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. 2002 Jun;110(Suppl 3):423–428. doi: 10.1289/ehp.02110s3423

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.

Gian Carlo Panzica 1, Jacques Bakthazart 1, Marzia Pessatti 1, Carla Viglietti-Panzica 1
PMCID: PMC1241193  PMID: 12060839

Abstract

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 immunoreactivity 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.

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Selected References

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  1. Absil P., Baillien M., Ball G. F., Panzica G. C., Balthazart J. The control of preoptic aromatase activity by afferent inputs in Japanese quail. Brain Res Brain Res Rev. 2001 Nov;37(1-3):38–58. doi: 10.1016/s0165-0173(01)00122-9. [DOI] [PubMed] [Google Scholar]
  2. Acher R., Chauvet J. The neurohypophysial endocrine regulatory cascade: precursors, mediators, receptors, and effectors. Front Neuroendocrinol. 1995 Jul;16(3):237–289. doi: 10.1006/frne.1995.1009. [DOI] [PubMed] [Google Scholar]
  3. Adkins-Regan E., Pickett P., Koutnik D. Sexual differentiation in quail: conversion of androgen to estrogen mediates testosterone-induced demasculinization of copulation but not other male characteristics. Horm Behav. 1982 Sep;16(3):259–278. doi: 10.1016/0018-506x(82)90026-5. [DOI] [PubMed] [Google Scholar]
  4. Adkins E. K., Adler N. T. Hormonal control of behavior in the Japanese quail. J Comp Physiol Psychol. 1972 Oct;81(1):27–36. doi: 10.1037/h0033315. [DOI] [PubMed] [Google Scholar]
  5. Adkins E. K. Effect of embryonic treatment with estradiol or testosterone on sexual differentiation of the quail brain. Critical period and dose-response relationships. Neuroendocrinology. 1979;29(3):178–185. doi: 10.1159/000122920. [DOI] [PubMed] [Google Scholar]
  6. Aste N., Balthazart J., Absil P., Grossmann R., Mülhbauer E., Viglietti-Panzica C., Panzica G. C. Anatomical and neurochemical definition of the nucleus of the stria terminalis in Japanese quail (Coturnix japonica). J Comp Neurol. 1998 Jun 29;396(2):141–157. [PubMed] [Google Scholar]
  7. Aste N., Mühlbauer E., Grossmann R. Distribution of AVT gene expressing neurons in the prosencephalon of japanese quail and chicken. Cell Tissue Res. 1996 Dec;286(3):365–373. doi: 10.1007/s004410050706. [DOI] [PubMed] [Google Scholar]
  8. Aste N., Panzica G. C., Aimar P., Viglietti-Panzica C., Foidart A., Balthazart J. Implication of testosterone metabolism in the control of the sexually dimorphic nucleus of the quail preoptic area. Brain Res Bull. 1993;31(5):601–611. doi: 10.1016/0361-9230(93)90129-y. [DOI] [PubMed] [Google Scholar]
  9. Aste N., Panzica G. C., Aimar P., Viglietti-Panzica C., Harada N., Foidart A., Balthazart J. Morphometric studies demonstrate that aromatase-immunoreactive cells are the main target of androgens and estrogens in the quail medial preoptic nucleus. Exp Brain Res. 1994;101(2):241–252. doi: 10.1007/BF00228744. [DOI] [PubMed] [Google Scholar]
  10. Aste N., Panzica G. C., Viglietti-Panzica C., Balthazart J. 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. 1991 Nov;27(5):713–720. doi: 10.1016/0361-9230(91)90051-k. [DOI] [PubMed] [Google Scholar]
