Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action

[en] In many species, copulatory behavior and appetitive (anticipatory/motivational) aspects of male sexual behavior are activated by the action in the preoptic area of estrogens locally produced by testosterone aromatization. Estrogens bind to intracellular receptors, which then act as transcription factors to activate the behavior. Accordingly, changes in aromatase activity (AA) result from slow steroid-induced modifications of enzyme transcription. More recently, rapid nongenomic effects of estrogens have been described and evidence has accumulated indicating that AA can be modulated by rapid (minutes to hour) nongenomic mechanisms in addition to the slower transcriptional changes. Hypothalamic AA is rapidly down-regulated in conditions that enhance protein phosphorylation, in particular, increases in the intracellular calcium concentration, such as those triggered by neurotransmitter (e.g., glutamate) activity. Fast changes in brain estrogens can thus be caused by aromatase phosphorylation as a result of changes in neurotransmission. In parallel, recent studies demonstrate that the pharmacological blockade of AA by specific inhibitors rapidly (within 15-45 min) down-regulates motivational and consummatory aspects of male sexual behavior in quail while injections of estradiol can rapidly increase the expression of copulatory behavior. These data collectively support an emerging concept in neuroendocrinology, namely that estrogen, locally produced in the brain, regulates male sexual behavior via a combination of genomic and nongenomic mechanisms. Rapid and slower changes of brain AA match well with these two modes of estrogen action and provide temporal variations in the estrogen's bioavailability that can support the entire range of established effects for this steroid. (C) 2004 Elsevier Inc. All rights reserved.

Disciplines :

Neurosciences & behavior
Animal psychology, ethology & psychobiology

Author, co-author :

Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau

Baillien, M.

Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau

Ball, G. F.

Language :

English

Title :

Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action

Publication date :

15 November 2004

Journal title :

Physiology and Behavior

ISSN :

0031-9384

eISSN :

1873-507X

Publisher :

Pergamon-Elsevier Science Ltd, Oxford, United Kingdom

Volume :

Issue :

Pages :

