[en] Neural production of 17β-oestradiol via aromatisation of testosterone may play a critical role in rapid, non-genomic regulation of physiological and behavioural processes. In brain nuclei implicated in the control of sexual behaviour, sexual or stressfull stimuli induce respectively a rapid inhibition or increase in preoptic aromatase activity (AA). Here, we tested quail that were either non-stressed or acutely stressed (15 min restraint) immediately prior to sexual interaction (5 min) with stressed or non-stressed partners. We measured nuclei-specific AA changes, corresponding behavioural output, fertilisation rates and corticosterone (CORT) concentrations. In males, sexual interaction rapidly reversed stress-induced increases of AA in the medial preoptic nucleus (POM). This time scale (<5min) highlights the dynamic potential of the aromatase system to integrate input from stimuli that drive AA in opposing directions. Moreover, acute stress had minimal effects on male behaviour suggesting that the input from the sexual stimuli on POM AA may actively preserve sexual behaviour despite stress exposure. We also found distinct sex differences in contextual physiological responses: while males did not show any effect of partner status, females responded to both their stress exposure and the male partner's stress exposure at the level of circulating CORT and AA. In addition, fertilisation rates and female CORT correlated with the male partner's exhibition of sexually aggressive behaviour suggesting that female perception of the male can affect their physiology as much as direct stress. Overall, male reproduction appears relatively simple - sexual stimuli, irrespective of stress, drives major neural changes including rapid reversal of stress-induced changes of AA. In contrast, female reproduction appears more nuanced and context specific, with subjects responding physiologically and behaviourally to stress, the male partner's stress exposure, and female-directed male behaviour.
Research center :
Giga-Neurosciences - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
Dickens, Molly J.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Language :
English
Title :
Brain aromatase and circulating corticosterone are rapidly regulated by combined acute stress and sexual interaction in a sex specific manner.
Publication date :
2012
Journal title :
Journal of Neuroendocrinology
ISSN :
0953-8194
eISSN :
1365-2826
Publisher :
Blackwell Publishing, Oxford, United Kingdom
Volume :
24
Issue :
10
Pages :
1322-34
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NIH - National Institutes of Health [US-MD] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] NSF - National Science Foundation [US-VA] FRFC - Fonds de la Recherche Fondamentale Collective [BE] ULiège - Université de Liège [BE]
Balthazart J, Cornil CA, Charlier TD, Taziaux M, Ball GF. Estradiol, a key endocrine signal in the sexual differentiation and activation of reproductive behavior in Quail. J Exp Zool A Ecol Genet Physiol 2009; 311: 323-345.
Trainor BC, Marler CA. Testosterone promotes paternal behaviour in a monogamous mammal via conversion to oestrogen. Proc Biol Sci 2002; 269: 823-829.
Trainor BC, Kyomen HH, Marler CA. Estrogenic encounters: how interactions between aromatase and the environment modulate aggression. Front Neuroendocrinol 2006; 27: 170-179.
Evrard HC, Balthazart J. Aromatization of androgens into estrogens reduces response latency to a noxious thermal stimulus in male quail. Horm Behav 2004; 45: 181-189.
Garcia-Segura LM. Aromatase in the brain: not just for reproduction anymore. J Neuroendocrinol 2008; 20: 705-712.
McEwen BS, Alves SE. Estrogen actions in the central nervous system. Endocr Rev 1999; 20: 279-307.
Woolley CS. Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 2007; 47: 657-680.
Balthazart J, Ball GF. Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 2006; 29: 241-249.
Cornil CA, Dalla C, Papadopoulou-Daifoti Z, Baillien M, Dejace C, Ball GF, Balthazart J. Rapid decreases in preoptic aromatase activity and brain monoamine concentrations after engaging in male sexual behavior. Endocrinology 2005; 146: 3809-3820.
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.
Remage-Healey L, Maidment NT, Schlinger BA. Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 2008; 11: 1327-1334.
de Bournonville C, Ball GF, Balthazart J, Cornil CA. Rapid changes of aromatase activity in discrete brain regions following social interactions. Steroids and Nervous System, Torino, Italy, 2011.
Wingfield JC, Sapolsky RM. Reproduction and resistance to stress: when and how. J Neuroendocrinol 2003; 15: 711-724.
Bian J, Wu Y, Liu J. Breeding behavior under temporal risk of predation in male root voles (Microtus oeconomus). J Mammal 2005; 86: 953-960.
Cecconello AL, Raineki C, Sebben V, Lucion AB, Sanvitto GL. Effect of acute stress on sexual behavior in female rats: participation of the central angiotensinergic system. Behav Brain Res 2010; 207: 429-433.
Moore FL, Miller LJ. Stress-induced inhibition of sexual behavior: corticosterone inhibits courtship behaviors of a male amphibian. Horm Behav 1984; 18: 400-410.
Lynn SE, Stamplis TB, Barrington WT, Weida N, Hudak CA. Food, stress, and reproduction: short-term fasting alters endocrine physiology and reproductive behavior in the zebra finch. Horm Behav 2010; 58: 214-222.
Retana-Marquez S, Salazar ED, Velazquez-Moctezuma J. Effect of acute and chronic stress on masculine sexual behavior in the rat. Psychoneuroendocrinology 1996; 21: 39-50.
Balthazart J, Ball GF. The Japanese quail as a model system for the investigation of steroid-catecholamine interactions mediating appetitive and consummatory aspects of male sexual behavior. Annu Rev Sex Res 1998; 9: 96-176.
Adkins EK, Adler NT. Hormonal control of behavior in the Japanese quail. J Comp Physiol Psychol 1972; 81: 27-36.
Hutchison RE. Hormonal differentiation of sexual-behavior in Japanese quail. Horm Behav 1978; 11: 363-387.