  11. Ball G. F., Foidart A., Balthazart J. A dorsomedial subdivision within the nucleus intercollicularis identified in the Japanese quail (Coturnix coturnix japonica) by means of alpha 2-adrenergic receptor autoradiography and estrogen receptor immunohistochemistry. Cell Tissue Res. 1989 Jul;257(1):123–128. doi: 10.1007/BF00221641. [DOI] [PubMed] [Google Scholar]
  12. Balthazart J., Absil P., Viglietti-Panzica C., Panzica G. C. Vasotocinergic innervation of areas containing aromatase-immunoreactive cells in the quail forebrain. J Neurobiol. 1997 Jul;33(1):45–60. [PubMed] [Google Scholar]
  13. Balthazart J., Ball G. F. Effects of the noradrenergic neurotoxin DSP-4 on luteinizing hormone levels, catecholamine concentrations, alpha 2-adrenergic receptor binding, and aromatase activity in the brain of the Japanese quail. Brain Res. 1989 Jul 17;492(1-2):163–175. doi: 10.1016/0006-8993(89)90899-8. [DOI] [PubMed] [Google Scholar]
  14. Balthazart J., De Clerck A., Foidart A. Behavioral demasculinization of female quail is induced by estrogens: studies with the new aromatase inhibitor, R76713. Horm Behav. 1992 Jun;26(2):179–203. doi: 10.1016/0018-506x(92)90041-s. [DOI] [PubMed] [Google Scholar]
  15. Balthazart J., Schumacher M., Malacarne G. Interaction of androgens and estrogens in the control of sexual behavior in male Japanese quail. Physiol Behav. 1985 Aug;35(2):157–166. doi: 10.1016/0031-9384(85)90330-0. [DOI] [PubMed] [Google Scholar]
  16. Balthazart J., Tlemçani O., Ball G. F. 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. 1996 Dec;30(4):627–661. doi: 10.1006/hbeh.1996.0066. [DOI] [PubMed] [Google Scholar]
  17. Berg C., Halldin K., Brunström B., Brandt I. Methods for studying xenoestrogenic effects in birds. Toxicol Lett. 1998 Dec 28;102-103:671–676. doi: 10.1016/s0378-4274(98)00285-9. [DOI] [PubMed] [Google Scholar]
  18. Castagna C., Absil P., Foidart A., Balthazart J. Systemic and intracerebroventricular injections of vasotocin inhibit appetitive and consummatory components of male sexual behavior in Japanese quail. Behav Neurosci. 1998 Feb;112(1):233–250. doi: 10.1037//0735-7044.112.1.233. [DOI] [PubMed] [Google Scholar]
  19. Castagna C., Ball G. F., Balthazart J. Effects of dopamine agonists on appetitive and consummatory male sexual behavior in Japanese quail. Pharmacol Biochem Behav. 1997 Oct;58(2):403–414. doi: 10.1016/s0091-3057(97)00243-8. [DOI] [PubMed] [Google Scholar]
  20. Davies D. C., Horn G., McCabe B. J. Noradrenaline and learning: effects of the noradrenergic neurotoxin DSP4 on imprinting in the domestic chick. Behav Neurosci. 1985 Aug;99(4):652–660. doi: 10.1037//0735-7044.99.4.652. [DOI] [PubMed] [Google Scholar]
  21. Everitt B. J., Cador M., Robbins T. W. Interactions between the amygdala and ventral striatum in stimulus-reward associations: studies using a second-order schedule of sexual reinforcement. Neuroscience. 1989;30(1):63–75. doi: 10.1016/0306-4522(89)90353-9. [DOI] [PubMed] [Google Scholar]
  22. Everitt B. J. Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci Biobehav Rev. 1990 Summer;14(2):217–232. doi: 10.1016/s0149-7634(05)80222-2. [DOI] [PubMed] [Google Scholar]
