Animals; Aromatase/physiology; Estradiol/physiology; Female; Male; Quail/physiology; Reproduction/physiology; Sex Differentiation/physiology; Sexual Behavior, Animal/physiology; Testosterone/physiology
Abstract :
[en] In Japanese quail, estrogen's effects on sexual behavior can be divided into three classes based on the underlying mechanisms and time-course of action and release. During embryonic life, the embryonic ovary secretes large amounts of estrogens. In contrast to what is observed in mammals where sexual differentiation essentially proceeds via masculinization of the males, in quail, females are demasculinized by their endogenous ovarian estrogens, an effect that can be blocked by injection of an aromatase inhibitor and mimicked in male embryos by an injection of estradiol. In adulthood, testosterone secreted by the testes is converted into estrogens by the preoptic aromatase. Locally produced estrogens activate male sexual behavior largely through the activation of estrogen receptors resulting in the transcription of a variety of genes, including brain aromatase (genomic effect). Both changes in estrogen production and action are observed within latencies ranging from a few hours to a few days, and are completely reversible. Additionally, brain aromatase activity can be modulated within minutes by calcium-dependent phosphorylations, triggered by variations in glutamatergic neurotransmission. These rapid changes in aromatase activity affect with relatively short latencies (10-15 min) the expression of male sexual behavior in quail and also in mice. Overall, the effects of estrogens on sexual behavior can thus be categorized into three classes: organizational (irreversible genomic action during ontogeny), activational (reversible genomic action during adulthood) and rapid nongenomic effects. Rapid and slower changes in brain aromatase activity match well with the two modes of estrogen action on behavior and provide temporal variations in the estrogens' bioavailability that should be able to support the entire range of established effects for this steroid.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Charlier, Thierry ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Taziaux, Mélanie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Ball, Gregory F
Language :
English
Title :
Estradiol, a key endocrine signal in the sexual differentiation and activation of reproductive behavior in quail.
Publication date :
2009
Journal title :
Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology
ISSN :
1932-5223
eISSN :
1932-5231
Publisher :
John Wiley & Sons, Hoboken, United States - New Jersey
Adkins EK. 1975. Hormonal basis of sexual differentiation in the Japanese quail. J Comp Physiol Psychol 89:61-71.
Adkins EK. 1976. Embryonic exposure to an antiestrogen masculinizes behavior of female quail. Physiol Behav 17:357-359.
Adkins EK. 1979. Effect of embryonic treatment with estradiol or testosterone on sexual differentiation of the quail brain. J Neuroendocrinol 29:178-185.
Adkins EK, Adler NT. 1972. Hormonal control of behavior in the Japanese quail. J Comp Physiol Psychol 81:27-36.
Adkins EK, Boop JJ, Koutnik DL, Morris JB, Pniewski EE. 1980. Further evidence that androgen aromatization is essential for the activation of copulation in male quail. Physiol Behav 24:441-446.
Adkins-Regan E. 1983. Sex steroids and the differentiation and activation of avian reproductive behaviour. In: Balthazart J, Gilles R, editors. Hormones and behaviour in higher vertebrates. Berlin: Springer. p219-228.
Adkins-Regan E, Leung CH. 2006. Hormonal and social modulation of cloacal muscle activity in female Japanese quail. Physiol Behav 87:82-87.
Agrati P, Garnier M, Patrone C, Pollio G, Santagati S, Vegeto E, Maggi A. 1997. SK-ER3 neuroblastoma cells as a model for the study of estrogen influence on neural cells. Brain Res Bull 44:519-523.
Albert KA, Helmer-Matyjek E, Nairn AA, Müller TH, Haycock JW, Greene LA, Goldstein M, Greengard P. 1984. Calcium/ phospholipid-dependent protein kinase (protein kinase C) phosphorylates and activates tyrosine hydroxylase. Proc Natl Acad Sci USA 81:7713-7717.
Alexandre C, Balthazart J. 1986. Effects of metabolism inhibitors, antiestrogens and antiandrogens on the androgen and estrogen induced sexual behavior in Japanese quail. Physiol Behav 38:581-591.
Ames MM, Lerner P, Lovenberg W. 1978. Tyrosine hydroxylase: activation by protein phosphorylation and end product inhibition. J Biol Chem 253:27-31.
Arnold AP. 2003. The gender of the voice within: the neural origin of sex differences in the brain. Curr Opin Neurobiol 13:759-764.
Arnold AP, Gorski RA. 1984. Gonadal steroid induction of structural sex differences in the central nervous system. Ann Rev Neurosci 7:413-442.