Delville Y, Balthazart J. Hormonal control of female sexual behavior in the Japanese quail. Horm Behav 1987; 21: 288-309.
Takada S, Otaa J, Kansakuc N, Yamashitad H, Izumie T, Ishikawaa M, Wadaa T, Kanedaa R, YL C, K K, Fujiwaraa S, Aokia H, Kisanukia H, Yamashitaa Y, Mano H. Nucleotide sequence and embryonic expression of quail and duck Sox9 genes. Gen Comp Endocrinol 2006; 145: 208-213.
Clinton M, Haines L, Belloir B, McBride D. Sexing chick embryos: a rapid and simple protocol. Br Poult Sci 2001; 42: 134-138.
Cornil CA, Ball GF, Balthazart J, Charlier TD. Organizing effects of sex steroids on brain aromatase activity in quail. PLoS ONE 2011; 6: e19196.
Palkovits M. Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 1973; 59: 449-450.
Schumacher M, Balthazart J. Neuroanatomical distribution of testosterone-metabolizing enzymes in the Japanese quail. Brain Res 1987; 422: 137-148.
Foidart A, Reid J, Absil P, Yoshimura N, Harada N, Balthazart J. 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.
Bayle JD, Ramade F, Oliver J. Stereotaxic topography of the brain of the quail (Coturnix coturnix japonica). J Physiol 1974; 68: 219-241.
Roselli CE, Resko JA. In vitro assay of aromatase activity in the central nervous system. In: Greenstein B, ed. Neuroendocrine Research Methods. Chur: Harwood Academic Publishers, 1991: 937-951.
Baillien M, Balthazart J. A direct dopaminergic control of aromatase activity in the quail preoptic area. J Steroid Biochem Mol Biol 1997; 63: 99-113.
Persaud KN, Galef BG. Female Japanese quail (Coturnix japonica) mated with males that harassed them are unlikely to lay fertilized eggs. J Comp Psychol 2005; 119: 440-446.
Correa SM, Horan CM, Johnson PA, Adkins-Regan E. Copulatory behaviors and body condition predict post-mating female hormone concentrations, fertilization success, and primary sex ratios in Japanese quail. Horm Behav 2011; 59: 556-564.
Watson JT, Adkins-Regan E. 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 1989; 23: 251-68.
Watson JT, Adkins-Regan E. Testosterone implanted in the preoptic area of male Japanese quail must be aromatized to activate copulation. Horm Behav 1989; 23: 432-47.
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, Harada N, Balthazart J, Cornil CA. Human and quail aromatase activity is rapidly and reversibly inhibited by phosphorylating conditions. Endocrinology 2011; 152: 4199-4210.
Woodley SK, Lacy EL. An acute stressor alters steroid hormone levels and activity but not sexual behavior in male and female Ocoee salamanders (Desmognathus ocoee). Horm Behav 2010; 58: 427-432.
Wu Y, Bian J. Effect of acute administration of corticosterone on male sexual behavior in root voles. Acta Theriologica Sinica 2006; 26: 354-358.
Retana-Marquez S, Bonilla-Jaime H, Velazquez-Moctezuma J. Lack of effect of corticosterone administration on male sexual behavior of rats. Physiol Behav 1998; 63: 367-370.
Pfaff DW, Schwartz-Giblin S, McCarthy MM, Kow LM. Cellular and molecular mechanisms of female reproductive behaviors. In: Knobil E, Neill JD, eds. The Physiology of Reproduction, 2nd edn. New York, NY: Raven Press, 1994: 107-220.
Blaustein JD. Feminine reproductive behavior and physiology in rodents: integration of hormonal, behavioral, and environmental influences. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, eds. Hormones, Brain and Behavior. San Diego, CA: Academic Press, 2009: 68-1007.
Gibson MJ, Cheng MF. Neural mediation of estrogen-dependent courtship behavior in female ring doves. J Comp Physiol Psychol 1979; 93: 855-867.
Meddle SL, Foidart A, Wingfield JC, Ramenofsky M, Balthazart J. Effects of sexual interactions with a male on Fos-like immunoreactivity in the female quail brain. J Neuroendocrinol 1999; 11: 771-784.
Adkins-Regan E. Predictors of fertilization in the Japanese quail, Coturnix japonica. Anim Behav 1995; 50: 1405-1415.
Rutkowska J, Adkins-Regan E. Learning enhances female control over reproductive investment in the Japanese quail. Proc Biol Sci 2009; 276: 3327-3334.
Delville Y, Sulon J, Hendrick JC, Balthazart J. Effect of the presence of females on the pituitary-testicular activity in male Japanese quail (Coturnix coturnix japonica). Gen Comp Endocrinol 1984; 55: 295-305.
Waldherr M, Nyuyki K, Maloumby R, Bosch OJ, Neumann ID. Attenuation of the neuronal stress responsiveness and corticotrophin releasing hormone synthesis after sexual activity in male rats. Horm Behav 2010; 57: 222-229.
Ophir AG, Persaud KN, Galef BG. Avoidance of relatively aggressive male Japanese quail (Coturnix japonica) by sexually experienced conspecific females. J Comp Psychol 2005; 119: 3-7.
Ophir AG, Galef BG. Female Japanese quail that 'eavesdrop' on fighting males prefer losers to winners. Anim Behav 2003; 66: 399-407.
Romero LM, Reed JM. Collecting baseline corticosterone samples in the field: is under three minutes good enough? Comp Biochem Physiol A Mol Integr Physiol 2005; 140: 73-79.
Dickens MJ, Cornil CA, Balthazart J. Acute stress alters brain aromatase activity in Japanese quail (Coturnix japonica) in a sex-specific manner. Salt Lake City, UT: Society for Integrative and Comparative Biology, 2011.