  23. Everitt B. J., Stacey P. Studies of instrumental behavior with sexual reinforcement in male rats (Rattus norvegicus): II. Effects of preoptic area lesions, castration, and testosterone. J Comp Psychol. 1987 Dec;101(4):407–419. [PubMed] [Google Scholar]
  24. 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 Jan;11(1):19–25. doi: 10.1046/j.1365-2826.1999.00284.x. [DOI] [PubMed] [Google Scholar]
  25. Goodson J. L., Bass A. H. Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Brain Res Rev. 2001 Jul;35(3):246–265. doi: 10.1016/s0165-0173(01)00043-1. [DOI] [PubMed] [Google Scholar]
  26. Halldin K., Berg C., Brandt I., Brunström B. 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. 1999 Nov;107(11):861–866. doi: 10.1289/ehp.99107861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jurkevich A., Barth S. W., Aste N., Panzica G., Grossmann R. Intracerebral sex differences in the vasotocin system in birds: possible implication in behavioral and autonomic functions. Horm Behav. 1996 Dec;30(4):673–681. doi: 10.1006/hbeh.1996.0068. [DOI] [PubMed] [Google Scholar]
  28. Jurkevich A., Barth S. W., Grossmann R. 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. 1997 Jan;287(1):69–77. doi: 10.1007/s004410050732. [DOI] [PubMed] [Google Scholar]
  29. Jurkevich A., Barth S. W., Kuenzel W. J., Köhler A., Grossmann R. Development of sexually dimorphic vasotocinergic system in the bed nucleus of stria terminalis in chickens. J Comp Neurol. 1999 May 24;408(1):46–60. doi: 10.1002/(sici)1096-9861(19990524)408:1<46::aid-cne4>3.0.co;2-5. [DOI] [PubMed] [Google Scholar]
  30. Jurkevich A., Grossmann R., Balthazart J., Viglietti-Panzica C. Gender-related changes in the avian vasotocin system during ontogeny. Microsc Res Tech. 2001 Oct 1;55(1):27–36. doi: 10.1002/jemt.1153. [DOI] [PubMed] [Google Scholar]
  31. Kihlström J. E., Danninge I. Neurohypophysial hormones and sexual behavior in males of the domestic fowl (Gallus domesticus L.) and the pigeon (Columba livia Gmel.). Gen Comp Endocrinol. 1972 Feb;18(1):115–120. doi: 10.1016/0016-6480(72)90087-1. [DOI] [PubMed] [Google Scholar]
  32. Kimura T., Okanoya K., Wada M. Effect of testosterone on the distribution of vasotocin immunoreactivity in the brain of the zebra finch, Taeniopygia guttata castanotis. Life Sci. 1999;65(16):1663–1670. doi: 10.1016/s0024-3205(99)00415-4. [DOI] [PubMed] [Google Scholar]
  33. Kiss J. Z., Voorhuis T. A., van Eekelen J. A., de Kloet E. R., de Wied D. Organization of vasotocin-immunoreactive cells and fibers in the canary brain. J Comp Neurol. 1987 Sep 15;263(3):347–364. doi: 10.1002/cne.902630304. [DOI] [PubMed] [Google Scholar]
  34. Koike T. I., Shimada K., Cornett L. E. 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. 1988 Apr;70(1):119–126. doi: 10.1016/0016-6480(88)90100-1. [DOI] [PubMed] [Google Scholar]
  35. Leng G., Dyball R. E., Luckman S. M. Mechanisms of vasopressin secretion. Horm Res. 1992;37(1-2):33–38. doi: 10.1159/000182278. [DOI] [PubMed] [Google Scholar]
  36. Millam J. R., Ottinger M. A., Craig-Veit C. B., Fan Y., Chaiseha Y., el Halawani M. Multiple forms of GnRH are released from perifused medial basal hypothalamic/preoptic area (MBH/POA) explants in birds. Gen Comp Endocrinol. 1998 Jul;111(1):95–101. doi: 10.1006/gcen.1998.7094. [DOI] [PubMed] [Google Scholar]