247-270

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 20 April 2009

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136

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112

Bibliography

S.E. Abdelgadir, C.E. Roselli, J.V.A. Choate, and J.A. Resko Distribution of aromatase cytochrome P450 messenger ribonucleic acid in adult rhesus monkey brains Biol. Reprod. 57 1997 772 777
P. Absil, L.V. Riters, and J. Balthazart Preoptic aromatase cells project to the mesencephalic central gray in the male Japanese quail (Coturnix japonica) Horm. Behav. 40 2001 369 383
E.K. Adkins Effects of diverse androgens on the sexual behavior and morphology of castrated male quail Horm. Behav. 8 1977 201 207
E.K. Adkins, and N.T. Adler Hormonal control of behavior in the Japanese quail J. Comp. Physiol. Psychol. 81 1972 27 36
E.K. Adkins, J.J. Boop, D.L. Koutnik, J.B. Morris, and E.E. Pniewski Further evidence that androgen aromatization is essential for the activation of copulation in male quail Physiol. Behav. 24 1980 441 446
E.K. Adkins, and B.L. Nock The effects of the antiestrogen CI-628 on sexual behavior activated by androgen and estrogen in quail Horm. Behav. 7 1976 417 429
E.K. Adkins, and E.E. Pniewski Control of reproductive behavior by sex steroids in male quail J. Comp. Physiol. Psychol. 92 1978 1169 1178
A. Agmo, and P. Södersten Sexual behavior in castrated rabbits treated with testosterone, oestradiol, DHT or oestradiol in combination with DHT J. Endocrinol. 67 1975 327 332
K.A. Albert, E. Helmer-Matyjek, A.A. Nairn, T.H. Müller, J.W. Haycock, and L.A. Greene Calcium/phospholipid-dependent protein kinase (protein kinase C) phosphorylates and activates tyrosine hydroxylase Proc. Natl. Acad. Sci. U. S. A. 81 1984 7713 7717
C. Alexandre, and J. Balthazart Effects of metabolism inhibitors, antiestrogens and antiandrogens on the androgen and estrogen induced sexual behavior in Japanese quail Physiol. Behav. 38 1986 581 591
P. Alsum, and R.W. Goy Actions of esters of T, DHT and estradiol on sexual behavior in castrated male guinea pigs Horm. Behav. 5 1974 207 218
M.M. Ames, P. Lerner, and W. Lovenberg Tyrosine hydroxylase: activation by protein phosphorylation and end product inhibition J. Biol. Chem. 253 1978 27 31
N. Aste, G.C. Panzica, P. Aimar, C. Viglietti-Panzica, A. Foidart, and J. Balthazart Implication of testosterone metabolism in the control of the sexually dimorphic nucleus of the quail preoptic area Brain Res. Bull. 31 1993 601 611
N. Aste, G.C. Panzica, C. Viglietti-Panzica, N. Harada, and J. Balthazart Distribution and effects of testosterone on aromatase mRNA in the quail forebrain: a non-radioactive in situ hybridization study J. Chem. Neuroanat. 14 1998 103 115
I. Azcoitia, A. Sierra, S. Veiga, S. Honda, N. Harada, and L.M. Garcia-Segura Brain aromatase is neuroprotective J. Neurobiol. 47 2001 318 329
G.P. Baerends Ethology R.C. Atkinson R.J. Herrnstein G. Lindzey R.D. Luce Steven's handbook of experimental psychology 2nd Edition Learning and Cognition vol. 1 1988 Wiley New York 765 830
C.J. Bagatell, J.R. Heiman, J.E. Rivier, and W.J. Bremner Effects of endogenous testosterone and estradiol on sexual behavior in normal young men J. Clin. Endocrinol. Metab. 78 1994 711 716
M. Baillien, G.F. Ball, J. Bakker, and J. Balthazart Calcium, calmodulin and aromatase: a key trio in the rapid control of estrogen concentration in the brain Abstr. - Soc. Neurosci. 33 2003 726.3
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. Ball Sex activity of castrated male rats increased by estrin administration J. Comp. Psychol. 24 1937 135 144
J. Balthazart Steroid control and sexual differentiation of brain aromatase J. Steroid Biochem. Mol. Biol. 61 1997 323 339
J. Balthazart, P. Absil, M. Gérard, D. Appeltants, and G.F. Ball Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus J. Neurosci. 18 1998 6512 6527
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, 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 Interactions between aromatase (estrogen synthase) and dopamine in the control of male sexual behavior in quail Comp. Biochem. Physiol., B 132 2002 37 55
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 1591 1606
J. Balthazart, and G.F. Ball The Japanese quail as a model system for the investigation of steroid-catecholamine interactions mediating appetitive and consummatory aspects of male sexual behavior Ann. Rev. Sex Res. 9 1998 96 176
J. Balthazart, and G.F. Ball New insights into the regulation and function of brain estrogen synthase (aromatase) TINS 21 1998 243 249
J. Balthazart, C. Castagna, and G.F. Ball Aromatase inhibition blocks the activation and sexual differentiation of appetitive male sexual behavior in Japanese quail Behav. Neurosci. 111 1997 381 397
J. Balthazart, L. Evrard, and C. Surlemont Effects of the non-steroidal aromatase inhibitor, R76713 on testosterone-induced sexual behavior in the Japanese quail (Coturnix coturnix japonica) Horm. Behav. 24 1990 510 531
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, A. Foidart, and N. Harada Immunocytochemical localization of aromatase in the brain Brain Res. 514 1990 327 333
