The parvocellular vasotocin system of Japanese quail: A developmental and adult model for the study of influences of gonadal hormones on sexually differentiated and behaviorally relevant neural circuits
Panzica, G. C.; Balthazart, Jacques; Pessatti, M.et al.
2002 • In Environmental Health Perspectives, 110 (Suppl. 3), p. 423-428
avian brain; copulatory behavior; development; sexual dimorphism; vasotocin
Abstract :
[en] Vasotocin (VT; the antidiuretic hormone of birds) is synthesized by diencephalic magnocellular neurons projecting to the neurohypophysis. A sexually dimorphic system of VT-immunoreactive (ir) parvocellular elements has been described within the male medial preoptic nucleus (POM) and the nucleus of the stria terminalis, pars medialis (BSTm). VT-ir fibers are present in many diencephalic and extradiencephalic locations, and quantitative morphometric analyses demonstrated their sexually dimorphic distribution in regions involved in the control of different aspects of reproduction. Moreover, systemic or intracerebroventricular injections of VT markedly inhibit the expression of some aspects of male sexual behavior. In adult animals, circulating levels of testosterone (T) have a profound influence on the VT immunoreactivity within BSTm, POM, and lateral septum. Castration markedly decreases the immunoreaction, whereas T-replacement therapy restores a situation similar to the intact birds. We observed no changes in gonadectomized females treated with T. These changes parallel similar changes in male copulatory behavior (not present in castrated male quail, fully expressed in castrated, T-treated males). The restoration by T of the VT immunoreactivity in castrated male quail could be fully mimicked by a treatment with estradiol (E-2), suggesting that the aromatization of T into E-2 may play a key limiting role in both the activation of male sexual behavior and the induction of VT synthesis. This dimorphism has an organizational nature: administration of E-2 to quail embryos (a treatment that abolishes male sexual behavior) results in a dramatic decrease of the VT immuno reactivity in sexually dimorphic regions. Conversely, the inhibition of E-2 synthesis during embryonic life (a treatment that stimulates the expression of male copulatory behavior in treated females exposed in adulthood to T) results in a malelike distribution of VT immunoreactivity. The VT parvocellular system of the Japanese quail can therefore be considered an accurate marker of the sexual differentiation of brain circuits mediating copulatory behavior and could be a very sensitive indicator of the activity of estrogenlike substances on neural circuits.
Disciplines :
Public health, health care sciences & services Neurosciences & behavior Environmental sciences & ecology
Author, co-author :
Panzica, G. C.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Pessatti, M.
Viglietti-Panzica, C.
Language :
English
Title :
The parvocellular vasotocin system of Japanese quail: A developmental and adult model for the study of influences of gonadal hormones on sexually differentiated and behaviorally relevant neural circuits
Publication date :
June 2002
Journal title :
Environmental Health Perspectives
ISSN :
0091-6765
Publisher :
Us Dept Health Human Sciences Public Health Science, Res Triangle Pk, United States - North Carolina
Leng G., Dyball R.E.J., Luckman S.M. (1992) Mechanisms of vasopressin secretion. Horm. Res 37:33-38.
Acher R., Chauvet J. (1995) The neurohypophysial endocrine regulatory cascade: Precursors, mediators, receptors, and effectors. Front Neuroendocrinol 16:237-289.
Panzica G.C., Calcagni M., Ramieri G., Viglietti-Panzica C. (1988) Extrahypothalamic distribution of vasotocin-immunoreactive fibers and perikarya in the avian central nervous system. Basic Appl. Histochem 32:89-94.
Aste N., Mühlbauer E., Grossmann R. (1996) Distribution of AVT gene expressing neurons in the prosencephalon of Japanese quail and chicken. Cell Tissue Res 286:365-373.
Kiss J.Z., Voorhuis T.A.M., Van Eekelen J.A.M., De Kloet E.R., De Wied D. (1987) Organization of vasotocin-immunoreactive cells and fibers in the canary brain. J. Comp. Neurol 263:347-364.
Voorhuis T.A.M., Kiss J.Z., De Kloet E.R., De Wied D. (1988) Testosterone-sensitive vasotocin-immunoreactive cells and fibers in the canary brain. Brain Res 442:139-146.
Voorhuis T.A.M., De Kloet E.R. (1992) Immunoreactive vasotocin in the zebra finch brain (Taeniopygia guttata). Dev. Brain Res 69:1-10.
Panzica G.C., Plumari L., Garcia-Ojeda E., Deviche P. (1999) Central vasotocin-immunoreactive system in a male passerine bird (Junco hyemalis). J. Comp. Neurol 409:105-117.