  37. Ottinger M. A., Schumacher M., Clarke R. N., Duchala C. S., Turek R., Balthazart J. Comparison of monoamine concentrations in the brains of adult male and female Japanese quail. Poult Sci. 1986 Jul;65(7):1413–1420. doi: 10.3382/ps.0651413. [DOI] [PubMed] [Google Scholar]
  38. Panzica G. C., Aste N., Castagna C., Viglietti-Panzica C., Balthazart J. Steroid-induced plasticity in the sexually dimorphic vasotocinergic innervation of the avian brain: behavioral implications. Brain Res Brain Res Rev. 2001 Nov;37(1-3):178–200. doi: 10.1016/s0165-0173(01)00118-7. [DOI] [PubMed] [Google Scholar]
  39. Panzica G. C., Aste N., Coscia A., De Bernardi W., Viglietti-Panzica C., Balthazart J. A sex-dependent influence of testosterone on the dorso-medial neuronal population of the Japanese quail intercollicular nucleus. J Hirnforsch. 1991;32(4):469–475. [PubMed] [Google Scholar]
  40. Panzica G. C., Calcagni M., Ramieri G., Viglietti-Panzica C. Extrahypothalamic distribution of vasotocin-immunoreactive fibers and perikarya in the avian central nervous system. Basic Appl Histochem. 1988;32(1):89–94. [PubMed] [Google Scholar]
  41. Panzica G. C., Castagna C., Viglietti-Panzica C., Russo C., Tlemçani O., Balthazart J. Organizational effects of estrogens on brain vasotocin and sexual behavior in quail. J Neurobiol. 1998 Dec;37(4):684–699. doi: 10.1002/(sici)1097-4695(199812)37:4<684::aid-neu15>3.0.co;2-u. [DOI] [PubMed] [Google Scholar]
  42. Panzica G. C., García-Ojeda E., Viglietti-Panzica C., Thompson N. E., Ottinger M. A. Testosterone effects on vasotocinergic innervation of sexually dimorphic medial preoptic nucleus and lateral septum during aging in male quail. Brain Res. 1996 Mar 18;712(2):190–198. doi: 10.1016/0006-8993(95)01386-5. [DOI] [PubMed] [Google Scholar]
  43. Panzica G. C., Plumari L., García-Ojeda E., Deviche P. Central vasotocin-immunoreactive system in a male passerine bird (Junco hyemalis). J Comp Neurol. 1999 Jun 21;409(1):105–117. [PubMed] [Google Scholar]
  44. Panzica G. C., Viglietti-Panzica C., Balthazart J. The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front Neuroendocrinol. 1996 Jan;17(1):51–125. doi: 10.1006/frne.1996.0002. [DOI] [PubMed] [Google Scholar]
  45. Panzica G., Pessatti M., Viglietti-Panzica C., Grossmann R., Balthazart J. Effects of testosterone on sexually dimorphic parvocellular neurons expressing vasotocin mRNA in the male quail brain. Brain Res. 1999 Dec 11;850(1-2):55–62. doi: 10.1016/s0006-8993(99)02098-3. [DOI] [PubMed] [Google Scholar]
  46. Potash L. M. Neuroanatomical regions relevant to production and analysis of vocalization within the avian torus semicircularis. Experientia. 1970 Oct 15;26(10):1104–1105. doi: 10.1007/BF02112701. [DOI] [PubMed] [Google Scholar]
  47. Rice G. E., Arnason S. S., Arad Z., Skadhauge E. Plasma concentrations of arginine vasotocin, prolactin, aldosterone and corticosterone in relation to oviposition and dietary NaCl in the domestic fowl. Comp Biochem Physiol A Comp Physiol. 1985;81(4):769–777. doi: 10.1016/0300-9629(85)90907-7. [DOI] [PubMed] [Google Scholar]