Arnold AP, Xu J, Grisham W, Chen XQ, Kim YH, Itoh Y. 2004. Minireview: sex chromosomes and brain sexual differentiation. Endocrinology 145:1057-1062.
Aste N, Panzica GC, Viglietti-Panzica C, 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 GC, Viglietti-Panzica C, Harada N, Balthazart
J. 1998. Distribution and effects of testosterone on aromatase mRNA in the quail forebrain: a non-radioactive in situ hybridization study. J Chem Neuroanat 14:103-115.
Bagatell CJ, Heiman JR, Rivier JE, Bremner WJ. 1994. Effects of endogenous testosterone and estradiol on sexual behavior in normal young men. J Clin Endocrinol Metab 78:711-716.
Bakker J, Honda SI, Harada N, Balthazart J. 2002. The aromatase knock-out mouse provides new evidence that estradiol is required during development in the female for the expression of sociosexual behaviors in adulthood. J Neurosci 22:9104-9112.
Bakker J, De Mees C, Douhard Q, Balthazart J, Gabant P, Szpirer J, Szpirer C. 2006. Alpha-fetoprotein protects the developing female mouse brain from masculinization and defeminization by estrogens. Nat Neurosci 9:220-226.
Ball GF, Balthazart J. 2002. Neuroendocrine mechanisms regulating reproductive cycles and reproductive behavior in birds. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior. San Diego, CA: Academic Press. p 649-798.
Balthazart J. 1989. Steroid metabolism and the activation of social behavior. In: Balthazart J, editor. Advances in comparative and environmental physiology, Vol 3. Berlin: Springer. p 105-159.
Balthazart J, Adkins-Regan E. 2002. Sexual differentiation of brain and behavior in birds. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior. San Diego, CA: Academic Press. p 223-301.
Balthazart J, Ball GF. 2006. Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 29:241-249.
Balthazart J, Ball GF. 2007. Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors. Front Neuroendocrinol. 28:161-178.
Balthazart J, Surlemont C. 1990a. Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol Behav 48:599-609.
Balthazart J, Surlemont C. 1990b. Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail POA. Brain Res Bull 25:7-14.
Balthazart J, Schumacher M, Ottinger MA. 1983. Sexual differences in the Japanese quail: behavior, morphology and intracellular metabolism of testosterone. Gen Comp Endocrinol 51:191-207.
Balthazart J, Schumacher M, 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, De Clerck A, 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, Surlemont C. 1990a. Effects of the non-steroidal aromatase inhibitor, R76713 on testosteroneinduced sexual behavior in the Japanese quail (Coturnix coturnix japonica). Horm Behav 24:510-531.
Balthazart J, Foidart A, Harada N. 1990b. Immunocytochemical localization of aromatase in the brain. Brain Res 514:327-333.
Balthazart J, Foidart A, Hendrick JC. 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, Surlemont C, Vockel A, 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, Schumacher M, Evrard L. 1990e. Sex differences and steroid control of testosterone-metabolizing enzyme activity in the quail brain. J Neuroendocrinol 2:675-683.
Balthazart J, Surlemont C, Harada N. 1992. Aromatase as a cellular marker of testosterone action in the preoptic area. Physiol Behav 51:395-409.
Balthazart J, Stoop R, Foidart A, Harada N. 1994. Synergistic control by androgens and estrogens of aromatase in the quail brain. Neuroreport 5:1729-1732.
Balthazart J, Tlemc-ani O, Ball GF. 1996a. 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. Horm Behav 30:627-661.
Balthazart J, Tlemc-ani O, Harada N. 1996b. Localization of testosterone-sensitive and sexually dimorphic aromataseimmunoreactive cells in the quail preoptic area. J Chem Neuroanat 11:147-171.
Balthazart J, Absil P, Ge'rard M, Appeltants D, Ball GF. 1998. Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J Neurosci 18: 6512-6527.
Balthazart J, Baillien M, Ball GF. 2001. Rapid and reversible inhibition of brain aromatase activity. J Neuroendocrinol 13:61-71.
Balthazart J, Baillien M, Charlier TD, Ball GF. 2003. Calciumdependent phosphorylation processes control brain aromatase in quail. Eur J Neurosci 17:1591-1606.
Balthazart J, Baillien M, Cornil CA, Ball GF. 2004. Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol Behav 83:247-270.
Balthazart J, Baillien M, Ball GF. 2006. Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology 147:359-366.