Jurkevich A., Barth S.W., Aste N., Panzica G.C., Grossmann R. (1996) Intracerebral sex differences in the vasotocin system in birds: Possible implication on behavioral and autonomic functions. Horm. Behav 30:673-681.
Aste N., Balthazart J., Absil P., Grossmann R., Mühlbauer E., Viglietti-Panzica C., Panzica G.C. (1998) Anatomical and neurochemical definition of the nucleus of the stria terminalis in Japanese quail (Coturnix japonica). J. Comp. Neurol 396:141-157.
Jurkevich A., Barth S.W., Grossmann R. (1997) Sexual dimorphism of arg-vasotocin gene expressing neurons in the telencephalon and dorsal diencephalon of the domestic fowl. An immunocytochemical and in situ hybridization study. Cell Tissue Res 287:69-77.
Van Leeuwen F.W., Caffé A.R., De Vries G.J. (1985) Vasopressin cells in the bed nucleus of the stria terminalis of the rat: Sex differences and the influence of androgens. Brain Res 325:391-394.
Voorhuis T.A.M., De Kloet E.R., De Wied D. (1990) The vasotocin system in the canary brain., Hormones, Brain and Behaviour in Vertebrates. Sexual Differentiation, Neuroanatomical Aspects, Neurotransmitters and Neuropeptides (Balthazart J, ed). Basel/New York:Karger; 1:168-179.
Panzica G.C., Aste N., Castagna C., Viglietti-Panzica C., Balthazart J. (2001) Steroid-induced plasticity in the sexually dimorphic vasotocinergic innervation of the avian brain: Behavioral implications. Brain Res. Rev 37:178-200.
Absil P., Papello M., Viglietti Panzica C., Balthazart J., Panzica G.C. The medial preoptic nucleus recieves vasotocinergic inputs in male quail: A tract-tracing and immunocytochemical study. Congr Soc. Ital. Neuroscienze. J. Chem. Neuromat, (in press); .
Panzica G.C., 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.
Viglietti-Panzica C., Anselmetti G.C., Balthazart J., Aste N., Panzica G.C. (1992) Vasotocinergic innervation of the septal region in the Japanese quail: Sexual differences and the influence of testosterone. Cell Tissue Res 267:261-265.
De Vries G.J., Miller M.A. (1998) Anatomy and function of extrahypothalamic vasopressin systems in the brain. Prog. Brain Res 119:3-20.
Panzica G.C., Viglietti-Panzica C., Sizzano F., Solow R., Thompson N., Ottinger M.A. (1999) Gender differences in relationships among vasotocin and VIP containing axons and avian GnRH neurons., 3rd annual meeting of the Society for Behavioral Neuroendorcrinology, 27-29 June 1999, Charlottesville, Virginia. Abstract book; 142.
Balthazart J., Absil P., Viglietti-Panzica C., Panzica G.C. (1997) Vasotocinergic innervation of areas containing aromatase-immunoreactive cells in the quail forebrain. J. Neurobiol 33:45-60.
Absil P., Baillen M., Ball G.F., Panzica G.C., Balthazart J. (2001) The control of preoptic aromatase activity by afferent inputs in Japanese quail. Brain Res. Rev 37:38-58.
Potash L.M. (1970) Neuroanatomical regions relevant to production and analysis of vocalization within the avian torus semicircularis. Experientia 26:1104-1105.
De Lanerolle N., Andrew R.J. (1974) Midbrain structures controlling vocalization in the domestic chick. Brain Behav. Evol 10:354-376.
Armitage S.E., Seller T.J. (1981) Midbrain regions involved in call production in Japanese quail. Experientia 37:847-848.
Adkins-Regan E., Pickett P., Koutnik D. (1982) Sexual differentiation in quail: Conversion of androgen to estrogen mediates testosterone-induced demasculinization of copulation but not other male characteristics. Horm. Behav 16:259-278.
Yazaki Y., Matsushima T., Aoki K. (1999) Testosterone modulates stimulation-induced calling behavior in Japanese quails. J. Comp. Physiol. [A] 184:13-19.
Ball G.F., Foidart A., Balthazart J. (1989) A dorsomedial subdivision within the nucleus intercollicularis identified in the Japanese quail (Coturnix coturnix japonica) by means of α2-adrenergic receptor autoradiography and estrogen receptor immunohistochemistry. Cell Tissue Res 257:123-128.
Panzica G.C., Aste N., Coscia A., De Bernardi W., Viglietti-Panzica C., Balthazart J. (1991) A sex-dependent influence of testosterone on the dorso-medial neuronal population of the Japanese quail intercollicular nucleus. J. Hirnforsch 32:469-475.
