Do Sex Differences in the Brain Explain Sex Differences in the Hormonal Induction of Reproductive Behavior? What 25 Years of Research on the Japanese Quail Tells Us
Balthazart, Jacques; Tlemcani, O.; Ball, G. F.
1996 • In Hormones and Behavior, 30 (4), p. 627-61
[en] Early workers interested in the mechanisms mediating sex differences in morphology and behavior assumed that differences in behavior that are commonly observed between males and females result from the sex specificity of androgens and estrogens.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Tlemcani, O.
Ball, G. F.
Language :
English
Title :
Do Sex Differences in the Brain Explain Sex Differences in the Hormonal Induction of Reproductive Behavior? What 25 Years of Research on the Japanese Quail Tells Us
Absil, P., and Balthazart, J. (1994a). Sex difference in the neurotensin-immunoreactive cell populations of the preoptic area in quail (Coturnix japonica). Cell Tissue Res. 276, 99-116.
Absil, P., and Balthazart, J. (1994b). Testosterone effects on neurotensin-immunoreactive cells in the quail preoptic area. Neuroreport 5, 1129-1132.
Absil, P., Das, S., and Balthazart, J. (1994). Effects of apomorphine on sexual behavior in male quail. Pharmacol. Biochem. Behav. 47, 77-88.
Adkins, E. K. (1975). Hormonal basis of sexual differentiation in the Japanese quail. J. Comp. Physiol. Psychol. 89, 61-71.
Adkins, E. K. (1976). Embryonic exposure to an antiestrogen masculinizes behavior of female quail. Physiol. Behav. 17, 357-359.
Adkins, E. K. (1979). Effect of embryonic treatment with estradiol or testosterone on sexual differentiation of the quail brain. Neuroendocrinology 29, 178-185.
Adkins, E. K., and Adler, N. T. (1972). Hormonal control of behavior in the Japanese quail. J. Comp. Physiol. Psychol. 81, 27-36.
Adkins-Regan, E. (1983). Sex steroids and the differentiation and activation of avian reproductive behaviour. In J. Balthazart and R. Gilles (Eds.), Hormones and Behaviour in Higher Vertebrates, pp. 219-228. Springer-Verlag, Berlin.
Adkins-Regan, E., Ottinger, M. A., and Park, J. (1995). Maternal transfer of estradiol to egg yolks alters sexual differentiation of avian offspring. J. Exp. Zool. 271, 466-470.
Allen, L. S., Hines, M., Shryne, J. E., and Gorski, R. A. (1989). Two sexually dimorphic cell groups in the human brain. J. Neurosci. 9, 497-506.
Arendash, G. W., and Gorski, R. A. (1983). Effects of discrete lesions of the sexually dimorphic nucleus of the preoptic area or other medial preoptic regions on the sexual behavior of male rats. Brain Res. Bull. 10, 147-154.
Arnold, A. P. (1992). Developmental plasticity in neural circuits controlling birdsong: Sexual differentiation and the neural basis of learning. J. Neurobiol. 23, 1506-1528.
Arnold, A. P., Bottjer, S. W., Brenowitz, E. A., Nordeen, E. J., and Nordeen, K. W. (1986). Sexual dimorphisms in the neural vocal control system in song birds: Ontogeny and phylogeny. Brain Behav. Evol. 28, 22-31.
Arnold, A. P., and Gorski, R. A. (1984). Gonadal steroid induction of structural sex differences in the central nervous system. Annu. Rev. Neurosci. 7, 413-442.
Arnold, A. P., and Schlinger, B. A. (1993). Sexual differentiation of brain and behavior: The zebra finch is not just a flying rat. Brain Behav. Evol. 42, 231-241.
Aste, N., Panzica, G. C., Viglietti-Panzica, C., and Balthazart, J. (1991). Effects of in ovo estradiol benzoate treatments on sexual behavior and size of neurons in the sexually dimorphic medial preoptic nucleus of Japanese quail. Brain Res. Bull. 27, 713-720.
Aste, N., Panzica, G. C., Aimar, P., Viglietti-Panzica, C., Foidart, A., and Balthazart, J. (1993). Implication of testosterone metabolism in the control of the sexually dimorphic nucleus of the quail preoptic area. Brain Res. Bull. 31, 601-611.