J. Balthazart, A. Foidart, and J.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, A. Foidart, C. Surlemont, and N. Harada Distribution of aromatase-immunoreactive cells in the mouse forebrain Cell Tissue Res. 263 1991 71 79
J. Balthazart, A. Foidart, C. Surlemont, and N. Harada Neuroanatomical specificity in the co-localization of aromatase and estrogen receptors J. Neurobiol. 22 1991 143 157
J. Balthazart, A. Foidart, C. Surlemont, A. Vockel, and N. Harada Distribution of aromatase in the brain of the Japanese quail, ring dove, and zebra finch: an immunocytochemical study J. Comp. Neurol. 301 1990 276 288
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, R. Massa, and P. Negri-Cesi Photoperiodic control of testosterone metabolism, plasma gonadotrophins, cloacal gland growth, and reproductive behavior in the Japanese quail Gen. Comp. Endocrinol. 39 1979 222 235
J. Balthazart, J. Reid, P. Absil, A. Foidart, and G.F. Ball Appetitive as well as consummatory aspects of male sexual behavior in quail are activated by androgens and estrogens Behav. Neurosci. 109 1995 485 501
J. Balthazart, M. Schumacher, and G. Malacarne Interaction of androgens and estrogens in the control of sexual behavior in male Japanese quail Physiol. Behav. 35 1985 157 166
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, R. Stoop, A. Foidart, and N. Harada Synergistic control by androgens and estrogens of aromatase in the quail brain NeuroReport 5 1994 1729 1732
J. Balthazart, and C. Surlemont Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail Physiol. Behav. 48 1990 599 609
J. Balthazart, and C. Surlemont Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail POA Brain Res. Bull. 25 1990 7 14
J. Balthazart, C. Surlemont, and N. Harada Aromatase as a cellular marker of testosterone action in the preoptic area Physiol. Behav. 51 1992 395 409
R. Bandler, and M.T. Shipley Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? TINS 17 1994 379 389
R.J. Barfield Activation of copulatory behavior by androgen implanted into the preoptic area of the male fowl Horm. Behav. 1 1969 37 52
R.J. Barfield Activation of sexual and aggressive behavior by androgen implantation into the male ring dove brain Endocrinology 89 1971 1470 1476
F.A. Beach Copulatory behavior in prebutertally castrated male rats and its modification by estrogen administration Endocrinology 31 1942 679 683
F.A. Beach Hormones and behavior 1948 Paul B. Hoeber New York 1â€"368 pp.
F.A. Beach Characteristics of masculine "sex drive" Neb. Symp. Motiv. 4 1956 1 32
C. Beyer, G. Morali, F. Naftolin, K. Larsson, and G. Perez-Palacios Effect of some antiestrogens and aromatase inhibitors on androgen-induced sexual behavior in castrated male rats Horm. Behav. 7 1976 353 363
C. Beyer, and N. Vidal Inhibitory action of MER-25 on androgen-induced oestrus behaviour in the ovariectomized rabbit J. Endocrinol. 51 1971 401 402
J.D. Blaustein, and D.H. Olster Gonadal steroid hormone receptors and social behaviors J. Balthazart Advances in Comparative and Environmental Physiology vol. 3 1989 Springer Verlag Berlin 31 104
R.W. Bonsall, and R.P. Michael Pretreatments with 5alpha- dihydrotestosterone and the uptake of testosterone by cell nuclei in the brains of male rhesus monkeys J. Steroid Biochem. 33 1989 405 411
K. Brown-Grant, A. Munck, F. Naftolin, and M.R. Sherwood The effects of the administration of testosterone propionate alone or with phenobarbitone and of testosterone metabolites to neonatal female rats Horm. Behav. 2 1971 173 182
C. Carani, V. Rochira, M. Faustini-Fustini, A. Balestrieri, and A.R.M. Granata Role of oestrogen in male sexual behaviour: insights from the natural model of aromatase deficiency Clin. Endocrinol. 51 1999 517 524
S.G. Carriedo, H.Z. Yin, S.L. Sensi, and J.H. Weiss Rapid Ca2+ entry through Ca2+-permeable AMPA/kainate channels triggers marked intracellular Ca2+ rises and consequent oxygen radical production J. Neurosci. 18 1998 7727 7738
K.M. Cheng, A.R. Hickman, and C.R. Nichols Role of the proctodeal gland foam of male Japanese quail in natural copulations Auk 106 1989 279 285
K.M. Cheng, R.F. McIntyre, and A.R. Hickman Proctodeal gland foam enhances competitive fertilization in domestic Japanese quail Auk 106 1989 286 291
M.F. Cheng, and D. Lehrman Gonadal hormone specificity in the sexual behavior of ring doves Psychoneuroendocrinology 1 1975 95 102
L.W. Christensen, and L.G. Clemens Intrahypothalamic implants of testosterone or estradiol and resumption of masculine sexual behavior in long-term castrated male rats Endocrinology 95 1974 984 990
L.W. Christensen, and L.G. Clemens Blockade of testosterone-induce mounting behavior in the male rat with intracranial application of the aromatization inhibitor, androst-1,4,6-triene-3,17-dione Endocrinology 97 1975 1545 1551
C.J. Corbin, S. Graham-Lorence, M. McPhaul, J.I. Mason, C.R. Mendelson, and E.R. Simpson Isolation of a full-length cDNA insert encoding human aromatase system cytochrome P450 and its expression in nonsteroidogenic cells Proc. Natl. Acad. Sci. U. S. A. 85 1988 8948 8952
C.A. Cornil, H.C. Evrard, G.F. Ball, and J. Balthazart Rapid effects of 17β-Estradiol and vorozole, an aromatase inhibitor, on male sexual behavior in Japanese quail Abstr. - Soc. Neurosci. 33 2003 726.5
