[en] Steroids are generally viewed as transcription factors binding to intracellular receptors and activating gene transcription. Rapid cellular effects mediated via non-genomic mechanisms have however been identified and one report showed that injections of estradiol rapidly stimulate chemoinvestigation and mounting behavior in castrated male rats. It is not known whether such effects take place in other species and what are the cellular underlying mechanisms. We show here that a single injection of estradiol (500 wg/kg) rapidly and transiently activates copulatory behavior in castrated male quail pre-treated with a dose of testosterone behaviorally ineffective by itself. The maximal behavioral effect was observed after 15 min. In a second experiment, the brain of all subjects was immediately collected after behavioral tests performed 15 min after injection. The preoptic area-hypothalamus (HPOA), hindbrain, telencephalon and cerebellum were isolated and monoamines measured by HPLC-ED. Estradiol increased levels of the serotonin metabolite 5-hydroxyindoleacetic acid (5-HIAA) and 5-HIAA/serotonin ratios in the telencephalon and hindbrain independently of whether animals had mated or not. Estradiol also affected these measures in HPOA and cerebellum but this effect was correlated with the level of sexual activity so that significant effects of the treatment only appeared when sexual activity was used as a covariate. Interactions between estradiol effects and sexual activity were also observed for dopamine in the HPOA and for serotonin in the hindbrain and cerebellum. Together, these data demonstrate that a single estradiol injection rapidly activates male sexual behavior in quail and that this behavioral effect is correlated with changes in monoaminergic activity. (c) 2005 Elsevier B.V. All rights reserved.
Disciplines :
Neurosciences & behavior
Author, co-author :
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Dalla, C.
Papadopoulou-Daifoti, Z.
Baillien, M.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Language :
English
Title :
Estradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain
I.M. Abraham, S.-K. Han, M.G. Todman, K.S. Korach, and A.E. Herbison Estrogen receptor beta mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo J Neurosci 23 2003 5771 5777
P. Absil, S. Das, and J. Balthazart Effects of apomorphine on sexual behavior in male quail Pharmacol Biochem Behav 47 1994 77 88
P. Absil, J.B. Braquenier, J. Balthazart, and G.F. Ball Effects of lesions of nucleus taeniae on appetitive and consummatory aspects of male sexual behavior in Japanese quail Brain Behav Evol 60 2002 13 35
E.K. Adkins, and N.T. Adler Hormonal control of behavior in the Japanese quail J Comp Physiol Psychol 81 1972 27 36
T. Bailhache, and J. Balthazart The catecholaminergic system of the quail brain: immunocytochemical studies of dopamine β-hydroxylase and tyrosine hydroxylase J Comp Neurol 329 1993 230 256
G.F. Ball, and J. Balthazart Neuroendocrine mechanisms regulating reproductive cycles and reproductive behavior in birds D.W. Pfaff A.P. Arnold A.M. Etgen S.E. Fahrbach R.T. Rubin Hormones, brain and behavior vol. 2 2002 Academic Press San Diego, CA 649 798
J. Balthazart, M. Schumacher, and M.A. Ottinger Sexual differences in the Japanese quail: behavior, morphology and intracellular metabolism of testosterone Gen Comp Endocrinol 51 1983 191 207
J. Balthazart, Y. Delville, Y. Sulon, and J.C. Hendrick Plasma levels of luteinizing hormone and of five steroids in photostimulated, castrated and testosterone-treated male and female Japanese quail (Coturnix coturnix japonica) Gen Endocrinol (Life Sci Adv) 5 1986 31 36
J. Balthazart, J.M. Libioulle, and P. Sante Stimulatory effects of the noradrenergic neurotoxin DSP4 on sexual behavior in male quail Behav Process 17 1988 27 44
J. Balthazart, M. Gahr, and C. Surlemont Distribution of estrogen receptors in the brain of the Japanese quail: an immunocytochemical study Brain Res 501 1989 205 214
J. Balthazart, A. Foidart, and C. Hendrick The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior Physiol Behav 47 1990 83 94
J. Balthazart, and A. Foidart Brain aromatase and the control of male sexual behavior J Steroid Biochem Mol Biol 44 1993 521 540
J. Balthazart, C. Castagna, and G.F. Ball Differential effect of D1 and D2 dopamine-receptor agonists and antagonists on appetitive and consummatory aspects of male sexual behavior in Japanese quail Physiol Behav 62 1997 571 580
J. Balthazart, and G.F. Ball New insights into the regulation and function of brain estrogen synthase (aromatase) Trends Neurosci 21 1998 243 249