Aste, N., Panzica, G. C., Aimar, P., Viglietti-Panzica, C., Harada, N., Foidart, A., and Balthazart, J. (1994). Morphometric studies demonstrate that aromatase-immunoreactive cells are the main target of androgens and estrogens in the quail medial preoptic nucleus. Exp. Brain Res. 101, 241-252.
Bailhache, T., and Balthazart, J. (1993). The catecholaminergic system of the quail brain: Irnmunocytochemical studies of dopamine β-hydroxylase and tyrosine hydroxylase. J. Comp. Neurol. 329, 230-256.
Ball, J. (1937). Sex activity of castrated male rats increased by estrin administration. J. Comp. Psychol. 24, 135-144.
Ball, G. F. (1994). Neurochemical specializations associated with vocal learning and production in songbirds and budgerigars. Brain Behav. Evol. 44, 234-246.
Ball, G. P., Casto, J. M., and Bernard, D. J. (1994). Sex differences in the volume of avian song control nuclei: Comparative studies and the issue of brain nucleus delineation. Psychoneuroendocrinology 19, 485-504.
Balthazart, J. (1989a). Steroid metabolism and the activation of social behavior. In J. Balthazart (Ed.), Advances in Comparative and Environmental Physiology, Vol. 3, pp. 105-159. Springer-Verlag, Berlin.
Balthazart, J. (1989b). Correlation between the sexually dimorphic aromatase of the preoptic area and sexual behavior in quail: Effects of neonatal manipulatons of the hormonal milieu. Arch. Int. Physiol. Biochem. 97, 465-481.
Balthazart, J. (1996). Steroid control and sexual differentiation of brain aromatase. J. Steroid Biochem. Mol. Biol., in press.
Balthazart, J., and Ball, G. F. (1989). Effects of the noradrenergic neurotoxin DSP-4 on luteinizing hormone levels, catecholamine concentrations, α2-adrenergic receptor binding, and aromatase activity in the brain of the Japanese quail. Brain Res. 492, 163-175.
Balthazart, J., and Ball, G. F. (1995). Sexual differentiation of brain and behavior in birds. Trends Endocrinol. Metab. 6, 21-29.
Balthazart, J., Castagna, C., and Ball, G. F. (1996a). Differential effects of D1 and D2 dopamine receptor agonists and antagonists on appetitive and consummatory aspects of male sexual behavior in Japanese quail. Soc. Neurosci. Abstr., 22, 158.
Balthazart, J., De Clerck, A., and Foidart, A. (1992a). Behavioral demasculinization of female quail is induced by estrogens: Studies with the new aromatase inhibitor, R76713. Horm. Behav. 26, 179-203.
Balthazart, J., Evrard, L., and Surlemont, C. (1990a). Effects of the non-steroidal aromatase inhibitor, R76713 on testosterone-induced sexual behavior in the Japanese quail (Coturnix coturnix japonica). Horm. Behav. 24, 510-531.
Balthazart, J., and Foidart, A. (1993). Brain aromatase and the control of male sexual behavior. J. Steroid Biochem. Mol. Biol. 44, 521-540.
Balthazart, J., Foidart, A., Absil, P., and Harada, N. (1996b). Effects of testosterone and its metabolites on aromatase-immunoreactive cells in the quail brain: Relationship with the activation of male reproductive behavior. J. Steroid Biochem. Mol. Biol. 56, 185-200.
Balthazart, J., Foidart, A., and Harada, N. (1990b). Immunocytochemical localization of aromatase in the brain. Brain Res. 514, 327-333.
Balthazart, J., Foidart, A., and Hendrick, J. C. (1990c). The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior. Physiol. Behav. 47, 83-94.
Balthazart, J., Foidart, A., Sante, P., and Hendrick, J. C. (1992b). Effects of a-methyl-para-tyrosine on monoamine levels in the Japanese quail: Sex differences and testosterone effects. Brain Res. Bull. 28, 275-288.
Balthazart, J., Foidart, A., Surlemont, C., Vockel, A., and Harada, N. (1990d). Distribution of aromatase in the brain of the Japanese quail, ring dove, and zebra finch: An immunocytochemical study. J. Comp. Neurol. 301, 276-288.