W. Craig Appetites and aversions as constituents of instincts Biol. Bull. 34 1918 91 107
E. Cross, and C.E. Roselli 17beta-estradiol rapidly facilitates chemoinvestigation and mounting in castrated male rats Am. J. Physiol., Regul. Integr. Comp. Physiol. 276 1999 R1346 R1350
S.C. Daubner, C. Lauriano, J.W. Haycock, and P.F. Fitzpatrick Site-directed mutagenesis of serine 40 of rat tyrosine hydroxylase J. Biol. Chem. 267 1992 12639 12646
P.G. Davis, and R.J. Barfield Activation of masculine sexual behavior by intracranial estradiol benzoate implants in male rats Neuroendocrinology 28 1979 217 227
J.F. DeBold, and C.A. Frye Genomic and non-genomic actions of progesterone in the control of female hamster sexual behavior Horm. Behav. 28 1994 445 453
P. Deviche, and M. Schumacher Behavioural and morphological dose-responses to testosterone and to 5alpha-dihydrotestosterone in the castrated male Japanese quail Behav. Processes 7 1982 107 121
M. Domjan, and S. Hall Determinants of social proximity in Japanese quail (Coturnix coturnix japonica): male behavior J. Comp. Psychol. 100 1986 59 67
M. Domjan, and S. Hall Sexual dimorphism in the social proximity behavior of Japanese quail (Coturnix coturnix japonica) J. Comp. Psychol. 100 1986 68 71
M. Domjan, and K.L. Hollis Reproductive behavior: a potential model system for adaptative specializations in learning R.C. Bolles M.D. Beecher Evolution and learning 1988 213 237 NJ, Hillsdale
H. Evrard, M. Baillien, A. Foidart, P. Absil, N. Harada, and J. Balthazart Localization and controls of aromatase in the quail spinal cord J. Comp. Neurol. 423 2000 552 564
H.C. Evrard, and J. Balthazart Aromatization of androgens into estrogens reduces response latency to a noxious thermal stimulus in male quail Horm. Behav. 45 2004 181 189
Evrard, H.C. Balthazart, J. Spinal estrogen synthesis rapidly increases responsiveness to noxious stimuli, Abst. 4th Congress of the EFIC2003.
S. Fang, K.M. Anderson, and S. Liao Receptor proteins for androgens. On the role of specific proteins in selective retention of 17-beta-hydroxy-5-alpha- androstan-3-one by rat ventral prostate in vivo and in vitro J. Biol. Chem. 244 1969 6584 6595
A. Foidart, N. Harada, and J. Balthazart Effects of steroidal and non steroidal aromatase inhibitors on sexual behavior and aromatase-immunoreactive cells and fibers in the quail brain Brain Res. 657 1994 105 123
A. Foidart, M. Houbart, N. Harada, and J. Balthazart Effects of castration and testosterone replacement on the colocalization of estrogen receptors and aromatase in the quail brain Abstr. - Soc. Neurosci. 22 1996 1588
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
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
B.K. Follett The neuroendocrine regulation of gonadotropin secretion in avian reproduction D.S. Farner Breeding biology of birds 1973 National Academy of Science Washington, DC 209 243
B.K. Follett Birds G.E. Lamming Marshall's physiology of reproduction 1984 Longman Greene Edinburgh 283 350
C.A. Frye The role of neurosteroids and non-genomic effects of progestins and androgens in mediating sexual receptivity of rodents Brain Res. Rev. 37 2001 201 222
C.A. Frye, and J.M. Vongher Progesterone has rapid and membrane effects in the facilitation of female mouse sexual behavior Brain Res. 815 1999 259 269
L.M. Garcia-Segura, A. Wozniak, I. Azcoitia, J.R. Rodriguez, R.E. Hutchison, and J.B. Hutchison Aromatase expression by astrocytes after brain injury: implications for local estrogen formation in brain repair Neuroscience 89 1999 567 578
B.A. Gladue, and L.G. Clemmens Flutamide inhibits testosterone-induced masculine sexual behavior in male and female rats Endocrinology 106 1980 1917 1922
R.A. Gorski Modification of ovulatory mechanisms by postnatal administration of estrogen to the rat Am. J. Physiol. 205 1963 842 844
R.A. Gorski, and C.A. Barraclough Effects of low dosages of androgen on the differentiation of hypothalamic regulatory control of ovulation in the rat Endocrinology 73 1963 210 216
J.M. Gray, and L. Ziemian Antiestrogen binding sites in brain and pituitary of ovariectomized rats Brain Res. 578 1992 55 60
N. Harada Cloning of a complete cDNA encoding human aromatase: immunochemical identification and sequence analysis Biochem. Biophys. Res. Commun. 156 1988 725 732
N. Harada, S. Abe-Dohmae, R. Loeffen, A. Foidart, and J. Balthazart Synergism between androgens and estrogens in the induction of aromatase and its messenger RNA in the brain Brain Res. 622 1993 243 256
N. Harada, K. Yamada, A. Foidart, and J. Balthazart Regulation of aromatase cytochrome P450 (estrogen synthetase) transcripts in the quail brain by testosterone Mol. Brain Res. 15 1992 19 26
C.F. Harding, K. Sheridan, and M.J. Walters Hormonal specificity and activation of sexual behavior in male zebra finches Horm. Behav. 17 1983 111 133
C.F. Harding, M.J. Walters, D. Collado, and K. Sheridan Hormonal specificity and activation of social behavior in male red-winged blackbirds Horm. Behav. 22 1988 402 418