J. Balthazart, M. Baillien, and G.F. Ball Rapid and reversible inhibition of brain aromatase activity J Neuroendocrinol 13 2001 63 73
J. Balthazart, M. Baillien, and G.F. Ball Phosphorylation processes mediate rapid changes of brain aromatase activity J Steroid Biochem Mol Biol 79 2001 261 277
J. Balthazart, M. Baillien, T.D. Charlier, and G.F. Ball Calcium-dependent phosphorylation processes control brain aromatase in quail Eur J Neurosci 17 2003 1 16
J.B. Becker Estrogen rapidly potentiates amphetamine-induced striatal dopamine release and rotational behavior during microdialysis Neurosci Lett 118 1990 169 171
C.L. Bethea, N.Z. Lu, C. Gundlah, and J.M. Streicher Diverse actions of ovarian steroids in the serotonin neural system Front Neuroendocrinol 23 2002 41 100
C. Castagna, G.F. Ball, and J. Balthazart Effects of dopamine agonists on appetitive and consummatory male sexual behavior in Japanese quail Pharmacol Biochem Behav 58 1997 403 414
T.D. Charlier, G.F. Ball, and J. Balthazart Sexual behavior activates the expression of the immediate early genes c-fos and zenk (EGR-1) in catecholaminergic neurons of male Japanese quail Neuroscience 51 2005 13 30
J.W. Commissiong Monoamine metabolites: their relationship and lack of relationship to monoaminergic neuronal activity Biochem Pharmacol 34 1985 1127 1131
Cornil CA, Taziaux M, Baillien M, Ball GF, Balthazart J. Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail. Horm Behav, in press [doi:10.1016/j.yhbeh.2005.05.003].
C.A. Cornil, C. Dalla, Z. Papadopoulou-Daifoti, M. Baillien, C. Dejace, G.F. Ball, and J. Balthazart Rapid decreases in preoptic aromatase activity and brain monoamine concentrations after engaging in male sexual behavior Endocrinology 146 2005 3809 3820
B. Cozzi, C. Viglietti-Panzica, N. Aste, and G.C. Panzica The serotoninergic system in the brain of the Japanese quail. An immunohistochemical study Cell Tissue Res 263 1991 271 284
H. Cransac, J.M. Cottet-Emard, J.M. Pequignot, and L. Peyrin Monoamines (norepinephrine, dopamine, serotonin) in the rat medial vestibular nucleus: endogenous levels and turnover J Neural Transm 103 1996 391 401
E. Cross, and C.E. Roselli 17β-Estradiol rapidly facilitates chemoinvestigation and mounting in castrated male rats Am J Physiol 276 1999 R1346 R1350
K.P. Datla, and G. Curzon Effect of p-chlorophenylalanine at moderate dosage on 5-HT and 5-HIAA concentrations in brain regions of control and p-chloroamphetamine treated rats Neuropharmacology 35 1996 315 320
W.R. Dawson, and G.C. Whittow Regulation of body temperature G.C. Wittow Strukie's avian physiology 2000 Academic Press
Y. Delville, J. Sulon, and J. Balthazart Hormonal correlates of gonadal regression and spontaneous recovery in Japanese quail exposed to short day-lengths Arch Int Physiol Bioch 93 1985 123 133
T. Di Paolo, C. Rouillard, and P. Bedard 17 Beta-estradiol at a physiological dose acutely increases dopamine turnover in rat brain Eur J Pharmacol 117 1985 197 203
P.H. Driggers, and J.H. Segars Estrogen action and cytoplasmic signaling pathways. Part II. The role of growth factors and phosphorylation in estrogen signaling Trends Endocrinol Metab 13 2002 422 427
A.S. Elhwuegi Central monoamines and their role in major depression Prog Neuro-Psychopharmacol Biol Psychiatry 28 2004 435 451
Etgen AM. Estrogen regulation of neurotransmitter and growth factor signaling in the brain. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior, vol. 3. San Diego, CA: Academic Press, 2002. p. 381-440.
A. Foidart, J. Reid, P. Absil, N. Yoshimura, N. Harada, and J. Balthazart Critical re-examination 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 1995 267 282
A. Foidart, B. Lakaye, T. Grisar, G.F. Ball, and J. Balthazart Estrogen receptor-beta in quail: Cloning, tissue expression and neuroanatomical distribution J Neurobiol 40 1999 327 342
G.B. Gu, A.A. Rojo, M.C. Zee, J.H. Yu, and R.B. Simerly Hormonal regulation of CREB phosphorylation in the anteroventral periventricular nucleus J Neurosci 16 1996 3035 3044
A.E. Herbison, S.X. Simonian, N.R. Thanky, and R.J. Bicknell Oestrogen modulation of noradrenaline neurotransmission Novartis Foundation 230 2000 74 93
E.M. Hull, J. Du, D.S. Lorrain, and L. Matuszewich Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation J Neurosci 15 1995 7465 7471
E.M. Hull, D.S. Lorrain, J. Du, L. Matuszewich, L.A. Lumley, and S.K. Putnam Hormone-neurotransmitter interactions in the control of sexual behavior Behav Brain Res 105 1999 105 116
Hull EM, Meisel RL, Sachs BD. Male sexual behavior. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior, vol. 2. San Diego, CA: Academic Press, 2002. p. 1-137.
