[en] The medial preoptic nucleus of the Japanese quail is a testosterone-sensitive structure that is involved in the control of male copulatory behavior. The full understanding of the role played by this nucleus in the control of reproduction requires the identification of its afferent and efferent connections. In order to identify neural circuits involved in the control of the medial preoptic nucleus, we used the lipophilic fluorescent tracer DiI implanted in aldheyde-fixed tissue. Different strategies of brain dissection and different implantation sites were used to establish and confirm afferent and efferent connections of the nucleus. Anterograde projections reached the tuberal hypothalamus, the area ventralis of Tsai, and the substantia grisea centralis. Dense networks of fluorescent fibers were also seen in several hypothalamic nuclei, such as the anterior medialis hypothalami, the paraventricularis magnocellularis, and the ventromedialis hypothalami. A major projection in the dorsal direction was also observed from the medial preoptic nucleus toward the nucleus septalis lateralis and medialis. Afferents to the nucleus were seen from all these regions. Implantation of DiI into the substantia grisea centralis also revealed massive bidirectional connections with a large number of more caudal mesencephalic and pontine structures. The substantia grisea centralis therefore appears to be an important center connecting anterior levels of the brain to brain-stem nuclei that may be involved in the control of male copulatory behavior.
Disciplines :
Neurosciences & behavior
Author, co-author :
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Dupiereux, V.
Aste, N.
Viglietti-Panzica, C.
Barrese, M.
Panzica, G. C.
Language :
English
Title :
Afferent and Efferent Connections of the Sexually Dimorphic Medial Preoptic Nucleus of the Male Quail Revealed by in Vitro Transport of Dii
Absil P., Foidart A., Balthazart J. (1993) The sexually dimorphic medial preoptic nucleus is specifically labelled by steroid-sensitive neurotensin-immunoreactive cells in Japanese quail. Soc Neurosci Abstr 19:732.
Adkins Regan E.K., Watson J.T. (1990) Sexual dimorphism in the avian brain is not limited to the song system of songbirds: a morphometric analysis of the brain of the quail (Coturnix japonica). Brain Research 514:320-326.
Allen L.S., Hines M., Shryne J.E., Gorski R.A. (1989) Two sexually dimorphic cell groups in the human brain. J Neurosci 9:497-506.
Anderson K.D., Reiner A. (1991) Striatonigral projection neurons: a retrograde labeling study of the percentages that contain substance P or enkephalin in pigeons. J Comp Neurol 303:658-673.
Arendash G.W., 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.
Aste N., Panzica G.C., Aimar P., Viglietti-Panzica C., Foidart A., Balthazart J. (1993) Implication of testosterone metabolism in the control of sexually dimorphic nucleus of the quail preoptic area. Brain Res Bull 31:601-611.
Ball G.F., Nock B., McEwen B.S., Balthazart J. (1989) Distribution of α2-adrenergic receptors in the brain of the Japanese quail as determined by quantitative autoradiography: implication for the control of sexually dimorphic reproductive processes. Brain Res 491:68-79.
Balthazart J. (1991) Testosterone metabolism in the avian hypothalamus. J Steroid Biochem Mol Biol 40:557-570.
Balthazart J., Foidart A. (1993) Brain aromatase and the control of male sexual behavior. J Steroid Biochem Mol Biol 44:521-540.
Balthazart J., Surlemont C. (1990) Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail preoptic area. Brain Res Bull 25:7-14.
Balthazart J., Surlemont C. (1990) Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol Behav 48:599-609.
Balthazart J., Schumacher M., 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., Gahr M., Surlemont C. (1989) Distribution of estrogen receptors in the brain of the Japanese quail: an immunocytochemical study. Brain Res 501:205-214.
Balthazart J., Evrard L., Surlemont C. (1990) Effects of the nonsteroidal inhibitor R76713 on testosterone-induced sexual behavior in the Japanese quail (Coturnix coturnix japonica). Horm Behav 24:510-531.
Balthazart J., Foidart A., Harada N. (1990) Immunocytochemical localization of aromatase in the brain. Brain Res 514:327-333.
Balthazart J., Foidart A., Surlemont C., Vockel A., Harada N. (1990) 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., Surlemont C., Harada N. (1991) Neuroanatomical specificity in the co-localization of aromatase and estrogen receptors. J Neurobiol 22:143-157.