Y. Hattori, I. Shibuya, K. Tanaka, N. Kabashima, Y. Ueta, and H. Yamashita Ionotropic and metabotropic glutamate receptor agonist-induced [Ca2+]i increase in isolated rat supraoptic neurons J. Neuroendocrinol. 10 1998 383 389
C. Hiemke, and R. Ghraf Interaction of non-steroidal antiestrogens with dopamine receptor binding J. Steroid Biochem. 21 1984 663 667
Z. Hochberg, T. Bick, R. Pelman, J.M. Brandes, and D. Barzilai The dual effect of calcium on aromatization by cultured human trophoblast J. Steroid Biochem. 24 1986 1217 1219
J.B. Hutchison Effects of hypothalamic implants of gonadal steroids on courtship behaviour in Barbary doves (Streptopelia risoria) J. Endocrinol. 50 1971 97 113
J.B. Hutchison Hypothalamic regulation of male sexual responsiveness to androgen J.B. Hutchison Biological determinants of sexual behaviour 1978 Wiley Chichester 277 319
J.B. Hutchison, and T.H. Steimer Formation of behaviorally effective 17beta-estradiol in the dove brain: steroid control of preoptic aromatase Endocrinology 118 1986 2180 2187
R.E. Hutchison Hormonal differentiation of sexual behavior in Japanese quail Horm. Behav. 11 1978 363 387
M. Inaba, and K. Kamata Effect of estradiol-17b and other steroids on noradrenaline and dopamine binding to synaptic membrane fragments of rat brain J. Steroid Biochem. 11 1979 1491 1497
R.L. Jakab, T.L. Horvath, C. Leranth, N. Harada, and F. Naftolin Aromatase immunoreactivity in the rat brain: gonadectomy-sensitive hypothalamic neurons and an unresponsive "limbic ring" of the lateral septum-bed nucleus-amygdala complex J. Steroid Biochem. Mol. Biol. 44 1993 481 498
M. Joëls Steroid hormones and excitability in the mammalian brain Front. Neuroendocrinol. 18 1997 2 48
M.J. Kelly, and O.K. Ronnekleiv Rapid membrane effects of estrogen in the central nervous system D.W. Pfaff A.P. Arnold A.M. Etgen S.E. Fahrbach R.T. Rubin Hormones, Brain and Behavior vol. 3 2002 Academic Press San Diego 361 380
S. Kirischuk, F. Kirschhoff, V. Matyash, H. Kettenmann, and A. Verkhratsky Glutamate-triggered calcium signalling in mouse Bergmann glial cells in situ: role of inositol-1,4,5-triphosphate-mediated intracellular calcium release Neuroscience 92 1999 1051 1059
E. Küppers, T. Ivanova, M. Karolczak, and C. Beyer Estrogen: a multifunctional messenger to nigrostriatal dopaminergic neurons J. Neurocytology 29 2000 375 385
E. Küppers, T. Ivanova, M. Karolczak, N. Lazarov, K. Föhr, and C. Beyer Classical and nonclassical estrogen action in the developing midbrain Horm. Behav. 40 2001 196 202
B. Lakaye, A. Foidart, T. Grisar, and J. Balthazart Partial cloning and distribution of estrogen receptor beta in the avian brain NeuroReport 9 1998 2743 2748
R.D. Lisk Diencephalic placement of estradiol and sexual receptivity in the female rat Am. J. Physiol. 203 1962 493 496
R.D. Lisk Neural localization for androgen activation of copulatory behavior in the male rat Endocrinology 80 1967 754 761
K. Lorenz The comparative method in studying innate behavior patterns Symp. Soc. Exp. Biol. 4 1950 221 268
W.G. Luttge Endocrine control of mammalian male sexual behavior: an analysis of the potential role of testosterone metabolites C. Beyer Endocrine control of sexual behavior 1979 Raven Press New York 341 363
W.G. Luttge, and N.R. Hall Androgen-induced agonistic behavior in castrate male Swissâ€"Webster mice: comparison of four naturally occurring androgens Behav. Biol. 8 1973 725 732
W.G. Luttge, and R.E. Whalen Dihydrotestosterone, androstenedione, testosterone: comparative effectiveness in masculinizing and defeminizing reproductive systems in male and female rats Horm. Behav. 1 1970 265 281
N.J. MacLusky, A. Philip, C. Hurlburt, and F. Naftolin Estrogen metabolism in neuroendocrine structures F. Celotti F. Naftolin L. Martini Metabolism of hormonal steroids in the neuroendocrine structures 1984 Raven Press New York 103 116
L. Martini The 5Î±-reduction of testosterone in the neuroendocrine structures. Biochemical and physiological implications Endocr. Rev. 3 1982 1 25
P. McDonald, C. Beyer, F. Newton, B. Brien, R. Baker, and H.S. Tan Failure of 5Î±-dihydrotestosterone to initiate sexual behavior in the castrated male rat Nature 277 1970 964 965
B.S. McEwen Steroid hormone actions on the brain: when is the genome involved? Horm. Behav. 28 1994 396 405
M.J. McPhaul, J.F. Noble, E.R. Simpson, C.R. Mendelson, and J.D. Wilson The expression of a functional cDNA encoding the chicken cytochrome P450arom (aromatase) that catalyzes the formation of estrogen from androgen J. Biol. Chem. 263 1988 16358 16363
G.D. Means, M.S. Mahendroo, C.J. Corbin, J.M. Mathis, F.E. Powell, and C.R. Mendelson Structural analysis of the gene encoding human aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis J. Biol. Chem. 264 1989 19385 19391
R.L. Meisel, and B.D. Sachs The physiology of male sexual behavior E. Knobil J.D. Neill The physiology of reproduction vol. 2 1994 Raven Press New York 3 105
S.D. Mendelson, and B.B. Gorzalka An improved chamber for the observation and analysis of the sexual behavior of the female rat Physiol. Behav. 39 1987 67 71
S.D. Mendelson, and J.G. Pfaus Level searching: a new assay of sexual motivation in the male rat Physiol. Behav. 45 1989 337 341