Beach FA, Inman NG. 1965. Effects of castration and androgen replacement on mating in male quail. Proc Natl Acad Sci USA 54:1426-1431.
Bridgham JT, Carroll SM, Thornton JW. 2006. Evolution of hormone-receptor complexity by molecular exploitation. Science 312:97-101.
Bryan MB, Scott AP, Li W. 2007. The sea lamprey (Petromyzon marinus) has a receptor for androstenedione. Biol Reprod 77:688-696.
Callard GV, Petro Z, Ryan KJ. 1978. Conversion of androgen to estrogen and other steroids in the vertebrate brain. Am Zool 18:511-523.
Callard GV, Tchoudakova A. 1997. Evolutionary and functional significance of two CYP19 genes differentially expressed in brain and ovary of goldfish. J Steroid Biochem Mol Biol 61:387-392.
Carani C, Granata AR, Rochira V, Caffagni G, Aranda C, Antunez P, Maffei LE. 2005. Sex steroids and sexual desire in a man with a novel mutation of aromatase gene and hypogonadism. Psychoneuroendocrinology 30:413-417.
Corbin CJ, Graham-Lorence S, McPhaul M, Mason JI, Mendelson CR, Simpson ER. 1988. Isolation of a full-length cDNA insert encoding human aromatase system cytochrome P-450 and its expression in nonsteroidogenic cells. Proc Natl Acad Sci USA 85:8948-8952.
Cornil CA, Seutin V, Motte P, Balthazart J. 2004. Electrophysiological and neurochemical characterization of neurons of the medical preoptic area in Japanese quail (Coturnix japonica). Brain Res 1029:224-240.
Cornil CA, Dalla C, Papadopoulu-Daifoti Z, Baillien M, Dejace C, Ball GF, Balthazart J. 2005. Rapid decreases in preoptic aromatase activity and brain monoamine concentrations after engaging in male sexual behavior. Endocrinology 146:3809-3820.
Cornil CA, Ball GF, Balthazart J. 2006a. Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res 1126:2-26.
Cornil CA, Dalla C, Papadopoulou-Daifoti Z, Baillien M, Balthazart J. 2006b. Estradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain. Behav Brain Res 166:110-123.
Cornil CA, Taziaux M, Baillien M, Ball GF, Balthazart J. 2006c. Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail. Horm Behav 49:45-67.
Cross E, Roselli CE. 1999. 17beta-estradiol rapidly facilitates chemoinvestigation and mounting in castrated male rats. Am J Physiol Regul Integr Comp Physiol 276:R1346-R1350.
Daubner SC, Lauriano C, Haycock JW, Fitzpatrick PF. 1992. Site-directed mutagenesis of serine 40 of rat tyrosine hydroxylase. J Biol Chem 267:12639-12646.
De Coster R, Wouters W, Bowden CR, Vanden Bossche H, Bruynseels J, Tuman RW, Van Ginckel R, Snoeck E, Van Peer A, Janssen PAJ. 1990. New non-steroidal aromatase inhibitors: focus on R76713. J Steroid Biochem 37:335-341.
Döhler KD, Hancke JL, Srivastava SS, Hofman C, Shryne JE, Gorski RA. 1984. Participation of estrogens in female sexual differentiation of the brain: neuroanatomical, neuroendocrine and behavioral evidence. In: De Vries GJ, De Bruin JPC, Uylings HBM, Corner MA, editors. Sex differences in the brain. Amsterdam: Elsevier. p 99-117.
Dominguez JM, Gil M, Hull EM. 2006. Preoptic glutamate facilitates male sexual behavior. J Neurosci 26:1699-1703.
Elbrecht A, Smith RG. 1992. Aromatase enzyme activity and sex determination in chickens. Science 255:467-470.
Etgen AM, Vathy I, Petitti N, Ungar S, Karkanias GB. 1990. Ovarian steroids, female reproductive behavior and norepinephrine neurotransmission in the hypothalamus. In: Balthazart J, editor. Hormones, brain and behaviour in vertebrates. 2. Behavioural activation in males and females- social interactions and reproductive physiology, Comp Physiol, Vol 9. Basel: Karger. p 116-128.
Etgen AM, Ungar S, Petitti N. 1992. Estradiol and progesterone modulation of norepinephrine neurotransmission: implications for the regulation of female reproductive behavior. J Neuroendocrinol 4:255-271.
Evrard H, Baillien M, Foidart A, Absil P, Harada N, Balthazart J. 2000. Localization and controls of aromatase in the quail spinal cord. J Comp Neurol 423:552-564.