Balthazart J., Surlemont C., Harada N. (1992) Aromatase as a cellular marker of testosterone action in the preoptic area. Physiol Behav 51:395-409.
Baylé J.D., Ramade F., Oliver J. (1974) Stereotaxic topography of the brain of the quail (Coturnix coturnix japonica). J Physiol (Paris) 68:219-241.
Berk M.L. (1987) Projections of the lateral hypothalamus and bed nucleus of the stria terminalis to the dorsal vagal complex in the pegeon. J Comp Neurol 260:140-156.
Berk M.L., Butler A.B. (1981) Efferent projections of the medial preoptic nucleus and medial hypothalamus in the pigeon. J Comp Neurol 203:379-399.
Berk M.L., Finkelstein J.A. (1983) Long descending projections of the hypothalamus in the pigeon Columba livia. J Comp Neurol 220:127-136.
Cederbaum J.M., Aghajanian G.K. (1978) Afferent projections of the rat locus coeruleus as determined by a retrograde technique. The Journal of Comparative Neurology 178:1-16.
Chan A., Webb R.M., Yang C.M., Jin C.B. (1987) The effect of estrogen on the luteinizing hormone-releasing hormone binding sites in hypothalamic membranes. Neuropharmacology 26:1395-1401.
Chiba T., Murata Y. (1985) Afferent and efferent connections of the medial preoptic area in the rat: a WGA-HRP study. Brain Res Bull 14:261-272.
Commins D., Yahr P. (1984) Adult testosterone levels influence the morphology of a sexually dimorphic area in the Mongolian gerbil brain. J Comp Neurol 224:132-140.
Commins D., Yahr P. (1984) Lesions of the sexually dimorphic area disrupt mating and marking in male gerbils. Brain Res Bull 13:185-193.
Condon T.P., Handa R.J., Gorski R.A., Sawyer C.H., Whitmoyer D.I. (1986) Ovarian steroid modulation of norepinephrine action on luteinizing hormone release. Analogous effects in male and female rats. Neuroendocrinology 43:550-556.
Conrad L.C.A., Pfaff D.W. (1976) Efferents from medial basal forebrain and hypothalamus in the rat. An autoradiographic study of the medial preoptic area. J Comp Neurol 169:185-220.
Crosby E.C., Showers M.J.C. (1969) Comparative anatomy of the preoptic and hypothalamic areas. The hypothalamus , W., Haymaker, E., Anderson, W.T.H., Nauta, Thomas, Springfield; 61-13.
Dahlström A., Fuxe K. (1964) Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brainstem neurons. Acta Physiol Scand 62:1-55.
De Jonge F.H., Louwerse A.L., Oo M.P., Evers P., Endert E., Van De Poll N.E. (1990) Lesions of the SDN-POA inhibit sexual behavior of male Wistar rats. Brain Res Bull 23:483-492.
De Vries G.J., Gonzales C.L., Yahr P. (1988) Afferent connections of the sexually dimorphic area of the hypothalamus of male and female gerbils. J Comp Neurol 271:91-105.
Dornan W.A., Malsbury C.W. (1989) Neuropeptides and male sexual behavior. Neurosci Biobehav Rev 13:1-15.
Fahrbach S.E., Morrell J.I., Pfaff D.W. (1986) Identification of medial preoptic neurons that concentrate estradiol and project to the midbrain in the rat. J Comp Neurol 247:364-382.
Fink G. (1988) Steroid control of brain and pituitary function. Q J Exp Physiol 73:257-293.
Fink G., Rosie R., Thoon E. (1991) Steroid actions on hypothalamic neurons with special reference to estrogen control of luteinizing hormone releasing hormone biosynthesis and release. Volume transmission in the brain: novel mechanisms for neural transmission , K., Fuxe, L.F., Agnati, Raven Press, New York; 195-211.
.
Foster R.G., Panzica G.C., Parry D.M., Viglietti-Panzica C. (1988) Immunocytochemical studies on the LHRH system of the Japanese quail: influence by photoperiod and aspects of sexual differentiation. Cell Tissue Res 253:327-335.
van Gils J., Absil P., Grauwels L., Vandesande F., Balthazart J. (1993) Distribution of luteinizing hormone-releasing hormones I and II (LHRH-I and II) in the quail and chicken brain: an immunocytochemical study using antibodies directed against synthetic peptides. J Comp Neurol 334:304-323.