Balthazart, J., Foidart, A., Wilson, E. M., and Ball, G. F. (1992c). Immunocytochemical localization of androgen receptors in the male song-bird and quail brain. J. Comp. Neurol. 317, 407-420.
Balthazart, J., Gahr, M., and Surlemont, C. (1989). Distribution of estrogen receptors in the brain of the Japanese quail: An immunocytochemical study. Brain Res. 501, 205-214.
Balthazart, J., Schumacher, M., and Evrard, L. (1990e). Sex differences and steroid control of testosterone-metabolizing enzyme activity in the quail brain. J. Neuroendocrinol. 2, 675-683.
Balthazart, J., Schumacher, M., and Ottinger, M. A. (1983). Sexual differences in the Japanese quail: Behavior, morphology and intracellular metabolism of testosterone. Gen. Comp. Endocrinol. 51, 191-207.
Balthazart, J., Schumacher, M., and Malacarne, G. (1985). Interaction of androgens and estrogens in the control of sexual behavior in male Japanese quail. Physiol. Behav. 35, 157-166.
Balthazart, J., and Surlemont, C. (1990a). Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail POA. Brain Res. Bull. 25, 7-14.
Balthazart, J., and Surlemont, C. (1990b). Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol. Behav. 48, 599-609.
Balthazart, J., Surlemont, C., and Harada, N. (1992d). Aromatase as a cellular marker of testosterone action in the preoptic area. Physiol. Behav. 51, 395-409.
Balthazart, J., Tlemçani, O., and Harada, N. (1996c). Localization of testosterone-sensitive and sexually dimorphic aromatase-immunoreactive cells in the quail preoptic area. J. Chem. Neuroanat., 11, 147-171.
Bass, A. (1992). Dimorphic male brains and alternative reproductive tactics in a vocalizing fish. Trends Neurosci. 15, 139-145.
Baum, M. J., Carroll, R. S., Cherry, J. A., and Tobet, S. A. (1990). Steroidal control of behavioural, neuroendocrine and brain sexual differentiation: Studies in a carnivore, the ferret. J. Neuroendocrinol. 2, 401-418.
Beach, F. (1948). Hormones and Behavior. Hoeber, New York.
Beach, F., and Inman, N. G. (1965). Effects of castration and androgen replacement on mating in male quail. Proc. Natl. Acad. Sci. USA 54, 1426-1431.
Berthold, A. A. (1849). Transplantation der Hoden. Arch. Anat. Physiol. 16, 42-46.
Blaustein, J. D., and Olster, D. H. (1989). Gonadal steroid hormone receptors and social behaviors. In J. Balthazart (Eds.), Advances in Comparative and Environmental Physiology, Vol. 3, pp. 31-104. Springer-Verlag, Berlin.
Breedlove, S. M. (1992). Sexual dimorphism in the vertebrate nervous system. J. Neurosci. 12, 4133-4142.
Breedlove, S. M. (1994). Sexual differentiation of the human nervous system. Annu. Rev. Psychol. 45, 389-418.
Brenowitz, E. A. (1991). Evolution of the vocal control system in the avian brain. Semin. Neurosci. 3, 399-407.
Brown, T. J., Hochberg, R. B., Zielinski, J. E., and MacLusky, N. J. (1988). Regional sex differences in cell nuclear estrogen-binding capacity in the rat hypothalamus and preoptic area. Endocrinology 123, 1761-1770.
Brown, T. J., Naftolin, F., and MacLusky, N. J. (1992). Sex differences in estrogen receptor binding in the rat hypothalamus: Effects of subsaturating pulses of estradiol. Brain Res. 578, 129-134.
Brown, T. J., Yu, J., Gagnon, M., Sharma, M., and MacLusky, N. J. (1996). Sex differences in estrogen receptor and progestin receptor induction in the guinea pig hypothalamus and preoptic area. Brain Res. 725, 37-48.
Castagna, C., and Balthazart, J. (1996). Effects of vasotocin on sexual behavior and crowing in male Japanese quail. Soc. Neurosci. Abstr., 22, 2068.
Cherry, J. A., and Baum, M. J. (1990). 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, 191-203.
Cohen, R. S., and Pfaff, D. W. (1981). Ultrastructure of neurons in the ventromedial nucleus of the hypothalamus in ovariectomized rats with or without estrogen treatment. Cell Tissue Res. 217, 451-470.
