appetitive sexual behavior; consummatory sexual behavior; Fos expression; Japanese quail; sexual differentiation
Abstract :
[en] Sexual behavior can be usefully parsed into an appetitive and a consummatory component. Both appetitive and consummatory male-typical sexual behaviors (respectively, ASB and CSB) are activated in male Japanese quail by testosterone (T) acting in the medial preoptic nucleus (POM), but never observed in females. This sex difference is based on a demasculinization (= organizational effect) by estradiol during embryonic life for CSB, but a differential activation by T in adulthood for ASB. Males expressing rhythmic cloacal sphincter movements (RCSMs; a form of ASB) or allowed to copulate display increased Fos expression in POM. We investigated Fos brain responses in females exposed to behavioral tests after various endocrine treat- ments. T-treated females displayed RCSM, but never copulated when exposed to another female. Accordingly they showed an increased Fos expression in POM after ASB but not CSB tests. Females treated with the aromatase inhibitor Vorozole in ovo and T in adulthood displayed both male-typical ASB and CSB, and Fos expression in POM was increased after both types of tests. Thus, the neural circuit mediating ASB is present or can develop in both sexes, but is inactive in females unless they are exposed to exogenous T. In contrast, the neural mechanism mediating CSB is not normally present in females, but can be pre- served by blocking the embryonic production of estrogens. Overall these data confirm the difference in endocrine controls and probably neural mechanisms supporting ASB and CSB in quail, and highlight the complexity of mechanisms underlying sexual differentiation of behavior.
Research center :
Giga-Neurosciences - ULiège
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
Corbisier de Méaultsart, Céline
Ball, Gregory
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Language :
English
Title :
Distinct Neuroendocrine mechanisms control neural activity underlying sex differences in sexual motivation and performance
Publication date :
2013
Journal title :
European Journal of Neuroscience
ISSN :
0953-816X
eISSN :
1460-9568
Publisher :
Blackwell Science, Paris, France
Volume :
37
Issue :
5
Pages :
735-42
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NIH - National Institutes of Health [US-MD] [US-MD] FRFC - Fonds de la Recherche Fondamentale Collective [BE] ULg FSR - Université de Liège. Fonds spéciaux pour la recherche [BE] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture [BE]
Funding number :
National Institutes of Health - NIH (MH50388); FRFC (2.4537.09)
Absil, P., Braquenier, J.B., Balthazart, J. & Ball, G.F. (2002) Effects of lesions of nucleus taeniae on appetitive and consummatory aspects of male sexual behavior in Japanese quail. Brain Behav. Evol., 60, 13-35.
Adkins, E.K. (1975) Hormonal basis of sexual differentiation in the Japanese quail. J. Comp. Physiol. Psychol., 89, 61-71.
Adkins, E.K. (1976) Embryonic exposure to an antiestrogen masculinizes behavior of female quail. Physiol. Behav., 17, 357-359.
Adkins, E.K. & Adler, N.T. (1972) Hormonal control of behavior in the Japanese quail. J. Comp. Physiol. Psychol., 81, 27-36.
Adkins-Regan, E. & Leung, C.H. (2006) Hormonal and social modulation of cloacal muscle activity in female Japanese quail. Physiol. Behav., 87, 82-87.
Ball, G.F. & Balthazart, J. (2008) How useful is the appetitive and consummatory distinction for our understanding of the neuroendocrine control of sexual behavior? Horm. Behav., 53, 307-311; author reply 315-308.
Ball, G.F. & Balthazart, J. (2010) Japanese quail as a model system for studying the neuroendocrine control of reproductive and social behaviors. ILAR J., 51, 310-325.
Ball, G.F. & Balthazart, J. (2011) Sexual arousal, is it for mammals only? Horm. Behav., 59, 645-655.
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., De Clerck, A. & Foidart, A. (1992) Behavioral demasculinization of female quail is induced by estrogens: studies with the new aromatase inhibitor, R76713. Horm. Behav., 26, 179-203.
