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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
Open accessAbstract
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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“Together, the coordinated actions of both androgens and estrogens are necessary for complete masculinization of the brain and behavior in rodents (McCarthy, 2008; Zuloaga et al., 2008).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Zuloaga et al., 2008
Citations
Cites
Sexual differentiation of the vertebrate nervous system
Morris, J. A., Jordan, C. L., & Breedlove, S. M. (2004) · Nature Neuroscience · doi:10.1038/nn1325 · Cited by 627
Self-citationJonasson, Z. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.10.006 · Cited by 498
Novel Actions of Estrogen Receptor-β on Anxiety-Related Behaviors
Lund, T. D., Rovis, T., Chung, W. C. J., & Handa, R. J. (2005) · Endocrinology · doi:10.1210/en.2004-1158 · Cited by 436 · cited 4×
“…also play a role in the display of anxietyrelated behavior in rodents as assessed by open field testing, exposure to a novel object, the elevated plus maze task, and light dark box (Edinger and Frye, 2004; Walf and Frye, 2005; Lund et al., 2005; Bridges and Starkey, 2004; Frye and Lacey, 2001).”
BackgroundInfluentialDe Vries, G. J., & Panzica, G. C. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.050 · Cited by 346
Psychological outcomes and gender-related development in complete androgen insensitivity syndrome
Hines, M., Ahmed, S. F., & Hughes, I. A. (2003) · Archives of Sexual Behavior · doi:10.1023/a:1022492106974 · Cited by 320
Bakker, J., De Mees, C., Douhard, Q., Balthazart, J., Gabant, P., Szpirer, J., & Szpirer, C. (2006) · Nature Neuroscience · doi:10.1038/nn1624 · Cited by 305
Brain masculinization requires androgen receptor function
Sato, T., Matsumoto, T., Kawano, H., Watanabe, T., Uematsu, Y., Sekine, K., Fukuda, T., Aihara, K.-I., Krust, A., Yamada, T., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305303101 · Cited by 303
Pellis, S. M., & Pellis, V. C. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230303 · Cited by 255
Handa, R. J., Pak, T. R., Kudwa, A. E., Lund, T. D., & Hinds, L. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.09.012 · Cited by 205
Yarbrough, W. G., Quarmby, V. E., Simental, J. A., Joseph, D. R., Sar, M., Lubahn, D. B., Olsen, K. L., French, F. S., & Wilson, E. M. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)38972-0 · Cited by 199 · cited 3×
“Due to differences in the nature of these mutations, Tfm rats have some residual sensitivity to androgens through ARs, although it is greatly reduced (Yarbrough et al., 1990), while Tfm mice have virtually no sensitivity to androgen through ARs, as in CAIS women (Drews, 1998).”
BackgroundFrye, C. A., & Walf, A. A. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.2.306 · Cited by 172 · cited 1×
“In general, increases in either T or E2 in both male and female rodents are correlated with a decrease in anxiety-related behaviors (Frye and Walf, 2004; Bing et al., 1998; Frye et al., in press).”
BackgroundWang, Z., Bullock, N. A., & De Vries, G. J. (1993) · Endocrinology · doi:10.1210/endo.132.6.8504734 · Cited by 123
Han, T. M., & De Vries, G. J. (2003) · Journal of Neurobiology · doi:10.1002/neu.10157 · Cited by 116
Temporal boundary of the sensitive period for hormonal organization of social play in juvenile rats.
Beatty, W. W., Dodge, A. M., Traylor, K. L., & Meaney, M. J. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90017-2 · Cited by 70 · cited 1×
“Play fighting is decreased inmale rats castrated at birth and its frequency begins to decline at the onset of puberty (Beatty et al., 1981; Meaney, 1988; Pellis and Pellis, 1990).”
BackgroundSpatial memory performance in androgen insensitive male rats
JONES, B., & WATSON, N. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.03.023 · Cited by 57
Field, E. F., Whishaw, I. Q., Pellis, S. M., & Watson, N. V. (2006) · Developmental Psychobiology · doi:10.1002/dev.20121 · Cited by 30 · cited 4×
“, 1983; Meaney, 1988), although recent data suggest that this difference may depend on the testing paradigm (Field et al., 2006).”
BackgroundInfluentialEstrogen binds to hypothalamic nuclei of androgen-insensitive (tfm) rats
Olsen, K. L., & Whalen, R. E. (1982) · Experientia · doi:10.1007/bf01944575 · Cited by 17
Research works printed but not linked: 121
- 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
- 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
- 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
- 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
- Beach, 1977, Male rats with inherited insensitivity to androgen show reduced sexual behavior, Endocrinology, 100, 197, 10.1210/endo-100-1-197 · DOI
- Bing, 1998, High doses of testosterone increase anticonflict behaviour in rat, Eur. Neuropsychopharmacol., 8, 321, 10.1016/S0924-977X(97)00095-3 · DOI
- 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
- 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
- Breedlove, 1980, Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord, Science, 210, 564, 10.1126/science.7423210 · DOI
- 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
- Bridges, 2004, Sex differences in Mongolian gerbils in four tests of anxiety, Physiol. Behav., 83, 119, 10.1016/j.physbeh.2004.08.002 · DOI
- 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
- 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
- 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
- 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
- Clos, 1988, Microsomal effects of cyproterone acetate and flutamide in rat testis, Gen. Pharmacol., 19, 393, 10.1016/0306-3623(88)90035-3 · DOI
- De Blas, 1990, Effect of postpuberal gonadectomy on cell population of the locus coeruleus in the rat, Med. Sci. Res., 18, 355
- De Blas, 1995, Feminization of the rat locus coeruleus: the role of estradiol, Conf. Reprod. Behav., 27
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Frye, C.A., Edinger, K., Sumida, K., in press. Androgen Administration to Aged Male Mice Increases Anti-Anxiety Behavior and Enhances Cognitive Performance. Neuropsychopharmacology.