Coolen, L. M., and Wood, R. I. (1996). Dual testosterone stimulation of medial amygdala and medial preoptic area fails to amplify sexual behavior in the male hamster. Ital. J. Anat. Embryol. 101(Suppl. 1), 53-54.
Crews, D., Wade, J., and Wilczynski, W. (1990). Sexually dimorphic areas in the brain of whiptail lizards. Brain Behav. Evol. 36, 262-270.
De Jonge, F. H., Louwerse, A. L., Ooms, M. P., Evers, P., Endert, E., and Van De Poll, N. E. (1989). Lesions of the SDN-POA inhibit sexual behavior of male Wistar rats. Brain Res. Bull. 23, 483-492.
DeVries, G. J. (1990). Sex differences in neurotransmitter systems. J. Neuroendocrinol. 2, 1-13.
DeVries, G. J. (1995). Studying neurotransmitter systems to understand the development and function of sex differences in the brain: the case of vasopressin. In P. E. Micevych and R. P. Hammer, Jr. (Eds.), Neurobiological Effects of Sex Steroid Hormones, pp. 254-278. Cambridge Univ. Press, Cambridge.
DeVries, G. J., De Bruin, J. P. C., Uylings, H. B. M., and Corner, M. A. (1984). Sex Differences in the Brain. Progress in Brain Research, Vol. 61. Elsevier/North-Holland, Amsterdam.
Dörner, G., and Staudt, J. (1968). Structural changes in the preoptic anterior hypothalamic area of the male rat, following neonatal castration and androgen substitution. Neuroendocrinology 3, 136-140.
Etgen, A. M., Ungar, S., and Petitti, N. (1992). Estradiol and progesterone modulation of norepinephrine neurotransmission: Implications for the regulation of female reproductive behavior. J. Neuroendocrinol. 4, 255-271.
Etgen, A. M., Vathy, I, Petitti, N., Ungar, S., and Karkanias, G. B. (1990). Ovarian steroids, female reproductive behavior, and norepinephrine neurotransmission in the hypothalamus. In J. Balthazart (Ed.) Hormones, Brain and Behaviour in Vertebrates. 2. Behavioral activation in males and females - Social Interaction and Reproductive Endocrinlogy. Comp. Physiol. 9, 116-128.
Foidart, A., De Clerck, A., Harada, N., and Balthazart, J. (1994). Aromatase-immunoreactive cells in the quail brain: Effects of testosterone and sex dimorphism. Physiol. Behav. 55, 453-464.
Foidart, A., Reid, J., Absil, P., Yoshimura, N., Harada, N., and Balthazart, J. (1995). Critical reexamination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme. J. Chem. Neuroanat. 8, 267-282.
Funabashi, T., Brooks, P. J., Mobbs, C. V., and Pfaff, D. W. (1993). DNA methylation and DNase-hypersensitive sites in the 5′ flanking and transcribed regions of the rat preproenkephalin gene: Studies of mediobasal hypothalamus. Mol. Cell. Neurosci. 4, 499-509.
Gerall, A. A., Moltz, H., and Ward, I. L. (1992). Handbook of Behavioral Neurobiology. Vol 11: Sexual Differentiation. Plenum, New York.
Gorski, R. A. (1987). Sexual differentiation of the brain: Mechanisms and implications for neuroscience. In S. S. Easter, Jr., K. F. Barald, and B. M. Carlson (Eds.), From Message to Mind, pp. 256-271. Sinauer Associates, Sunderland, MA.
Gorski, R. A., Gordon, J. H., Shryne, J. E., and Southam, A. M. (1978). Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res. 148, 333-346.
Goy, R. W., and McEwen, B. S. (1980). Sexual Differentiation of the Brain. MIT Press, Cambridge, MA.
Gu, G., and Simerly, R. B. (1994). Hormonal regulation of opioid peptide neurons in the anteroventral periventricular nucleus. Horm. Behav. 28, 503-511.
Harada, N. (1988). Novel properties of human placental aromatase as cytochrome P-450: Purification and characterization of a unique form of aromatase. J. Biochem. 103, 106-113.