Davies D.C., Horn G., McCabe B.J. (1985) Noradrenaline and learning: Effects of the noradrenergic neurotoxin DSP4 on imprinting in the domestic chick. Behav. Neurosci 99:652-660.
Balthazart J., Libioulle J.M., Sante P. (1988) Stimulatory effects of the noradrenergic neurotoxin DSP4 on sexual behavior in male quail. Behav. Processes 17:27-44.
Ottinger M.A., Schumacher M., Clarke R.N., Duchala C.S., Turek R., Balthazart J. (1986) Comparison of monoamine concentrations in the brains of adult male and female Japanese quail. Poultry Sci 65:1413-1420.
Ottinger M.A., Balthazart J. (1987) Brain monoamines and sexual behavior in Japanese quail: Effects of castration and steroid replacement therapy. Behav. Processes 14:197-216.
Millam J.R., Ottinger M.A., Craig-Veit C.B., Fan Y., Chaiseha Y., El Halawani M.E. (1998) Multiple forms of GnRH are released from perifused medial basal hypothalamic/preoptic area (MBH/POA) explants in birds. Gen. Comp. Endocrinol 111:95-101.
Balthazart J., 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.
Kimura T., Okanoya K., Wada M. (1999) Effect of testosterone on the distribution of vasotocin immunoreactivity in the brain of the zebra finch, Taeniopygia guttata castanotis. Life Sci 65:1663-1670.
Panzica G.C., Castagna C., Viglietti-Panzica C., Russo C., Tlemçani O., Balthazart J. (1998) Organizational effects of estrogens on brain vasotocin and sexual behavior in quail. J. Neurobiol 37:684-699.
Voorhuis T.A.M., De Kloet E.R., De Wied D. (1991) Ontogenetic and seasonal changes in immunoreactive vasotocin in the canary brain. Dev. Brain Res 61:23-31.
Deviche P., García-Ojeda E., Plumari L., Panzica G.C. (1996) Vasotocinergic innervation in a male passerine bird (Junco hyemalis): effect of photoperiodic condition. Soc. Neurosci. Abstr , [Abstract]; 22:1551.
Panzica G.C., Garcia-Ojeda E., Viglietti-Panzica C., Thompson N.E., Ottinger M.A. (1996) Testosterone effects on vasotocinergic innervation of sexually dimorphic medial preoptic nucleus and lateral septum during aging in male quail. Brain Res 712:190-198.
Viglietti-Panzica C., Aste N., Balthazart J., 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.
Panzica G.C., Pessatti M., Viglietti-Panzica C., Grossmann R., Balthazart J. (1999) Effects of testosterone on sexually dimorphic parvocellular neurons expressing vasotocin mRNA in the male quail brain. Brain Res 850:55-62.
Viglietti Panzica C., Balthazart J., Fratesi S., Plumari L., Absil P., Panzica G.C. (2001) Estradiol mediates effects of testosterone on vasotocin-immunoreactivity in the adult quail brain. Horm. Behav 40:445-461.
Adkins E.K., Pniewski E.E. (1978) Control of reproductive behavior by sex steroids in male quail. J. Comp. Physiol. Psychol 92:1169-1178.
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.
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.
Aste N., Panzica G.C., Aimar P., Viglietti-Panzica C., Foidart A., 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., 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.
Schumacher M., Sulon J., 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.
Adkins E.K., Adler N.T. (1972) Hormonal control of behavior in the Japanese quail. J. Comp. Physiol. Psychol 81:27-36.
Adkins E.K. (1979) Effect of embryonic treatment with estradiol or testosterone on sexual differentiation of the quail brain. Critical period and dose-response relationship. Neuroendocrinology 29:178-185.
Schumacher M., Hendrick J.C., Balthazart J. (1989) Sexual differentiation in quail: Critical period and hormonal specificity. Horm. Behav 23:130-149.
Balthazart J., De Clerck A., Foidart A. (1992) Behavioral demasculinization of female quail is induced by estrogens: Studies with the new aromatase inhibitor, R76713. Horm. Behav 26:179-203.
Balthazart J., Ball G.F. (1995) Sexual differentiation of brain and behavior in birds. Trends Endocrinol. Metab 6:21-29.
Aste N., Panzica G.C., 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.
Grossmann R., Jurkevich A. (2000) Estradiol treatment during embryogenesis affects masculine behavior and sex dimorphic vasotocin system in adult male chickens. Soc. Neurosci. Abstr , [Abstract]; 26:306.