R.E. Hutchison Hormonal differentiation of sexual behavior in Japanese quail Horm Behav 11 1978 363 387
T. Improta-Brears, A.R. whorton, F. Codazzi, J.D. York, T. Meyer, and D.P. McDonnell Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium PNAS 96 1999 4686 4691
J.-M. Israel, and D.A. Poulain 17β-Oestradiol modulates in vitro electrical properties and responses to kainate of oxytocin neurones in lactating rats J Physiol 524 2000 457 470
M. Joels Steroid hormones and excitability in the mammalian brain Front Neuroendocrinol 18 1997 2 48
P.J. Karstaedt, H. Kerasidis, J.H. Pincus, R. Meloni, J. Graham, and K. Gale Unilateral destruction of dopamine pathways increases ipsilateral striatal serotonin turnover in rats Exp Neurol 126 1994 25 30
M.J. Kelly, R.L. Moss, and C.A. Dudley The effects of microelectrophoretically applied estrogen, cortisol and acetylcholine on medial preoptic-septal unit activity throughout the estrous cycle of female rat Exp Brain Res 30 1977 53 64
Kelly MJ, Ronnekleiv OK. 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, vol. 3. San Diego: Academic Press, 2002. p. 361-80.
M.J. Kelly, J. Qiu, E.J. Wagner, and O.K. Ronnekleiv Rapid effects of estrogen on G protein-coupled receptor activation of potassium channels in the central nervous system (CNS) J Steroid Biochem Mol Biol 83 2003 187 193
I.C. Kilpatrick, M.W. Jones, and O.T. Phillipson A semiautomated analysis method for catecholamines, indoleamines, and some prominent metabolites in microdissected regions of the nervous system: an isocratic HPLC technique employing coulometric detection and minimal sample preparation J Neurochem 46 1986 1865 1876
A.H. Lagrange, O.K. Ronnekleiv, and M.J. Kelly Modulation of G protein-coupled receptors by an estrogen receptor that activates protein kinase A Mol Pharmacol 51 1997 605 612
J.J. Lambert, D. Belelli, S.E. Shepherd, M. Pistis, and J.A. Peters The selective interaction of neurosteroids with the GABAa receptor E.E. Baulieu P. Robel M. Schumacher Neurosteroids A new regulatory function in the nervous system 1999 Humana Press 125 142
D. Levesque, and T. Di Paolo Rapid conversion of high into low striatal D2-dopamine receptor agonist binding states after an acute physiological dose of 17 beta-estradiol Neurosci Lett 88 1988 113 118
A. Maggi, P. Ciana, S. Belcredito, and E. Vegeto Estrogens in the nervous system: mechanisms and non-reproductive functions Annu Rev Physiol 66 2004 291 313
M.D. Majewska, N.L. Harrison, R.D. Schwartz, J.L. Barker, and S.M. Paul Steroid hormone metabolites are barbiturate-like modulators of the GABA receptors Science 232 1986 1004 1008
M. Mas Neurobiological correlates of masculine sexual behavior Neurosci Biobehav Rev 19 1995 261 277
B.S. McEwen, and S.E. Alves Estrogen actions in the central nervous system Endocrine Rev 20 1999 279 307
P.G. Mermelstein, J.B. Becker, and D.J. Surmeier Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor J Neurosci 16 1996 595 604
T. Minami, Y. Oomura, J. Nabekura, and A. Fukuda 17β-Estradiol depolarization of hypothalamic neurons is mediated by cyclic AMP Brain Res 519 1990 301 307
A.L. Mize, and R.H. Alper Acute and long-term effects of 17β-estradiol on Gi/o coupled neurotransmitter receptor function in the female rat brain as assessed by agonist-stimulated [35S] GTPgS binding Brain Res 859 2000 326 333
A.L. Mize, L.J. Young, and R.H. Alper Uncoupling of 5-HT1A receptors in the brain by estrogens: regional variations in antagonism by ICI 182,780 Neuropharmacology 44 2003 584 591
F.L. Moore, and M. Orchinik Membrane receptors for corticosterone: a mechanism for rapid behavioral responses in an amphibian Horm Behav 28 1994 512 519
M. Morissette, D. Biron, and T. Di Paolo Effect of estradiol and progesterone on rat striatal dopamine uptake sites Brain Res Bull 25 1990 419 422
R.L. Moss, Q. Gu, and M. Wong Estrogen: non-transcriptional signaling pathway Recent Progr Horm Res 52 1997 33 69