Harada, N., Abe-Dohmae, S., Loeffen, R., Foidart, A., and Balthazart, J. (1993). Synergism between androgens and estrogens in the induction of aromatase and its messenger RNA in the brain. Brain Res. 622, 243-256.
Harada, N., Yamada, K., Foidart, A., and Balthazart, J. (1992). Regulation of aromatase cytochrome P-450 (estrogen synthetase) transcripts in the quail brain by testosterone. Mol. Brain Res. 15, 19-26.
Jones, K. J., Pfaff, D. W., and McEwen, B. S. (1991). Ultrastructural and morphometric analysis of neurons in the arcuate nucleus of female rat hypothalamus following estradiol. Brain Res. Bull. 26, 181-184.
Jost, A. (1960). Hormonal influences on the sex development of the bird and mammalian embryo. Mem. Soc. Endocrinol. 7, 49-62.
Jost, A. (1985). Sexual organogenesis. In N. Adler, D. Pfaff, and R. W. Goy, (Eds.), Handbook of Behavioral Neurobiology. Vol 7: Reproduction, pp. 3-19. Plenum, New York.
Kelley, D. B. (1992). Opening and closing a hormone-regulated period for development of courtship song: A cellular and molecular analysis of vocal neuroeffectors. Ann. N.Y. Acad. Sci. 662, 178-188.
Konishi, M., and Akutagawa, E. (1985). Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch. Nature 315, 145-147.
Kühneman, S., Brown, T. J., Hochberg, R. B., and MacLusky, N. J. (1994). Sex differences in the development of estrogen receptors in the rat brain. Horm. Behav. 28, 483-491.
Kuiper, G. G. J. M., Enmark, E., Pelto-Huikko, M., Nilsson, S., and Gustafsson, J. A. (1996). Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA 93, 5925-5930.
Landel, C. C. Kushner, P. K., and Green, G. L. (1995) Estrogen receptor accessory proteins: Effects on receptor-DNA interactions. Environ. Health Perspect. 103(Suppl. 7), 23-28.
Matsumoto, A., and Arai, Y. (1986). Male-female differences in synaptic organization of the ventromedial nucleus of the hypothalamus in the rat. Neuroendocrinology 42, 232-236.
McEwen, B. S. (1994). Steroid hormone actions on the brain: When is the genome involved? Horm. Behav. 28, 396-405.
McEwen, B. S., Luine, V. N., and Fischette, C. T. (1988). Developmental actions of hormones: From receptors to function. In S. S. Easter, Jr., K. F. Barald, and B. M. Carlson, (Eds.), From Message to Mind, pp. 272-287. Sinauer Associates, Sunderland, MA.
Naftolin, F., and MacLusky, N. J. (1984). Aromatization hypothesis revisited. In M. Serio, M. Motta, M. Zanisi, and L. Martini, (Eds.), Sexual Differentiation: Basic and Clinical Aspects, pp. 79-91. Raven Press, New York.
Naftolin, F., Ryan, K. J., Davies, I. J., Reddy, V. V., Flores, F., Petro, Z., Kuhn, M., White, R. J., Takaoka, Y., and Wolin, L. (1975). The formation of estrogens by central neuroendocrine tissues. Recent Prog. Horm. Res. 31, 295-319.
Nottebohm, F. (1980). Brain pathways for vocal learning in birds: A review of the first 10 years. In J. M. Sprague and A. N Epstein, (Eds.), Progress in Psychobiology and Physiological Psychology, Vol. 9, pp. 85-214. Academic Press, New York.
Nottebohm, F., and Arnold, A. P. (1976). Sexual dimorphism in the vocal control areas in the song bird brain. Science 194, 211-213.
Nottebohm, P., Kelley, D. B., and Paton, J. A. (1982). Connections of vocal control nuclei in the canary telencephalon. J. Comp. Neurol. 207, 344-357.
Ottinger, M. A., and Balthazart, J. (1987). Brain monoamines in Japanese quail: Effects of castration and steroid replacement therapy. Behav. Proc. 14, 197-216.
Ottinger, M. A., Schumacher, M., Clarke, R. N., Duchala, C. S., and Balthazart, J. (1986). Comparison of monoamine concentrations in the brains of adult male and female Japanese quail. Poultry Sci. 65, 1413-1420.