Aste N., Baiamonte G., Grossmann R., Panzica G.C. (1997) Postnatal development and sexual differentiation of quail vasotocin system. Italian J. Anat. Embriol , [Abstract]; 102(SUPPL. 1).
Jurkevich A., Barth S.W., Kuenzel W.J., Kohler A., Grossmann R. (1999) Development of sexually dimorphic vasotocinergic system in the bed nucleus of stria terminalis in chickens. J. Comp. Neurol 408:46-60.
Shimada K., Neldon H., Koike T.I. (1986) Arginine vasotocin (AVT) release in relation to uterine contractility in the hen. Gen. Comp. Endocrinol 64:362-367.
Koike T.I., Shimada K., Cornett L.E. (1988) Plasma levels of immunoreactive mesotocin and vasotocin during oviposition in chickens: Relationship to oxytocic action of the peptides in vitro and peptide interaction with myometrial membrane binding sites. Gen. Comp. Endocrinol 70:119-126.
Rice G.E., Arnason S.S., Arad Z., Skadhauge E. (1985) Plasma concentrations of arginine vasotocin, prolactin, aldosterone, and corticosterone in relation to ovoposition and dietary NaCl in the domestic fowl. Comp. Biochem. Physiol 81 A:769-777.
Kihlström J.E., Danninge I. (1972) Neurohypophysial hormones and sexual behavior in males of the domestic fowl (Gallus domesticus) and the pigeon (Columba livia Gmel.). Gen. Comp. Endocrinol 18:115-120.
Bernroider G., Leutgeb S. (1994) V1-receptor mediated effects of vasotocin on motivational, mnemonic and aversive components of sexual learning in quail. Soc. Neurosci. Abstr 20:1602.
Goodson J.L., Adkins-Regan E. Effect of intraseptal vasotocin and vasoactive intestinal polypeptide infusions on courtship song and aggression in the male zebra finch (Taeniopygia guttata). J. Neuroendocrinol , 1999; 11:19-25.
Castagna C., Absil P., Foidart A., Balthazart J. (1998) Systemic and intracerebroventricular injections of vasotocin inhibit appetitive and consummatory components of male sexual behavior in Japanese quail. Behav. Neurosci 112:233-250.
Voorhuis T.A.M., De Kloet E.R., De Wied D. (1991) Effect of a vasotocin analog on singing behavior in the canary. Horm. Behav 25:549-559.
Goodson J.L., Bass A.H. (2001) Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res. Rev 35:246-265.
Everitt B.J., Stacey P. (1987) Studies of instrumental behavior with sexual reinforcement in male rats (Rattus norvegicus): Effects of preoptic area lesions, castration and testosterone. J. Comp. Psychol 101:407-419.
Everitt B.J., Cador M., Robbins T.W. (1989) Interactions between the amygala and ventral striatum in stimulus-reward associations: Studies using a second-order schedule of sexual reinforcement. Neuroscience 30:63-75.
Everitt B.J. (1990) Sexual motivation: A neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses in male rats. Neurosci. Biobehav. Rev 14:217-232.
Balthazart J., Ball G.F. (1997) Neuroendocrine regulation of appetitive and consummatory aspects of male sexual behavior in Japanese quail. Perspectives in Avian Endocrinology , (Etches R, Harvey S, eds). Bristol, UK:Society for Endocrinology; 241-255.
Balthazart J., Tlemçani O., Ball G.F. (1996) Do sex differences 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.
Castagna C., Ball G.F., Balthazart J. (1997) Effects of dopamine receptor agonists on appetitive and consummatory male sexual behavior in Japanese quail. Pharmacol Biochem. Behav 58:403-414.
Panzica G.C., Aste N., Castagna C., Balthazart J., Viglietti-Panzica C. (1997) Sexual dimorphism, steroid-induced plasticity, and behavioral significance of the vasotocinergic innervation of the avian brain. Neuroendocrinology: Retrospect and Perspectives , (Korf H-W, Usadel KH, eds). Berlin:Springer Verlag; 127-150.
Berg C., Halldin K., Brunstrom B., Brandt I. (1998) Methods for studying xenoestrogenic effects in birds. Toxicol Lett 102-103:671-676.
Halldin K., Berg C., Brandt I., Brunström B. (1999) Sexual behavior in Japanese quail as a test end point for endocrine disruption: Effects of in ovo exposure to ethinylestradiol and diethylstilbestrol. Environ. Health Perspect 107:861-866.
Jurkevich A., Grossmann R., Balthazart J., Viglietti-Panzica C. (2001) Gender-related changes in the avian vasotocin system during ontogeny. Microsc. Res. Tech 55:27-36.