  48. Schumacher M., Balthazart J. The effects of testosterone and its metabolites on sexual behavior and morphology in male and female Japanese quail. Physiol Behav. 1983 Mar;30(3):335–339. doi: 10.1016/0031-9384(83)90135-x. [DOI] [PubMed] [Google Scholar]
  49. Schumacher M., Hendrick J. C., Balthazart J. Sexual differentiation in quail: critical period and hormonal specificity. Horm Behav. 1989 Mar;23(1):130–149. doi: 10.1016/0018-506x(89)90080-9. [DOI] [PubMed] [Google Scholar]
  50. Schumacher M., Sulon J., Balthazart J. Changes in serum concentrations of steroids during embryonic and post-hatching development of male and female Japanese quail (Coturnix coturnix japonica). J Endocrinol. 1988 Jul;118(1):127–134. doi: 10.1677/joe.0.1180127. [DOI] [PubMed] [Google Scholar]
  51. Shimada K., Neldon H. L., Koike T. I. Arginine vasotocin (AVT) release in relation to uterine contractility in the hen. Gen Comp Endocrinol. 1986 Dec;64(3):362–367. doi: 10.1016/0016-6480(86)90069-9. [DOI] [PubMed] [Google Scholar]
  52. Viglietti-Panzica C., Aste N., Balthazart J., Panzica G. C. Vasotocinergic innervation of sexually dimorphic medial preoptic nucleus of the male Japanese quail: influence of testosterone. Brain Res. 1994 Sep 19;657(1-2):171–184. doi: 10.1016/0006-8993(94)90965-2. [DOI] [PubMed] [Google Scholar]
  53. Viglietti-Panzica C., Balthazart J., Plumari L., Fratesi S., Absil P., Panzica G. C. Estradiol mediates effects of testosterone on vasotocin immunoreactivity in the adult quail brain. Horm Behav. 2001 Dec;40(4):445–461. doi: 10.1006/hbeh.2001.1710. [DOI] [PubMed] [Google Scholar]
  54. Voorhuis T. A., De Kloet E. R., De Wied D. Effect of a vasotocin analog on singing behavior in the canary. Horm Behav. 1991 Dec;25(4):549–559. doi: 10.1016/0018-506x(91)90020-i. [DOI] [PubMed] [Google Scholar]
  55. Voorhuis T. A., De Kloet E. R., De Wied D. Ontogenetic and seasonal changes in immunoreactive vasotocin in the canary brain. Brain Res Dev Brain Res. 1991 Jul 16;61(1):23–31. doi: 10.1016/0165-3806(91)90110-5. [DOI] [PubMed] [Google Scholar]
  56. Voorhuis T. A., Kiss J. Z., de Kloet E. R., de Wied D. Testosterone-sensitive vasotocin-immunoreactive cells and fibers in the canary brain. Brain Res. 1988 Feb 23;442(1):139–146. doi: 10.1016/0006-8993(88)91441-2. [DOI] [PubMed] [Google Scholar]
  57. Voorhuis T. A., de Kloet E. R. Immunoreactive vasotocin in the zebra finch brain (Taeniopygia guttata). Brain Res Dev Brain Res. 1992 Sep 18;69(1):1–10. doi: 10.1016/0165-3806(92)90116-e. [DOI] [PubMed] [Google Scholar]
  58. de Lanerolle N., Andrew R. J. Midbrain structures controlling vocalization in the domestic chick. Brain Behav Evol. 1975;10(4-5):354–376. doi: 10.1159/000124324. [DOI] [PubMed] [Google Scholar]
  59. de Vries G. J., Miller M. A. Anatomy and function of extrahypothalamic vasopressin systems in the brain. Prog Brain Res. 1998;119:3–20. doi: 10.1016/s0079-6123(08)61558-7. [DOI] [PubMed] [Google Scholar]
  60. van Leeuwen F. W., Caffe A. R., De Vries G. J. Vasopressin cells in the bed nucleus of the stria terminalis of the rat: sex differences and the influence of androgens. Brain Res. 1985 Jan 28;325(1-2):391–394. doi: 10.1016/0006-8993(85)90348-8. [DOI] [PubMed] [Google Scholar]

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