Palkovits, M., and Brownstein, M. J. (1983). Microdissection of brain areas by the punch technique. In A. C. Cuello (Ed.), Brain Microdissection Techniques, pp. 1-36. Wiley, New York.
Panzica, G. C. (1988). Sex differences in the avian brain. Sitta 2, 77-92.
Panzica, G. C., Castagna, C., Aste, N., Viglietti-Panzica, C., and Balthazart, J. (1996a). Testosterone effects on the neuronal ultrastructure in the medial preoptic nucleus of male Japanese quail. Brain Res. Bull. 39, 281-292.
Panzica, G. C., Viglietti-Panzica, C., and Balthazart, J. (1996b). The sexually dimorphic medial preoptic nucleus of quail: A key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrinol. 17, 51-125.
Panzica, G. C, Viglietti-Panzica, C., Sanchez, P., Sante, P., and Balthazart, J. (1991). Effects of testosterone on a selected neuronal population within the preoptic sexually dimorphic nucleus of the Japanese quail. J. Comp. Neurol. 303, 443-456.
Panzica, G. C., Viglietti-Panzica, C., Calcagni, M., Anselmetti, G. C., Schumacher, M., and Balthazart, J. (1987). Sexual differentiation and hormonal control of the sexually dimorphic preoptic medial nucleus in quail. Brain Res. 416, 59-68.
Pfaff, D. W. (1966). Morphological changes in the brains of adult male rats after neonatal castration. J. Endocrinol. 36, 415-416.
Pfaff, D. W. (1989). Features of a hormone-driven defined neural circuit for a mammalian behavior: Principles illustrated, neuroendocrine syllogisms, and multiplicative steroid effects. Ann. NY Acad. Sci. 563, 131-147.
Phoenix, C. H., Goy, R. W., Gerall, A. A., and Young, W. C. (1959). Organizational action of prenatally administered testosterone propionate on the tissues mediating behavior in the female guinea pig. Endocrinology 65, 369-382.
Rainbow, T. C., Parsons, B., and McEwen, B. S. (1982). Sex differences in rat brain estrogen and progestin receptors. Nature 300, 648-649.
Raisman, G., and Field, P. M. (1973). Sexual dimorphism in the neuropil of the preoptic area of the rat and its dependence on neonatal androgens. Brain Res. 54, 1-29.
Ramirez, V. D., Zheng, J. B., and Siddique, K. M. (1996). Membrane receptors for estrogen, progesterone, and testosterone in the rat brain: Fantasy or reality. Cell. Mol. Neurobiol. 16, 175-198.
Reinoso, B. S., and Simerly, R. B. (1991). Hormone-sensitive sexually dimorphic neurons in the anteroventral periventricular nucleus project to the arcuate nucleus of the hypothalamus. Soc. Neurosci. Abstr. 17, 1229.
Romano, G. J., Mobbs, C. V., Lauber, A., Howells, R. D., and Pfaff, D. W. (1990). Differential regulation of proenkephalin gene expression by estrogen in the ventromedial hypothalamus of male and female rats: Implications for the molecular basis of a sexually differentiated behavior. Brain Res. 536, 63-68.
Roselli, C. E. (1991). Sex differences in androgen receptors and aromatase activity in microdissected regions of the rat brain. Endocrinology 128, 1310-1316.
Roselli, C. E. (1996). Sex differences in androgen-regulated expression of cytochrome P450 aromatase in the rat brain. In Abstracts, 4th Aromatase Conference, Tahoe City, CA, Abstract 20.
Roselli, C. E., Klosterman, S. A., and Fasasi, T. A. (1996). Sex differences in androgen responsiveness in the rat brain: Regional differences in the induction of aromatase activity. Neuroendocrinology 64, 139-145.
Schumacher, M., and Balthazart, J. (1986). Testosterone-induced brain aromatase is sexually dimorphic. Brain Res. 370, 285-293.
Schumacher, M., and Balthazart, J. (1987). Neuroanatomical distribution of testosterone metabolizing enzymes in the Japanese quail. Brain Res. 422, 137-148.
Schumacher, M., Hendrick, J. C., and Balthazart, J. (1989). Sexual differentiation in quail: Critical period and hormonal specificity. Horm. Behav. 23, 130-149.
