., 53, 1, 10.1016/S0166-4328(05)80261-X · DOI
  97. Roselli, 1991, Sex-differences in androgen receptors and aromatase-activity in microdissected regions of the rat-brain, Endocrinology, 128, 1310, 10.1210/endo-128-3-1310 · DOI · Paper page
  98. Roselli, 1987, Genetic evidence for androgen-dependent and independent control of aromatase activity in the rat brain, Endocrinology, 121, 2205, 10.1210/endo-121-6-2205 · DOI
  99. Rosenfeld, 1977, Central aromatization of testosterone in testicular feminized mice, Experientia, 33, 1392, 10.1007/BF01920200 · DOI
  100. Salomé, 2004, Neurobiological correlates of high (HAB) versus low anxiety-related behavior (LAB): differential Fos expression in HAB and LAB rats, Biol. Psychiatry, 55, 715, 10.1016/j.biopsych.2003.10.021 · DOI
  101. Sandstrom, 2006, Testosterone modulates performance on a spatial working memory task in male rats, Horm. Behav., 50, 18, 10.1016/j.yhbeh.2005.09.008 · DOI
  102. Scordalakes, 2004, Aggression and arginine vasopressin immunoreactivity regulation by androgen receptor and estrogen receptor alpha, Genes Brain Behav., 3, 20, 10.1111/j.1601-183X.2004.00036.x · DOI
  103. Sengelaub, D.R., Forger, N.G., 2008. The spinal nucleus of the bulbocavernosus: Firsts in androgen-dependent neural sex differences. Horm. Behav. (this issue). · DOI
  104. Shapiro, 1976, Is feminine differentiation of the brain hormonally determined?, Experientia, 32, 650, 10.1007/BF01990214 · DOI
  105. Swaab, 1985, The vasopressin containing neurons in the human brain; changes during ageing and senile dementia, Br. J. Clin. Pract. Suppl., 39, 7
  106. Swaab, 1990, An enlarged suprachiasmatic nucleus in homosexual men, Brain Res.,, 537, 141, 10.1016/0006-8993(90)90350-K · DOI
  107. Swaab, 1994, Development of vasoactive intestinal polypeptide neurons in the human suprachiasmatic nucleus in relation to birth and sex, Brain Res. Dev. Brain Res., 79, 249, 10.1016/0165-3806(94)90129-5 · DOI · Paper page
  108. Swartz, 1974, The lack of estrogen binding by human alpha fetoprotein, J. Clin. Endocrinol. Metab., 39, 589, 10.1210/jcem-39-3-589 · DOI
  109. Tabibnia, 1999, Sex difference and laterality in the volume of mouse dentate gyrus granule cell layer, Brain Res., 827, 41, 10.1016/S0006-8993(99)01262-7 · DOI
  110. Thor, 1984, Social play in juvenile rats: a decade of methodological and experimental research, Neurosci. Biobehav. Rev., 8, 455, 10.1016/0149-7634(84)90004-6 · DOI · Paper page
  111. Vague, 1983, Testicular feminization syndrome. An experimental model for the study of hormone action on sexual behavior, Horm. Res., 18, 62, 10.1159/000179779 · DOI
  112. Vreeburg, 1977, Prevention of central defeminization but not masculinization in male rats by inhibition neonatally of oestrogen biosynthesis, J. Endocrinol., 74, 375, 10.1677/joe.0.0740375 · DOI
  113. Walf, 2005, Antianxiety and antidepressive behavior produced by physiological estradiol regimen may be modulated by hypothalamic–pituitary–adrenal axis activity, Neuropsychopharmacology, 30, 1288, 10.1038/sj.npp.1300708 · DOI
  114. Walf, 2006, Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats, Neurobiol. Learn. Mem., 86, 35, 10.1016/j.nlm.2006.01.004 · DOI
  115. Weinstock, 1999, Gender differences in the presentation and management of social anxiety disorder, J. Clin. Psychiatry, 60, 9
  116. Williams, 1991, The organizational effects of gonadal steroids on sexually dimorphic spatial ability, Psychoneuroendocrinology, 16, 155, 10.1016/0306-4530(91)90076-6 · DOI
  117. Williams, 1990, Organizational effects of early gonadal secretions on sexual differentiation in spatial memory, Behav. Neurosci., 104, 84, 10.1037/0735-7044.104.1.84 · DOI
  118. Wimer, 1984, The sex dimorphisms in the granule cell layer of the hippocampus in house mice, Brain Res., 328, 105, 10.1016/0006-8993(85)91328-9 · DOI
  119. Wimer, 1989, On the sources of strain and sex differences in granule cell number in the dentate area of house mice, Dev. Brain Res., 48, 167, 10.1016/0165-3806(89)90073-4 · DOI
  120. Wimer, 1988, On the development of strain and sex differences in granule cell number in the area dentata in house mice, Dev. Brain Res., 42, 191, 10.1016/0165-3806(88)90237-4 · DOI
  121. Yazici, 2003, The effects of hormone replacement therapy in menopause on symptoms of anxiety and depression, Turk. J. Psychiatry, 14, 101

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Metadata

Authors
Zuloaga, D. G., Puts, D. A., Jordan, C. L., & Breedlove, S. M.
Affiliations
  • Michigan State University (US)
  • Pennsylvania State University (US)
Corresponding author
Zuloaga, Damian G.
ORCID
Venue
Hormones and Behavior
Publisher
Elsevier BV
Published
2008-05
Volume
53
Issue
5
Pages
613-626
ISSN
0018-506X (ISSN-L)
DOI
10.1016/j.yhbeh.2008.01.013
PMC
PMC2706155
OpenAlex
W1990168204
Cited by
236
References
0
Citations by year
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FWCI
6.99
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Hormones and Behavior (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health
  • National Institute of Mental Health (F31MH078273, F31 MH78273)
  • National Institute of Neurological Disorders and Stroke (R01NS028421, R01-NS28421, R01NS045195)
Topics
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Sexual Differentiation and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Keywords
androgen receptor, aromatase, estrogen receptor, sex differences in brain, sexual behavior, stress response, cognitive processes, androgen insensitivity syndrome, brain development
MeSH terms
Aggression, Animals, Behavior, Animal, Brain, Female, Feminization, Humans, Male, Mutation, Receptors, Androgen, Sex Differentiation, Social Behavior

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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