Balthazart, J., Absil, P., Gérard, M., Appeltants, D. & Ball, G.F. (1998) Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J. Neurosci., 18, 6512-6527.
Balthazart, J., Arnold, A.P. & Adkins-Regan, E. (2009) Sexual differentiation of brain and behavior in birds. In Pfaff, D.W., Arnold, A.P., Etgen, A.M., Fahrbach, S.E. & Rubin, R.T. (Eds), Hormones, Brain and Behavior. Academic Press, San Diego, CA, pp. 1745-1787.
Baum, M.J. & Everitt, B.J. (1992) Increased expression of c-fos in the medial preoptic area after mating in male rats: role of afferent inputs from the medial amygdala and midbrain central tegmental field. Neuroscience, 50, 627-646.
Baylé, J.D., Ramade, F. & Oliver, J. (1974) Stereotaxic topography of the brain of the quail. J. Physiol. (Paris), 68, 219-241.
Becker, J.B., Berkley, K.J., Geary, N., Hampson, E., Herman, J.P. & Young, E.A. (2008) Sex Differences in the Brain. From Genes to behavior. Oxford University Press, Oxford.
Bialy, M. & Kaczmarek, L. (1996) c-fos expression as a tool to search for the neurobiological base of the sexual behaviour of males. Acta Neurobiol. Exp., 56, 567-577.
de Bournonville, C.C., Dickens, M.J., Ball, G.F., Balthazart, J. & Cornil, C.A. (2012) Region- and context-specific rapid changes in brain aromatase activity following social interactions. Abst. Soc. Behav. Neuroendo., 16, 149-150.
Cahill, L. (2006) Why sex matters for neuroscience. Nature reviews. Neuroscience, 7, 477-484.
Charlier, T.D., Ball, G.F. & Balthazart, J. (2008) Rapid action on neuroplasticity precedes behavioral activation by testosterone. Horm. Behav., 54, 488-495.
Cheng, K.M., Hickman, A.R. & Nichols, C.R. (1989a) Role of the proctodeal gland foam of male Japanese quail in natural copulations. Auk, 106, 279-285.
Cornil, C.A., Ball, G.F., Balthazart, J. & Charlier, T.D. (2011) Organizing effects of sex steroids on brain aromatase activity in quail. PLoS ONE, 6, e19196.
De Coster, R., Wouters, W., Bowden, C.R., Vanden Bossche, H., Bruynseels, J., Tuman, R.W., Van Ginckel, R., Snoeck, E., Van Peer, A. & Janssen, P.A.J. (1990) New non-steroidal aromatase inhibitors: focus on R76713. J. Steroid Biochem., 37, 335-341.
D'Hondt, E., Vermeiren, J., Peeters, K., Balthazart, J., Tlemçani, O., Ball, G.F., Duffy, D.L., Vandesande, F. & Berghman, L.R. (1999) Validation of a new antiserum directed towards the synthetic c-terminus of the FOS protein in avian species: immunological, physiological and behavioral evidence. J. Neurosci. Methods, 91, 31-45.
Dulac, C. & Kimchi, T. (2007) Neural mechanisms underlying sex-specific behaviors in vertebrates. Curr. Opin. Neurobiol., 17, 675-683.
Elbrecht, A. & Smith, R.G. (1992) Aromatase enzyme activity and sex determination in chickens. Science, 255, 467-470.
Feder, H.H. (1981) Perinatal hormones and their role in the development of sexually dimorphic behaviors. In Adler, N. (Ed.), Neuroendocrinology of Reproduction. Plenum Press, New York, pp. 127-157.
Fujiwara, K.T., Ashida, K., Nishima, H., Iba, H., Miyajima, N., Nishizawa, M. & Kawai, S. (1987) The chicken c-fos gene: cloning and nucleotide sequence analysis. J. Virol., 61, 4012-4018.