Schumacher, M., Sulon, J., and Balthazart, J. (1988). Changes in serum concentrations of steroids during embryonic and post-hatching development of male and female Japanese quail (Coturnix coturnix japonica). J. Endocrinol. 118, 127-134.
Schwabl, H. (1993). Yolk is a source of maternal testosterone for developing birds. Proc. Natl. Acad. Sci. USA 90, 11446-11450.
Steimer, T., and Hutchison, J. B. (1981). Androgen increases formation of behaviourally effective oestrogen in dove brain. Nature 292, 345-347.
Steinach, E. (1940). Sex and Life. Viking Press, New York.
Swaab, D. F., and Fliers, E. (1985). A sexually dimorphic nucleus in the human brain. Science 228, 1112-1115.
Székely, T., Catchpole, C. K., DeVoogd, A., Marchl, Z., and DeVoogd, T. J. (1996). Evolutionary changes in a song control area of the brain (HVC) are associated with evolutionary changes in song repertoire among European warblers (Sylviidae). Proc. R. Soc. Lond. [Biol.] 263, 607-610.
Tobet, S. A., and Fox, T. O. (1992). Sex differences in neuronal morphology influenced hormonally throughout life. In A. A. Gerall, H. Moltz, and I. L. Ward, (Eds.), Handbook of Behavioral Neurobiology. Vol. 11: Sexual Differentiation, pp. 41-83. Plenum, New York.
Turner, C. D., and Bagnara, J. T. (1976). General Endocrinology, 6th ed. Saunders, Philadelphia.
Van Eerdenburg, F. J. C. M., and Swaab, D. F. (1991). Increasing neuron numbers in the vasopressin and oxytocin containing nucleus of the adult female pig hypothalamus. Neurosci. Lett. 132, 85-88.
Viglietti-Panzica, C., Aste, N., Balthazart, J., and Panzica, G. C. (1994). Vasotocinergic innervation of sexually dimorphic medial preoptic nucleus of the male Japanese quail: Influence of testosterone. Brain Res. 657, 171-184.
Viglietti-Panzica, C., and Panzica, G. C. (1991). Peptidergic neurons in the avian brain. Ann. Sci. Nat. Zool. Paris 12, 137-155.
Viglietti-Panzica, C., Panzica, G. C., Fiori, M. G., Calcagni, M., Anselmetti, G. C., and Balthazart, J. (1986). A sexually dimorphic nucleus in the quail preoptic area. Neurosci. Lett. 64, 129-134.
Wade, J., and Crews, D. (1992). Sexual dimorphisms in the soma size of neurons in the brain of whiptail lizards (Cnemidophorus species). Brain Res. 594, 311-314.
Watson, J. T., and Adkins-Regan, E. (1989a). Neuroanatomical localization of sex steroid-concentrating cells in the Japanese quail (Coturnix japonica): Autoradiography with [3H]-testosterone, [3H]-estradiol, and [3H]-dihydrotestosterone. Neuroendocrinology 49, 51-64.
Watson, J. T., and Adkins-Regan, E. (1989b). Testosterone implanted in the preoptic area of male Japanese quail must be aromatized to activate copulation. Horm. Behav. 23, 432-447.
Watson, J. T., and Adkins-Regan, E. (1989c). Activation of sexual behavior by implantation of testosterone propionate and estradiol benzoate into the preoptic area of the male Japanese quail (Coturnix japonica). Horm. Behav. 23, 251-268.
Wood, R. I., and Newman, S. W. (1995). Hormonal influence on neurons of the mating behavior pathway in male hamsters. In P. E. Micevych and R. P. Hammer, Jr. (Eds.), Neurobiological Effects of Sex Steroid Hormones, pp. 3-39. Cambridge Univ. Press, Cambridge.
Yahr, P. (1995). Neural circuitry for the hormonal control of male sexual behavior. In P. E. Micevych and R. P. Hammer, Jr. (Eds.), Neurobiological Effects of Sex Steroid Hormones, pp. 40-56. Cambridge Univ. Press, New York.
Yang, Na.N., Venugopalan, M., Hardikar, S., and Glasebrook, A. (1996). Identification of an estrogen response element activated by metabolites of 17β-estradiol and raloxifene. Science 273, 1222-1225.