Godement P., Vanselow J., Thanos S., Bonhoeffer F. (1987) A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development 101:697-713.
Gorski R.A., Harlan R.E., Jacobson C.D., Shryne J.E., Southam A.M. (1980) Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat. J Comp Neurol 193:529-539.
Hart B. (1986) Medial preoptic-anterior hypothalamic lesions and sociosexual behavior of male goats. Physiol Behav 36:301-305.
Hines M., Davis F.C., Coquelin A., Goy R.W., Gorski R.A. (1985) Sexually dimorphic regions in the medial preoptic area and the bed nucleus of the stria terminalis of the guinea pig brain: a description and an investigation of their relationship to gonadal steroids in adulthood. J Neurosci 5:40-47.
Holmqvist B.I., Östholm T., Ekström P. (1992) DiI tracing in combination with immunocytochemistry for analysis of connectivities and chemoarchitectonics of specific neural systems in a teleost, the Atlantic salmon. J Neurosci Methods 42:45-63.
Honig M.G., Hume R.I. (1989) DiI and DiO: versatile fluorescent dyes for neuronal labelling and pathway tracing. Trends Neurosci 12:333-341.
Johnson F., Bottjer S.W. (1992) Growth and regression of thalamic efferents in the song-control system of male zebra finches. J Comp Neurol 326:442-450.
Kelly M.J., Ronnekleiv O.K., Eskay R.L. (1984) Identification of estrogen-responsive LHRH neurons in the guinea pig hypothalamus. Brain Res Bull 12:399-407.
Kelly M.J., Garrett J., Bosch M.A., Roselli C.E., Douglass J., Adelman J.P., Ronnekleiv O.K. (1989) Effects of ovariectomy on GnRH mRNA, proGnRH and GnRH levels in the preoptic hypothalamus of the female rat. Neuroendocrinology 49:88-97.
Kiss J.Z. (1988) Dynamism of chemoarchitecture in the hypothalamic paraventricular nucleus. Brain Res Bull 20:699-708.
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.
Kitt C.A., Brauth S.E. (1981) Projections of the paleostriatum upon the midbrain tegmentum in the pigeon. Neuroscience 6:1551-1556.
Korf H.W. (1984) Neuronal organization of the avian paraventricular nucleus: intrinsic, afferent, and efferent connections. J Exp Zool 232:387-395.
Kuenzel W.J., Masson M. A stereotaxic atlas of the brain of the chick (Gallus domesticus) , Johns Hopkins University Press, Baltimore London; 1988, 1-165.
Kuenzel W.J., van Tienhoven A. (1982) Nomenciature and location of avian hypothalamic nuclei and associated circumventricular organs. J Comp Neurol 206:293-313.
Mikami S.I., Yamada S., Hasegawa Y., Miyamoto K. (1988) Localization of avian LHRH-immunoreactive neurons in the hypothalamus of the domestic fowl, Gallus domesticus, and the Japanese quail, Coturnix coturnix japonica. Cell Tissue Res 251:51-58.
Naftolin F., MacLusky N.J., Leranth C., Sakamoto H.S., Garcia-Segura L.M. (1988) The cellular effects of estrogens on neuroendocrine tissues. J Steroid Biochem 30:195-207.
.
Nottebohm F., Arnold A.P. (1976) Sexual dimorphism in vocal control areas of the songbird brain. Science 194:211-213.
Ohtsuka S., Nishizaki T., Tasaka K., Miyake A., Tanizawa O., Yamatodani A., Wada H. (1989) Estrogen stimulates gonadotropinreleasing hormone release from rat hypothalamus independently through catecholamine and histamine in vitro. Acta Endocrinol (Copenh) 120:644-648.
Orchinik M., McEwen B.S. (1993) Novel and classical actions of neuroactive steroids. Neurotransmission 9:1-6.
Panzica G.C., Viglietti-Panzica C., Calcagni M., Anselmetti G.C., Schumacher M., Balthazart J. (1987) Sexual differentiation and hormonal control of the sexually dimorphic medial preoptic nucleus in quail. Brain Res 416:59-68.
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.
Panzica G.C., Viglietti-Panzica C., Sánchez 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 G.C., Aste N., Viglietti-Panzica C., Fasolo A. (1992) Neuronal circuits controlling quail sexual behavior. Chemical neuroanatomy of the septo-preoptic region. Poultry Sci Rev 4:249-259.