P.G. Mermelstein, and J.B. Becker Increased extracellular dopamine in the nucleus accumbens and striatum of the female rat during paced copulatory behavior Behav. Neurosci. 109 1995 354 365
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
R.P. Michael, R.W. Bonsall, and D. Zumpe Testosterone and its metabolites in male cynomolgus monkeys (Macaca fascicularis): behavior and biochemistry Physiol. Behav. 40 1987 527 537
R.P. Michael, H.D. Rees, and R.W. Bonsall Sites in the male primate brain at which testosterone acts as an androgen Brain Res. 502 1989 11 20
G. Morali, K. Larsson, and C. Beyer Inhibition of testosterone-induced sexual behavior in the castrated male rat by aromatase blockers Horm. Behav. 9 1977 203 213
R.L. Moss, Q. Gu, and M. Wong Estrogen: nontranscriptional signaling pathway Rec. Prog. Horm. Res. 52 1997 33 69
A.Z. Murphy, and G.E. Hoffman Distribution of gonadal steroid receptor-containing neurons in the preoptic-periaqueductal gray-brainstem pathway: a potential circuit for the initiation of male sexual behavior J. Comp. Neurol. 438 2001 191 212
A.Z. Murphy, T.A. Rizvi, M. Ennis, and M.T. Shipley The organization of preoptic-medullary circuits in the male rat: evidence for interconnectivity of neural structures involved in reproductive behavior, antinociception and cardiovascular regulation Neuroscience 91 1999 1103 1116
F. Naftolin, and J.R. Brawer The effect of estrogens on hypothalamic structure and function Am. J. Obstet. Gynecol. 132 1978 758 765
F. Naftolin, L.M. Garcia-Segura, D. Keefe, C. Leranth, N.J. MacLusky, and J.R. Brawer Estrogen effects on the synaptology and neural membranes of the rat hypothalamic arcuate nucleus Biol. Reprod. 42 1990 21 28
F. Naftolin, T.L. Horvath, R.L. Jakab, C. Leranth, N. Harada, and J. Balthazart Aromatase immunoreactivity in axon terminals of the vertebrate brainâ€"an immunocytochemical study on quail, rat, monkey and human tissues Neuroendocrinology 63 1996 149 155
F. Naftolin, K.J. Ryan, I.J. Davies, V.V. Reddy, F. Flores, and Z. Petro The formation of estrogens by central neuroendocrine tissues Rec. Prog. Horm. Res. 31 1975 295 319
F. Naftolin, K.J. Ryan, and Z. Petro Aromatization of androstenedione by the anterior hypothalamus of adult male and female rats Endocrinology 90 1972 295 298
K.-I. Ohtani, H. Sakurai, E. Oh, E. Iwata, T. Tsuchiya, and M. Tsuda Involvement of protein kinase C in Ca2+-signaling pathways to activation of AP-1 DNA-binding activity evoked via NMDA- and voltage-gated Ca2+ channels J. Neurochem. 65 1995 605 614
O.M. Onagbesan, and M.J. Podie Calcium-dependent stimulation of estrogen secretion by FSH from theca cells of the domestic hen (Gallus domesticus) Gen. Comp. Endocrinol. 75 1989 177 186
Y. Osawa, T. Higashiyama, Y. Shimizu, and C. Yarborough Multiple functions of aromatase and the active site structure; Aromatase is the placental estrogen 2-hydroxylase J. Steroid Biochem. Mol. Biol. 44 1993 469 480
G.C. Panzica, N. Aste, A. Coscia, W. De Bernardi, C. Viglietti-Panzica, and J. Balthazart A sex-dependent influence of testosterone on the dorso-medial neuronal population of the Japanese quail Intercollicular nucleus J. Hirnforsch. 32 1991 469 475
G.C. Panzica, G. Malacarne, A. De Bernochi, and G.C. Viglietti-Panzica Effects of steroid hormones on the neuropil of the hypothalamic paraventricular nucleus of male chickens Cell Tissue Res. 240 1985 169 174
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 male sexual behavior Front. Neuroendocrinol. 17 1996 51 125
G.C. Panzica, C. Viglietti-Panzica, M. Calcagni, G.C. Anselmetti, M. Schumacher, and J. Balthazart Sexual differentiation and hormonal control of the sexually dimorphic preoptic medial nucleus in quail Brain Res. 416 1987 59 68
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
R.S. Peterson, C.J. Saldanha, and B.A. Schlinger Rapid upregulation of aromatase mRNA and protein following neural injury in the zebra finch (Taeniopygia guttata) J. Neuroendocrinol. 13 2001 317 323
D. Pfaff Nature of sex hormone effects on rat sex behavior: specificity of effects and individual patterns of response J. Comp. Physiol. Psychol. 73 1970 349 358
D. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, and R.T. Rubin Hormones, brain and behavior 2002 Academic Press Amsterdam
J.G. Pfaus Frank A. Beach Awardâ€"homologies of animal and human sexual behaviors Horm. Behav. 30 1996 187 200
J.G. Pfaus, S.D. Mendelson, and A.G. Phillips A correlational and factor analysis of anticipatory and consummatory measures of sexual behavior in the male rat Psychoneuroendocrinology 15 1990 329 340
R.E. Phillips, and R.J. Barfield Effects of testosterone implants in midbrain vocal areas of capons Brain Res. 122 1977 378 381
C.H. Phoenix Effects of DHT on sexual behavior of castrated rhesus monkeys Physiol. Behav. 12 1974 1045 1055
C.H. Phoenix, and K.C. Chambers Sexual behavior in adult gonadectomized female pseudohermaphrodite, female, and male rhesus macaques (Macaca mulatta) treated with estradiol benzoate and testosterone propionate J. Comp. Physiol. Psychol. 96 1982 823 833
V.D. Ramirez, J.B. Zheng, and K.M. Siddique Membrane receptors for estrogen, progesterone, and testosterone in the rat brain: fantasy or reality Cell. Mol. Neurobiol. 16 1996 175 198