Evrard HC, Balthazart J. 2004a. Aromatization of androgens into estrogens reduces response latency to a noxious thermal stimulus in male quail. Horm Behav 45:181-189.
Evrard HC, Balthazart J. 2004b. Rapid regulation of pain by estrogens synthesized in spinal dorsal horn neurons. J Neurosci 24:7225-7229.
Feder HH. 1981. Essentials of steroid structure, nomenclature, reactions, biosynthesis, and measurements. In: Adler NT, editor. Neuroendocrinology of reproduction. New York: Plenum Press. p 19-63.
Foidart A, De Clerck A, Harada N, Balthazart J. 1994. Aromatase-immunoreactive cells in the quail brain: effects of testosterone and sex dimorphism. Physiol Behav 55: 453-464.
Garnier M, Di Lorenzo D, Albertini A, Maggi A. 1997. Identification of estrogen-responsive genes in neuroblastoma SK-ER3 cells. J Neurosci 17:4591-4599.
Gorski RA. 1987. Sexual differentiation of the brain: mechanisms and implications for neuroscience. In: Easter SSJ, Barald KF, Carlson BM, editors. From message to mind. Sunderland, MA: Sinauer Associates Inc. p 256-271.
Guichard A, Cedard L, Mignot TM, Scheib D, Haffen K. 1977. Radioimmunoassay of steroids produced by cultured chick embryonic gonads: differences according to age, sex and side. Gen Comp Endocrinol 32:255-265.
Guichard A, Scheib D, Haffen K, Mignot TM, Cedard L. 1980. Comparative study in steroidogenesis by quail and chick embryonic gonads in organ culture. J Steroid Biochem 12:83-87.
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, Yamada K, Foidart A, Balthazart J. 1992. Regulation of aromatase cytochrome P-450 (estrogen synthetase) transcripts in the quail brain by testosterone. Mol Brain Res 15:19-26.
Harada N, Abe-Dohmae S, Loeffen R, Foidart A, 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.
Hutchison RE. 1978. Hormonal differentiation of sexual behavior in Japanese quail. Horm Behav 11:363-387.
Hutchison JB, Steimer TH. 1986. Formation of behaviorally effective 17beta-estradiol in the dove brain: steroid control of preoptic aromatase. Endocrinology 118:2180-2187.
Jarvis ED, Gunturkun O, Bruce L, Csillag A, Karten H, Kuenzel W, Medina L, Paxinos G, Perkel DJ, Shimizu T, Striedter G, Wild JM, Ball GF, Dugas-Ford J, Durand SE, Hough GE, Husband S, Kubikova L, Lee DW, Mello CV, Powers A, Siang C, Smulders TV, Wada K, White SA, Yamamoto K, Yu J, Reiner A, Butler AB. 2005. Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6:151-159.
Kelly MJ, Ronnekleiv OK. 2002. Rapid membrane effects of estrogen in the central nervous system. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior. San Diego: Academic press. p 361-380.
Kretz O, Fester L, Wehrenberg U, Zhou L, Brauckmann S, Zhao S, Prange-Kiel J, Naumann T, Jarry H, Frotscher M, Rune GM. 2004. Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci 24:5913-5921.
Lephart ED. 1996. A review of brain aromatase cytochrome P450. Brain Res Rev 22:1-26.
McEwen BS. 1994. Steroid hormone actions on the brain: when is the genome involved? Horm Behav 28:396-405.
McEwen BS. 2001a. Genome and hormones: gender differences in physiology-invited review: estrogens effects on the brain: multiple sites and molecular mechanisms. J Appl Physiol 91:2785-2801.
McEwen BS. 2001b. Invited review: estrogens effects on the brain: multiple sites and molecular mechanisms. J Appl Physiol 91:2785-2801.
McEwen BS, Alves SE. 1999. Estrogen actions in the central nervous system. Endocr Rev 20:279-307.
McEwen BS, Parsons B. 1982. Gonadal steroid action on the brain: neurochemistry and neuropharmacology. Ann Rev Pharmacol Toxicol 22:555-598.
McEwen BS, Alves SE, Bulloch K, Weiland NG. 1997. Ovarian steroids and the brain: implications for cognition and aging. Neurology 48:S8-S15.
McPhaul MJ, Noble JF, Simpson ER, Mendelson CR, Wilson JD. 1988. The expression of a functional cDNA encoding the chicken cytochrome P-450arom (aromatase) that catalyzes the formation of estrogen from androgen. J Biol Chem 263:16358-16363.