- 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
- Garcia-Falgueras, 2005, The role of the androgen receptor in CNS masculinization, Brain Res., 1035, 13, 10.1016/j.brainres.2004.11.060 · DOI
- 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
- Goldstein, 1972, Studies on the pathogenesis of the pseudohermaphroditism in the mouse with testicular feminization, J. Clin. Invest., 51, 1647, 10.1172/JCI106966 · DOI
- 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
- 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
- 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
- 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
- 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
- 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
- Hamson, 2005, Mating behavior and CNS morphology in rats carrying the testicular feminization mutation, Soc. Neurosci.
- Hamson, 2006, Patterns of ultrasonic vocalization in androgen-insensitive XY rats compared with normal males and females, Soc. Neurosci.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Juntti, S.A., Coats, J.K., Shah, N.M., 2008. A genetic approach to dissect sexually dimorphic behaviours. Horm. Behav. (this issue). · DOI
- 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
- Kuiper, 1998, Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta, Endocrinology, 139, 4252, 10.1210/en.139.10.4252 · DOI · Paper page
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Matsumoto, 2003, Alteration in sex-specific behaviors in male mice lacking the aromatase gene, Neuroendocrinology, 77, 416, 10.1159/000071313 · DOI
- 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
- 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
- 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
- McClellan, 2006, Development of the ventromedial nucleus of the hypothalamus, Front. Neuroendocrinol., 27, 193, 10.1016/j.yfrne.2006.02.002 · DOI
- Meaney, 1988, The sexual differentiation of social play, Trends Neurosci., 11, 54, 10.1016/0166-2236(88)90164-6 · DOI · Paper page
- 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
- Money, 1968, Fetal feminization induced by androgen insensitivity in the testicular feminizing syndrome: effect on marriage and maternalism, Johns Hopkins Med. J., 123, 105
- 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
- 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
- Naftolin, 1975, The formation and metabolism of estrogens in brain tissues, Adv. Biosci.,, 15, 105
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Olsen, 1979, Androgen-insensitive rats are defeminised by their testes, Nature, 279, 238, 10.1038/279238a0 · DOI · Paper page
- Olsen, 1992, Genetic influences on sexual behavior differentiation, 1, 10.1007/978-1-4899-2453-7_1 · DOI · Paper page
- 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
- Puts, 2006, Defending the brain from estrogen, Nat. Neurosci., 9, 155, 10.1038/nn0206-155 · DOI
- 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).
- 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
- 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
- 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
- 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
- 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
- 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
- Rosenfeld, 1977, Central aromatization of testosterone in testicular feminized mice, Experientia, 33, 1392, 10.1007/BF01920200 · DOI
- 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
- 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
- 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
- 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
- Shapiro, 1976, Is feminine differentiation of the brain hormonally determined?, Experientia, 32, 650, 10.1007/BF01990214 · DOI
- Swaab, 1985, The vasopressin containing neurons in the human brain; changes during ageing and senile dementia, Br. J. Clin. Pract. Suppl., 39, 7
- Swaab, 1990, An enlarged suprachiasmatic nucleus in homosexual men, Brain Res.,, 537, 141, 10.1016/0006-8993(90)90350-K · DOI
- 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
- Swartz, 1974, The lack of estrogen binding by human alpha fetoprotein, J. Clin. Endocrinol. Metab., 39, 589, 10.1210/jcem-39-3-589 · DOI
- 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
- 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
- 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
- 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
- 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
- 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
- Weinstock, 1999, Gender differences in the presentation and management of social anxiety disorder, J. Clin. Psychiatry, 60, 9
- Williams, 1991, The organizational effects of gonadal steroids on sexually dimorphic spatial ability, Psychoneuroendocrinology, 16, 155, 10.1016/0306-4530(91)90076-6 · DOI
- 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
- 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
- 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
- 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
- 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.
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2008-05
- Volume
- 53
- Issue
- 5
- Pages
- 613-626
- ISSN
- 0018-506X (ISSN-L)
- PMC
- PMC2706155
- OpenAlex
- W1990168204
- Cited by
- 236
- References
- 0
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 10 · 2023: 16 · 2022: 15 · 2021: 10 · 2020: 15 · 2019: 9 · 2018: 9 · 2017: 16 · 2016: 17 · 2015: 18 · 2014: 12 · 2013: 13 · 2012: 12
- FWCI
- 6.99
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- 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
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