Rapid changes in brain aromatase activity in the female quail brain following expression of sexual behaviour

[en] In male quail, oestrogens produced in the brain (neuro-oestrogens) exert a dual action on male sexual behaviour: they increase sexual motivation within minutes via mechanisms activated at the membrane but facilitate sexual performance by slower, presumably nuclear-initiated, mechanisms. Recent work indicates that neuro-oestrogens are also implicated in the control of female sexual motivation despite the presence of high circulating concentrations of oestrogens of ovarian origin. Interestingly, aromatase activity (AA) in the male brain is regulated in time domains corresponding to the slow “genomic” and faster “nongenomic” modes of action of oestrogens. Furthermore, rapid changes in brain AA are observed in males after sexual interactions with a female. In the present study, we investigated whether similar rapid changes in brain AA are observed in females allowed to interact sexually with males. A significant decrease in AA was observed in the medial preoptic nucleus after interactions that lasted 2, 5 or 10 minutes, although this decrease was no longer significant after 15 minutes of interaction. In the bed nucleus of the stria terminalis, a progressive decline of average AA was observed between 2 and 15 minutes, although it never reached statistical significance. AA in this nucleus was, however, negatively correlated with the sexual receptivity of the female. These data indicate that sexual interactions affect brain AA in females as in males in an anatomically specific manner and suggest that rapid changes in brain oestrogens production could also modulate female sexual behaviour. © 2017 British Society for Neuroendocrinology

Disciplines :

Neurosciences & behavior

Author, co-author :

de Bournonville, Catherine ; GIGA Neurosciences, Research Group in Behavioral Neuroendocrinology, University of Liège, Liège, Belgium, Department of Psychological and Brain Sciences, University of Massachusetts, Amherst, MA, United States

Ball, G. F.; Department of Psychology, University of Maryland, College ParkMD, United States

Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques

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

Language :

English

Title :

Rapid changes in brain aromatase activity in the female quail brain following expression of sexual behaviour

Publication date :

2017

Journal title :

Journal of Neuroendocrinology

ISSN :

0953-8194

eISSN :

1365-2826

Publisher :

Blackwell Publishing Ltd

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

NIMH - National Institute of Mental Health [US-MD]
ULiège - Université de Liège [BE]

Available on ORBi :