V.V.R. Reddy, F. Naftolin, and K.J. Ryan Conversion of androstenedione to estrone by neural tissues from fetal and neonatal rats Endocrinology 94 1974 117 121
L.V. Riters, P. Absil, and J. Balthazart Effects of brain testosterone implants on appetitive and consummatory components of male sexual behavior in Japanese quail Brain Res. Bull. 47 1998 69 79
T.A. Rizvi, M. Ennis, and M.T. Shipley Reciprocal connections between the medial preoptic area and the midbrain periaqueductal gray in rat: a WGA-HRP and PHA-L study J. Comp. Neurol. 315 1992 1 15
T.A. Rizvi, A.Z. Murphy, M. Ennis, M.M. Behbehani, and M.T. Shipley Medial preoptic area afferents to periaqueductal gray medullo-output neurons: a combined Fos and tract tracing study J. Neurosci. 16 1996 333 344
V. Rochira, M. Faustini-Fustini, A. Balestrieri, and C. Carani Estrogen replacement therapy in a man with congenital aromatase deficiency: effects of different doses of transdermal estradiol on bone mineral density and hormonal parameters J. Clin. Endocrinol. Metab. 85 2000 1841 1845
C.E. Roselli Synergistic induction of aromatase activity in the rat brain by estradiol and 5alpha-dihydrotestosterone Neuroendocrinology 53 1991 79 84
C.E. Roselli Subcellular localization and kinetic properties of aromatase activity in rat brain J. Steroid Biochem. Mol. Biol. 52 1995 469 477
C.E. Roselli, S.E. Abdelgadir, E. Jorgensen, and J.A. Resko Sex differences in androgen-regulated cytochrome P450 aromatase mRNA in the rat brain Endocrine 5 1996 59 65
C.E. Roselli, S.E. Abdelgadir, and J.A. Resko Regulation of aromatase gene expression in the adult rat brain Brain Res. Bull. 44 1997 351 357
C.E. Roselli, E. Cross, H.K. Poonyagariyagorn, and H.L. Stadelman Role of aromatization in anticipatory and consummatory aspects of sexual behavior in male rats Horm. Behav. 44 2003 146 151
C.E. Roselli, L.E. Horton, and J.A. Resko Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system Endocrinology 117 1985 2471 2477
C.E. Roselli, L.E. Horton, and J.A. Resko Time-course and steroid specificity of aromatase induction in rat hypothalamus-preoptic area Biol. Reprod. 37 1987 628 633
C.E. Roselli, S.A. Klosterman, and J.A. Resko Anatomic relationships between aromatase and androgen receptor mRNA expression in the hypothalamus and amygdala of adult male cynomolgus monkeys J. Comp. Neurol. 439 2001 208 223
C.E. Roselli, and J.A. Resko Androgens regulate brain aromatase activity in adult male rats through a receptor mechanism Endocrinology 114 1984 2183 2189
C.E. Roselli, F. Stormshak, and J.A. Resko Distribution of aromatase mRNA in the ram hypothalamus: an in situ hybridization study J. Neuroendocrinol. 12 2000 656 664
B.D. Sachs Photoperiodic control of the cloacal gland of the Japanese quail Science 157 1967 201 203
B.D. Sachs Context-sensitive variation in the regulation of erection J. Bancroft The pharmacology of sexual function and dysfunction 1995 Elsevier Amsterdam 97 108
B.D. Sachs Placing erection in context: the reflexogenicâ€ "psychogenic dichotomy reconsidered Neurosci. Biobehav. Rev. 19 1995 211 224
C.J. Saldanha, R.S. Peterson, L. Yarram, and B.A. Schlinger The synaptocrine hypothesis: a novel mechanism of estrogen delivery Horm. Behav. 44 2003 74
M.K. Sanghera, E.R. Simpson, M.J. McPhaul, G. Kozlowski, A.J. Conley, and E.D. Lephart Immunocytochemical distribution of aromatase cytochrome P450 in the rat brain using peptide-generated polyclonal antibodies Endocrinology 129 1991 2834 2844
B.A. Schlinger, S. Amur-Umarjee, P. Shen, A.T. Campagnoni, and A.P. Arnold Neuronal and non-neuronal aromatase in primary cultures of developing zebra finch telencephalon J. Neurosci. 14 1994 7541 7552
B.A. Schlinger, and G.V. Callard Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain Neuroendocrinology 49 1989 434 441
B.A. Schlinger, and G.V. Callard Aromatization mediates aggressive behavior in quail Gen. Comp. Endocrinol. 79 1990 39 53
M. Schumacher Rapid membrane effects of steroid hormones: an emerging concept in neuroendocrinology TINS 13 1990 359 362
M. Schumacher, C. Alexandre, and J. Balthazart Interactions des androgènes et des oestrogènes dans le contrôle de la reproduction C. R. Acad. Sci., Paris, Série III 305 1987 569 574
M. Schumacher, and J. Balthazart The effects of testosterone and its metabolites on sexual behavior and morphology in male and female Japanese quail Physiol. Behav. 30 1983 335 339
M. Schumacher, and J. Balthazart Neuroanatomical distribution of testosterone metabolizing enzymes in the Japanese quail Brain Res. 422 1987 137 148
C.M. Seiwert The neuromuscular system controlling foam production in Japanese quail: an investigation of structure and function 1994 Cornell University Ithaca, NY 241 pp.
C.M. Seiwert, and E. Adkins-Regan The foam production system of the male Japanese quail: characterization of structure and function Brain Behav. Evol. 52 1998 61 80
P. Shen, C.W. Campagnoni, K. Kampf, B.A. Schlinger, A.P. Arnold, and A.T. Campagnoni Isolation and characterization of a zebra finch aromatase cDNA: in situ hybridization reveals high aromatase expression in brain Mol. Brain Res. 24 1994 227 237