Means GD, Mahendroo MS, Corbin CJ, Mathis JM, Powell FE, Mendelson CR, Simpson ER. 1989. Structural analysis of the gene encoding human aromatase cytochrome P-450, the enzyme responsible for estrogen biosynthesis. J Biol Chem 264:19385-19391.
Mizuta T, Kubokawa K. 2007. Presence of sex steroids and cytochrome P450 genes in amphioxus. Endocrinology 148(8):3554-3565.
Naftolin F, Horvath TL, Jakab RL, Leranth C, Harada N, Balthazart J. 1996. Aromatase immunoreactivity in axon terminals of the vertebrate brain-an immunocytochemical study on quail, rat, monkey and human tissues. J Neuroendocrinol 63:149-155.
Nishikimi H, Kansaku N, Saito N, Usami M, Ohno Y, Shimada K. 2000. Sex differentiation and mRNA expression of P450c17, P450arom and AMH in gonads of the chicken. Mol Reprod Dev 55:20-30.
Ottinger MA, Pitts S, Abdelnabi MA. 2001. Steroid hormones during embryonic development in Japanese quail: plasma, gonadal, and adrenal levels. Poult Sci 80:795-799.
Panzica GC, Viglietti-Panzica C, Calcagni M, Anselmetti GC, Schumacher M, Balthazart J. 1987. Sexual differentiation and hormonal control of the sexually dimorphic preoptic medial nucleus in quail. Brain Res 416:59-68.
Panzica GC, Viglietti-Panzica C, Sanchez F, Sante P, 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 GC, Viglietti-Panzica C, Balthazart J. 1996. The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front Neuroendocrinol 17:51-125.
Peterson RS, Yarram L, Schlinger BA, Saldanha CJ. 2005. Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proc Biol Sci 272:2089-2096.
Pfaff DW, Schwartz-Giblin S, McCarthy MM, Kow LM. 1994. Cellular and molecular mechanisms of female reproductive behaviors. In: Knobil E, Neill JD, editors. The physiology of reproduction, second edition. New York: Raven Press. p 107-220.
Phoenix CH, Goy RW, Gerall AA, Young WC. 1959. Organizational action of prenatally administered testosterone propionate on the tissues mediating behavior in the female guinea pig. Endocrinology 65:369-382.
Ramirez VD, Zheng JB, Siddique KM. 1996. Membrane receptors for estrogen, progesterone, and testosterone in the rat brain: fantasy or reality. Cell Mol Neurobiol 16:175-198.
Rochira V, Balestrieri A, Madeo B, Spaggiari A, Carani C. 2002. Congenital estrogen deficiency in men: a new syndrome with different phenotypes; clinical and therapeutic implications in men. Mol Cell Endocrinol 193:19-28.
Rohmann KN, Schlinger BA, Saldanha CJ. 2007. Subcellular compartmentalization of aromatase is sexually dimorphic in the adult zebra finch brain. Dev Neurobiol 67:1-9.
Roselli CE. 1991a. Sex differences in androgen receptors and aromatase activity in microdissected regions of the rat brain. Endocrinology 128:1310-1316.
Roselli CE. 1991b. Synergistic induction of aromatase activity in the rat brain by estradiol and 5alpha-dihydrotestosterone. J Neuroendocrinol 53:79-84.
Roselli CE, Resko JA. 1984. Androgens regulate brain aromatase activity in adult male rats through a receptor mechanism. Endocrinology 114:2183-2189.
Roselli CE, Resko JA. 1989. Testosterone regulates aromatase activity in discrete brain areas of male rhesus macaques. Biol Reprod 40:929-934.
Roselli CE, Horton LE, Resko JA. 1987. Time-course and steroid specificity of aromatase induction in rat hypothalamus- preoptic area. Biol Reprod 37:628-633.
Rune GM, Lohse C, Prange-Kiel J, Fester L, Frotscher M. 2006. Synaptic plasticity in the hippocampus: effects of estrogen from the gonads or hippocampus? Neurochem Res 31:145-155.
Scheib D, Guichard A, Mignot TM, Reyss-Brion M. 1985. Early sex differences in hormonal potentialities of gonads from quail embryos with a sex-linked pigmentation marker. An in vitro radioimmunoassay study. Gen Comp Endocrinol 60:266-272.
Schlinger BA, Callard GV. 1989. Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain. J Neuroendocrinol 49: 434-441.