J. Nabekura, Y. Oomura, T. Minami, K. Mizuno, and A. Fukuda Mechanism of the rapid effect of 17β-estradiol on medial amygdala neurons Science 233 1986 226 228
A. Nadal, M. Diaz, and M.A. Valverde The estrogen trinity: membrane, cytosolic, and nuclear effects News Physiol Sci 16 2001 251 255
F. Naftolin, T.L. Horvath, R.L. Jakab, C. Leranth, N. Harada, and J. Balthazart Aromatase immunoreactivity in axon terminals of the vertebrate brain Neuroendocrinol 63 1996 149 155
M.K. Österlund, and Y.L. Hurd Acute 17β-estradiol treatment down-regulates serotonin 5HT1A receptor mRNA expression in the limbic system of female rats Mol Brain Res 55 1998 169 172
G.C. Panzica, C. Viglietti-Panzica, and J. Balthazart The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on the male sexual behavior Front Neuroendocrinol 17 1996 51 125
Z. Papadopoulou-Daifotis, K. Antoniou, A. Vamvakidis, I. Kalliteraki, and D.D. Varonos Neurochemical changes in dopamine and serotonin turnover rate in discrete regions of rat brain after the administration of glycinergic compounds Acta Ther 21 1995 5 18
R.G. Paredes, and A. Agmo Has dopamine a physiological role in the control of sexual behavior? A critical review of evidence Prog Neurobiol 73 2004 179 226
C. Pasqualini, V. Olivier, B. Guibert, O. Frain, and V. Leviel Acute stimulatory effect of estradiol on striatal dopamine synthesis J Neurochem 65 1995 1651 1657
S.K. Putnam, J.F. Du, S. Sato, and E.M. Hull Testosterone restoration of copulatory behavior correlates with medial preoptic dopamine release in castrated male rats Horm Behav 39 2001 216 224
S.K. Putnam, S. Sato, and E.M. Hull Effects of testosterone metabolites on copulation and medial preoptic dopamine release in castrated male rats Horm Behav 44 2003 419 426
J. Qiu, M.A. Bosch, S.C. Tobias, D.K. Grandy, T.S. Scanlan, and O.K. Ronnekleiv Rapid signalling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C J Neurosci 23 2003 9529 9540
B.D. Sachs Photoperiodic control of the cloacal gland of the Japanese quail Science 157 1967 201 203
B.A. Schlinger, and G.V. Callard Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain Neuroendocrinol 1989 434 441
J.H. Segars, and P.H. Driggers Estrogen action and cytoplasmic signaling cascades. Part I. Membrane-associated signaling complexes Trends Endocrinol Metab 13 2002 349 354
T. Sharp, T. Zetterstrom, H.G. Series, A. Carlsson, D.G. Grahame-Smith, and U. Ungerstedt HPLC-EC analysis of catechols and indoles in rat brain dialysates Life Sci 41 1987 869 872
T.L. Thompson, and R.L. Moss Estrogen regulation of dopamine release in the nucleus accumbens: genomic- and non-genomic-mediated effects J Neurochem 62 1994 1750 1756
C.D. Toran-Allerand A plethora of estrogen receptors in the brain: where will it end? Endocrinology 145 2004 1069 1074
M.A. Valverde, P. Rojas, J. Amigo, D. Cosmelli, P. Orio, and M.I. Bahamonde Acute activation of maxi-K channels (hSlo) by estradiol binding to the b subunit Science 285 1999 1929 1931
C.B. Wade, and D.M. Dorsa Estrogen activation of cyclic adenosine 5′-monophosphatase response element-mediated transcription requires the extracellularly regulated kinase/mitogen-activated protein kinase pathway Endocrinology 144 2003 832 838
H. Wang, A.R. Ward, and J.F. Morris Oestradiol acutely stimulates exocytosis of oxytocin and vasopressin from dendrites and somata of hypothalamic magnocellular neurons Neuroscience 68 1995 1179 1188
J.J. Watters, and D.M. Dorsa Transcriptional effects of estrogen on neuronal neurotensin gene expression involve cAMP/protein kinase A-dependent signalling mechanims J Neurosci 18 1998 6672 6680
C.H.R. Wetzel, B. Hermann, C. Behl, E. Pestel, G. Rammes, and W. Zieglgänsberger Functional antagonism of gonadal steroids at the 5-hydroxytryptamine type 3 receptor Mol Endocrinol 12 1998 1441 1451
Y. Zhou, J.J. Watters, and D.M. Dorsa Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain Endocrinology 137 1996 2163 2166