K. Shinoda, M. Nagano, and Y. Osawa An aromatase-associated cytoplasmic inclusion, the "stigmoid body," in the rat brain: II. Ultrastructure (with a review of its history and nomenclature) J. Comp. Neurol. 329 1993 1 19
K. Shinoda, M. Nagano, and Y. Osawa Neuronal aromatase expression in preoptic, strial, and amygdaloid regions during late prenatal and early postnatal development in the rat J. Comp. Neurol. 343 1994 113 129
K. Shinoda, T. Ohtsuki, M. Nagano, and T. Okumura A possible functional necklace formed by placental antigen X-P2-immunoreactive and intensely acetylcholinesterase-reactive (PAX/IAE) glomerular complexes in the rat olfactory bulb Brain Res. 618 1993 160 166
P. Södersten Estrogen-activated sexual behavior in male rats Horm. Behav. 4 1973 247 256
P. Södersten, and J.A. Gustafsson A way in which estradiol might play a role in the sexual behavior of male rats Horm. Behav. 14 1980 271 274
K.K. Soma, K. Sullivan, and J. Wingfield Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the nonbreeding season Gen. Comp. Endocrinol. 115 1999 442 453
K.K. Soma, A.D. Tramontin, and J.C. Wingfield Oestrogen regulates male aggression in the non-breeding season Proc. R. Soc. Lond. [Biol.] 267 2000 1089 1096
T. Steimer Aromatase activity in rat brain synaptosomes. Is an enzyme associated with the neuronal cell membrane involved in mediating non-genomic effects of androgens Eur. J. Neurosci., Suppl. 9 1988 (Abstract)
T. Steimer, and J.B. Hutchison Androgen increases formation of behaviourally effective oestrogen in dove brain Nature 292 1981 345 347
T. Steimer, and J.B. Hutchison Micromethods for the in vitro study of steroid metabolism in the brain using radiolabelled tracers B. Greenstein Neuroendocrine Research Methods vol. 2 1991 Harwood Academic Publishers Chur, Switzerland 875 919
M. Taziaux, C.A. Cornil, and J. Balthazart Aromatase inhibition blocks the expression of sexually-motivated cloacal gland movements in male quail Behav. Processes 2004 (in press)
R.R. Thompson, and E. Adkins Regan Ontogeny of a sexually dimorphic nucleus in the preoptic area of the Japanese quail (Coturnix japonica) Dev. Brain Res. 70 1992 231 237
R.R. Thompson, J.L. Goodson, M.G. Ruscio, and E. Adkins-Regan Role of the archistriatal nucleus taeniae in the sexual behavior of male Japanese quail (Coturnix japonica): a comparison of function with the medial nucleus of the amygdala in mammals Brain Behav. Evol. 51 1998 215 229
T.L. Thompson, and R.L. Moss Estrogen regulation of dopamine release in the nucleus accumbens: genomic- and nongenomic-mediated effects J. Neurochem. 62 1994 1750 1756
R.J.M. Timmers, J.C.M. Granneman, J.G.D. Lambert, and P.G.W.J. van Oordt Estrogen-2-hydroxylase in the brain of the male African catfish, Clarias gariepinus Gen. Comp. Endocrinol. 72 1988 190 203
R.J.M. Timmers, and J.G.D. Lambert Kinetic studies of the catechol-o-methyltransferase from the brain of the African catfish, Clarias gariepinus Comp. Biochem. Physiol. 91C 1988 399 402
R.J.M. Timmers, and J.G.D. Lambert Catechol-o-methyltransferase in the brain of the male African catfish, Clarias gariepinus; distribution and significance for the metabolism of catecholestrogens and dopamine Fish Physiol. Biochem. 7 1989 201 210
N. Tinbergen The study of Instinct 1951 Clarendon Press Oxford
S. Veiga, L.M. Garcia-Segura, and I. Azcoitia Neuroprotection by the steroids pregnenolone and dehydroepiandrosterone is mediated by the enzyme aromatase J. Neurobiol. 56 2003 398 406
C. Viglietti-Panzica, G.C. Panzica, M.G. Fiori, M. Calcagni, G.C. Anselmetti, and J. Balthazart A sexually dimorphic nucleus in the quail preoptic area Neurosci. Lett. 64 1986 129 134
C.K. Wagner, and J.I. Morrell Distribution and steroid hormone regulation of aromatase mRNA expression in the forebrain of adult male and female rats: a cellular-level analysis using in situ hybridization J. Comp. Neurol. 370 1996 71 84
M.J. Walters, and C.F. Harding The effects of an aromatization inhibitor on the reproductive behavior of male zebra finches Horm. Behav. 22 1988 207 218
J.T. Watson, and E. Adkins-Regan 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 1989 251 268
J.T. Watson, and E. Adkins-Regan Neuroanatomical localization of sex steroid-concentrating cells in the Japanese quail (Coturnix japonica): autoradiography with [3H]-testosterone, [3H]-estradiol, and [3H]-dihydrotestosterone Neuroendocrinology 49 1989 51 64
J.T. Watson, and E. Adkins-Regan Testosterone implanted in the preoptic area of male Japanese quail must be aromatized to activate copulation Horm. Behav. 23 1989 432 447
R.E. Whalen, and J.F. DeBold Comparative effectiveness of T, androstenedione and DHT in maintaining mating behavior in castrated male hamster Endocrinology 95 1974 1674 1679
R.E. Whalen, and W.G. Luttge Testosterone, androstenedione, and dihydrotestosterone: effects on mating behavior of male rats Horm. Behav. 2 1971 117 125
W. Wouters, E. Snoeck, and R. De Coster Vorozole, a specific non-steroidal aromatase inhibitor Breast Cancer Res. Treat. 30 1994 89 94
P. Yahr Data and hypotheses in tales of dihydrotestosterone Horm. Behav. 13 1979 92 96