Schumacher M. 1990. Rapid membrane effects of steroid hormones: an emerging concept in neuroendocrinology. Trends Neurosci 13:359-362.
Schumacher M, Balthazart J. 1983. The effects of testosterone and its metabolites on sexual behavior and morphology in male and female Japanese quail. Physiol Behav 30: 335-339.
Schumacher M, Balthazart J. 1986. Testosterone-induced brain aromatase is sexually dimorphic. Brain Res 370: 285-293.
Schumacher M, Alexandre C, Balthazart J. 1987. Interactions des androgènes et des oestrogènes dans le contrôle de la reproduction. C R Acad Sci Paris, Se'rie III 305:569-574.
Schumacher M, Sulon J, Balthazart J. 1988. Changes in serum concentrations of steroids during embryonic and posthatching development of male and female Japanese quail (Coturnix coturnix japonica). J Endocrinol 118:127-134.
Schumacher M, Hendrick JC, Balthazart J. 1989. Sexual differentiation in quail: critical period and hormonal specificity. Horm Behav 23:130-149.
Shen P, Campagnoni CW, Kampf K, Schlinger BA, Arnold AP, Campagnoni AT. 1994. Isolation and characterization of a zebra finch aromatase cDNA: in situ hybridization reveals high aromatase expression in brain. Mol Brain Res 24:227-237.
Shimada K. 1998. Gene expression of steroidogenic enzymes in chicken embryonic gonads. J Exp Zool 281:450-456.
Smith CA, Roeszler KN, Hudson QJ, Sinclair AH. 2007. Avian sex determination: what, when and where? Cytogenet Genome Res 117:165-173.
Steimer T, Hutchison JB. 1981. Androgen increases formation of behaviourally effective oestrogen in dove brain. Nature 292:345-347.
Stiglec R, Ezaz T, Graves JA. 2007. A new look at the evolution of avian sex chromosomes. Cytogenet Genome Res 117:103-109.
Taziaux M, Cornil CA, Dejace C, Arckens L, Ball GF, Balthazart J. 2006. Neuroanatomical specificity in the expression of the immediate early gene c-fos following expression of appetitive and consummatory male sexual behaviour in Japanese quail. Eur J Neurosci 23:1869-1887.
Taziaux M, Keller M, Bakker J, Balthazart J. 2007. Sexual behavior activity tracks rapid changes in brain estrogen concentrations. J Neurosci 27:6563-6572.
Thornton JW. 2001. Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc Natl Acad Sci USA 98:5671-5676.
Thornton JW, Need E, Crews D. 2003. Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301:1714-1717.
Tobet SA, Fox TO. 1992. Sex differences in neuronal morphology influenced hormonally throughout life. In: Gerall AA, Moltz H, Ward IL, editors. Handbook of behavioral neurobiology, Vol 11, Sexual differentiation. New York: Plenum Press. p 41-83.
Viglietti-Panzica C, Panzica GC, Fiori MG, Calcagni M, Anselmetti GC, Balthazart J. 1986. A sexually dimorphic nucleus in the quail preoptic area. Neurosci Lett 64:129-134.
Voigt C, Ball GF, Balthazart J. 2007. Neuroanatomical specificity of sex differences in expression of aromatase mRNA in the quail brain. J Chem Neuroanat 33:75-86.
Watson JT, Adkins-Regan E. 1989a. 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.
Watson JT, 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.
Wilson EO. 1975. Sociobiology: the new synthesis. Cambridge, MA: Belknap Press of Harvard University Press. 697p.
Wingfield JC, Kitaysky AS. 2002. Endocrine responses to unpredictable environmental events: stress or anti-stress hormones? Am Zool 42:600-609.
Wingfield JC, Silverin B. 2002. Ecophysiological studies of hormone-behavior relations in birds. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior. San Diego, CA: Academic Press. p 587-647.
Woods JE, Erton LH. 1978. The synthesis of estrogens in the gonads of the chick embryo. Gen Comp Endocrinol 36:360-370.
Wouters W, De Coster R, Krekels M, Van Dun J, Beerens D, Haelterman C, Raeymaekers A, Freyne E, Van Gelder J, Venet M, Janssen PAJ. 1989. R 76713, a new specific non-steroidal aromatase inhibitor. J Steroid Biochem 32:781-788.
Yoshida K, Shimada K, Saito N. 1996. Expression of P45017alpha hydroxylase and P450 aromatase genes in the chicken gonad before and after sexual differentiation. Gen Comp Endocrinol 102:233-240.