since 02 February 2018

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Bibliography

McEwen BS, Alves SE. Estrogen actions in the central nervous system. Endocr Rev. 1999;20:279-307.
Azcoitia I, Yague JG, Garcia-Segura LM. Estradiol synthesis within the human brain. Neuroscience. 2011;191:139-147.
Panzica GC, 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;17:51-125.
Ball GF, Balthazart J. Neuroendocrine Regulation of Reproductive Behavior in Birds. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, eds. Hormones, Brain and Behavior. San Diego, CA: Elsevier; 2009:855-897.
Tsai M, O'Malley BW. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem. 1994;63:451-486.
Cornil CA, de Bournonville C. Dual action of neuro-estrogens in the regulation of male sexual behavior. Gen Comp Endocrinol. 2017. https://doi.org/10.1016/j.ygcen.2017.05.002.
Balthazart J, Baillien M, Cornil CA, Ball GF. Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol Behav. 2004;83:247-270.
Balthazart J, Foidart A, Hendrick JC. The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior. Physiol Behav. 1990;47:83-94.
Charlier TD, Cornil CA, Patte-Mensah C, et al. Local modulation of steroid action: rapid control of enzymatic activity. Front Neurosci. 2015;9:1-9.
de Bournonville C, et al. Glutamate released in the preoptic area during sexual behavior controls local estrogen synthesis in male quail. Psychoneuroendocrinology. 2017;79:49-58.
Comito D, Pradhan DS, Karleen BJ, Schlinger BA. Region-specific rapid regulation of aromatase activity in zebra finch brain. J Neurochem. 2016;136:1177-1185.
Cornil CA, Leung CH, Pletcher ER, et al. Acute and specific modulation of presynaptic aromatization in the vertebrate brain. Endocrinology. 2012;153:2562-2567.
Dickens MJ, de Bournonville C, Balthazart J, Cornil CA. Relationships between rapid changes in local aromatase activity and estradiol concentrations in male and female quail brain. Horm Behav. 2014;65:154-164.
Dickens MJ, Cornil CA, Balthazart J. Acute stress differentially affects aromatase activity in specific brain nuclei of adult male and female quail. Endocrinology. 2011;152:4242-4251.
de Bournonville C, Dickens MJ, Ball GF, Balthazart J, Cornil CA. Dynamic changes in brain aromatase activity following sexual interactions in males: where, when and why? Psychoneuroendocrinology. 2013;38:789-799.
Cornil CA, Dalla C, Papadopoulou-Daifoti Z, et al. Rapid decreases in preoptic aromatase activity and brain monoamine concentrations after engaging in male sexual behavior. Endocrinology. 2005;146:3809-3820.
Noble R. Hormonal control of receptivity in female quail (Coturnix coturnix japonica). Horm Behav. 1973;4:61-72.
Adkins EK, Adler NT. Hormonal control of behavior in the Japanese quail. J Comp Physiol Psychol. 1972;81:27-36.
Delville Y, Balthazart J. Hormonal control of female sexual behavior in the Japanese quail. Horm Behav. 1987;21:288-309.
Adkins EK, Nock BL. The effects of the antiestrogen CI-628 on sexual behavior activated by androgen or estrogen in quail. Horm Behav. 1976;7:417-429.
Noble R. The effects of estrogen and progesterone on copulation in female quail (Coturnix coturnix japonica) housed in continuous dark. Horm Behav. 1972;3:199-204.
Pfaus JG, Jones SL, Flanagan-Cato LM, Blaustein JD. Female sexual behavior. In: Plant T.M., Zeleznik A.J. eds Knobil and Neill's Physiology of reproduction. Elsevier, Oxford: Academic press; 2015.
Vasudevan N, Pfaff DW. Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front Neuroendocrinol. 2008;29:238-257.
Christensen A, Dewing P, Micevych P. Membrane-initiated estradiol signaling induces spinogenesis required for female sexual receptivity. J Neurosci. 2011;31:17583-17589.
Goodson JL. The vertebrate social behavior network: evolutionary themes and variations. Horm Behav. 2005;48:11-22.
de Bournonville C, Balthazart J, Ball GF, Cornil CA. Non-ovarian aromatization is required to activate female sexual motivation in testosterone-treated ovariectomized quail. Horm Behav. 2016;83:45-59.
Balthazart J, Schumacher M, Evrard L. Sex differences and steroid control of testosterone-metabolizing enzyme activity in the quail brain. J Neuroendocrinol. 1990;2:675-683.
Voigt C, Ball GF, Balthazart J. Effects of sex steroids on aromatase mRNA expression in the male and female quail brain. Gen Comp Endocrinol. 2011;170:180-188.
Konkle ATM, Balthazart J. Sex differences in the rapid control of aromatase activity in the quail preoptic area. J Neuroendocrinol. 2011;23:424-434.
Dickens MJ, Balthazart J, Cornil CA. Brain aromatase and circulating corticosterone are rapidly regulated by combined acute stress and sexual interaction in a sex-specific manner. J Neuroendocrinol. 2012;24:1322-1334.
Remage-Healey L, Dong SM, Chao A, Schlinger BA. Sex-specific, rapid neuroestrogen fluctuations and neurophysiological actions in the songbird auditory forebrain. J Neurophysiol. 2012;107:1621-1631.
Delville Y, Sulon J, Balthazart J. Diurnal variations of sexual receptivity in the female Japanese quail. Horm Behav. 1986;20:13-33.
Beach A. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm Behav. 1976;7:105-138.
Palkovits M. Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res. 1973;59:449-450.
Cornil CA, Ball GF, Balthazart J, Charlier TD. Organizing effects of sex steroids on brain aromatase activity in quail. PLoS ONE. 2011;6:e19196.
Foidart A, Reid J, Absil P, et al. 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. 1995;8:267-282.
Roselli CE, Resko JA. In vitro assay of aromatase activity in the central nervous system. In: Greenstein B, ed. Neuroendocrin Research Methods. Chur: Hardwood Academic Publishers; 1991:937-954.
Balthazart J, Taziaux M, Holloway K, Ball GF, Cornil CA. Behavioral effects of brain-derived estrogens in birds. Ann NY Acad Sci. 2009;1163:31-48.
Hull EM, Rodríguez-Manzo G. Male sexual behavior. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, eds. Hormones, Brain and Behavior. San Diego, CA: Elsevier; 2009:6-65.
Gibson MJ, Cheng MF. Neural mediation of estrogen-dependent courtship behavior in female ring doves. J Comp Physiol Psychol. 1979;93:855-867.
Kenealy BP, et al. Neuroestradiol in the hypothalamus contributes to the regulation of gonadotropin releasing hormone release. J Neurosci. 2013;33:19051-19059.
Pfaus JG, Kippon TE, Coria-Avila GA, et al. Who, what, where, when (and maybe even why)? How the experience of sexual reward connects sexual desire, preference, and performance. Arch Sex Behav. 2012;41:31-62.
Sato SM, Woolley CS. Acute inhibition of neurosteroid estrogen synthesis suppresses status epilepticus in an animal model. Elife. 2016;5:e12917.
Cornil CA, Ball GF, Balthazart J. Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res. 2006;1126:2-26.
Cornil CA, Ball GF, Balthazart J. Rapid control of male typical behaviors by brain-derived estrogens. Front Neuroendocrinol. 2012;33:425-446.
Roepke TA, Ronnekleiv OK, Kelly MJ. Physiological consequences of membrane-initiated estrogen signaling in the brain. Front Biosci (Landmark Ed). 2011;16:1560-1573.
Cornil CA, Charlier TD. Rapid behavioural effects of oestrogens and fast regulation of their local synthesis by brain aromatase. J Neuroendocrinol. 2010;22:664-673.
Taziaux M, Cornil CA, Dejace C, et al. 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. 2006;23:1869-1887.
Xie J, Kuenzel WJ, Sharp PJ, Jurkevich A. Appetitive and consummatory sexual and agonistic behaviour elicits FOS expression in aromatase and vasotocin neurones within the preoptic area and bed nucleus of the stria terminalis of male domestic chickens. J Neuroendocrinol. 2011;23:232-243.