Reiner A., Karten H.J., Solina A.R. (1983) Substance P: localization within paleostriatal-tegmental pathways in the pigeon. Neuroscience 9:61-85.
Ricardo J.A., Koh E.T. (1978) Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala and other forebrain structures in the rat. Brain Res 153:1-26.
Rivzi T.A., Ennis M., Shipley M. (1992) Reciprocal connections between the medial preoptic area and the midbrain periaqueductal gray in rat: a WGA-HRP and PHA-L study. The Journal of Comparative Neurology 315:1-15.
Sachs B.D. (1969) Photoperiodic control of reproductive behavior and physiology of the male Japanese quail. Horm Behav 1:7-24.
Sachs B.D., Meisel R.L. (1988) The physiology of male sexual behavior. The physiology of reproduction , E., Knobil, J., Neill, Raven Press, New York; 1393-1485.
Schlinger B.A., Callard G.V. (1989) Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain. Neuroendocrinology 49:434-441.
Schumacher M. (1990) Rapid membrane effects of steroid hormones: an emerging concept in neuroendocrinology. Trends Neurosci 13:359-362.
Shivers B.D., Harlan R.E., Morrell J.I., Pfaff D.W. (1983) Absence of oestradiol concentration in cell nuclei of LHRH-immunoreactive neurones. Nature 304:345-347.
Simerly R.B., Swanson L.W. (1988) Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tracttracing study in the rat. J Comp Neurol 270:209-242.
Sterling R.J., Gasc J.M., Sharp P.J., Tuohimaa P., Baulieu E.E. (1984) Absence of nuclear progesterone receptor in LH releasing hormone neurones in laying hens. Journal of Endocrinology 102:R5-R7.
Swaab D.F., Fliers E. (1985) A sexually dimorphic nucleus in the human brain. Science 228:1112-1115.
Swanson L.W., Sawchenko P.E. (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6:269-324.
Ter Horst G.J., de Boer P., Luiten P.G.M., Van Willigen J.D. (1989) Ascending projections from the solitary tract nucleus to the hypothalamus. A Phaseolus vulgaris lectin tracing study. Neuroscience 31:785-797.
Tobet S.A., Zahineser D.J., Baum M.J. (1986) Sexual dimorphism in the preoptic/anterior hypothalamic area of ferrets: effects of adult exposure to sex steroids. Brain Res 364:249-257.
Turkenburg J.L., Swaab D.F., Endert E., Louwerse A.L., Van De Poll N.E. (1988) Effects of lesions of the sexually dimorphic nucleus on sexual behavior of testosterone-treated female Wistar rats. Brain Res Bull 21:215-224.
Van Eerdenburg F.J.C.M., 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., Panzica G.C., Fiori M.G., Calcagni M., Anselmetti G.C., Balthazart J. (1986) A sexually dimorphic nucleus in the quail preoptic area. Neurosci Lett 64:129-134.
Voorhuis T.A.M., De Kloet E.R. (1992) Immunoreactive vasotocin in the zebra finch brain (Taeniopygia guttata). Dev Brain Res 69:1-10.
Watson J.T., Adkins Regan E.K. (1988) 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.
Yahr P. (1985) Searching for neural correlates of sexual differentiation in a heterogeneous tissue. Comparative neurobiology , R., Gilles, J., Balthazart, Springer, Berlin Heidelberg; 180-202.
Yahr P. (1993) Sexually dimorphic hypothalamic cell groups and a related pathway that are essential for masculine copulatory behavior. The development of sex differences and similarities in behavior , M., Haug, R.E., Whalen, C., Aron, K.L., Olsen, Kluwer, Dordrecht NL; 409-419.
Yahr P., Finn P.D. (1990) Connections of the sexually dimorphic area of the gerbil hypothalamus: possible pathways for hormonal control of male sexual behavior and scent-marking. Hormones, brain and behaviour in vertebrates. 1. Sexual differentiation, neuroanatomical aspects, neurotransmitters and neuropeptides , J., Balthazart, Karger, Basel New York; 137-147.
Yahr P., Stephens D.R. (1987) Hormonal control of sexual and scent marking behaviors of male gerbils in relation to the sexually dimorphic area of the hypothalamus. Horm Behav 21:331-346.