Hutchison, R.E. (1978) Hormonal differentiation of sexual behavior in Japanese quail. Horm. Behav., 11, 363-387.
Jordan-Young, R.M. (2010) Brain Storm. The Flaws in the Science of Sex Differences. Harvard University Press, Cambridge MA.
Kimchi, T., Xu, J. & Dulac, C. (2007) A functional circuit underlying male sexual behaviour in the female mouse brain. Nature, 448, 1009-1014.
Kuenzel, W.J. & Masson, M. (1988) A stereotaxic Atlas of the Brain of the Chick (Gallus domesticus). The Johns Hopkins University Press, Baltimore.
Martel, K.L. & Baum, M.J. (2009) Adult testosterone treatment but not surgical disruption of vomeronasal function augments male-typical sexual behavior in female mice. J. Neurosci., 29, 7658-7666.
Meddle, S.L., King, V.M., Follett, B.K., Wingfield, J.C., Ramenofsky, M., Foidart, A. & Balthazart, J. (1997) Copulation activates Fos-like immunoreactivity in the male quail forebrain. Behav. Brain Res., 85, 143-159.
Meddle, S.L., Foidart, A., Wingfield, J.C., Ramenofsky, M. & Balthazart, J. (1999) Effects of sexual interactions with a male on Fos-like immunoreactivity in the female quail brain. J. Neuroendocrinol., 11, 771-784.
Ngun, T.C., Ghahramani, N., Sanchez, F.J., Bocklandt, S. & Vilain, E. (2011) The genetics of sex differences in brain and behavior. Front. Neuroendocrinol., 32, 227-246.
Panzica, G.C., Viglietti-Panzica, C. & Balthazart, J. (1996) The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrinol., 17, 51-125.
Phoenix, C.H., Goy, R.W., Gerall, A.A. & Young, W.C. (1959) Organizational action of prenatally administered testosterone propionate on the tissues mediating behavior in the female guinea pig. Endocrinology, 65, 369-382.
Sachs, B.D. (1967) Photoperiodic control of the cloacal gland of the Japanese quail. Science, 157, 201-203.
Sachs, B.D. (2007) A contextual definition of male sexual arousal. Horm. Behav., 51, 569-578.
Seiwert, C.M. & Adkins-Regan, E. (1998) The foam production system of the male Japanese quail: characterization of structure and function. Brain Behav. Evol., 52, 61-80.
Taziaux, M., Cornil, C.A., Dejace, C., Arckens, L., Ball, G.F. & Balthazart, J. (2006) Neuroanatomical specificity in the expression of the immediate early gene c-fos following expression of appetitive and consummatory male sexual behaviour in Japanese quail. Eur. J. Neurosci., 23, 1869-1887.
Taziaux, M., Kahn, A., Moore, J. 3rd, Balthazart, J. & Holloway, K.S. (2008a) Enhanced neural activation in brain regions mediating sexual responses following exposure to a conditioned stimulus that predicts copulation. Neuroscience, 151, 644-658.
Taziaux, M., Keller, M., Ball, G.F. & Balthazart, J. (2008b) Site-specific effects of anosmia and cloacal gland anesthesia on Fos expression induced in male quail brain by sexual behavior. Behav. Brain Res., 194, 52-65.
Truitt, W.A. & Coolen, L.M. (2002) Identification of a potential ejaculation generator in the spinal cord. Science, 297, 1566-1569.
Wade, J. & Arnold, A.P. (1996) Functional testicular tissue does not masculinize development of the zebra finch song system. Proc. Natl. Acad. Sci. USA, 93, 5264-5268.
Wouters, W., De Coster, R., Krekels, M., Van Dun, J., Beerens, D., Haelterman, C., Raeymaekers, A., Freyne, E., Van Gelder, J., Venet, M. & Janssen, P.A.J. (1989) R 76713, a new specific non-steroidal aromatase inhibitor. J. Steroid Biochem., 32, 781-788.
