Appetitive sexual behavior; Consummatory sexual behavior; Sexual experience; Sexual satiety; Coolidge effect; Brain estrogen synthesis
Abstract :
[en] This study was designed to determine whether changes in sexual motivation acutely regulate brain estrogen synthesis by aromatase. Five experiments (Exp.1–5) were first conducted to determine the effect of recent mating and of the presentation of a new female (Coolidge effect) on sexual motivation. Exp.1–2 showed that 10 min or overnight access to copulation decreases measures of male sexual motivation when male subjects were visually exposed to the female they had copulated with and this effect is not counteracted by the view of a new female. Exp.3 showed that sexual motivation is revived by the view of a new female in previously unmated males only allowed to see another female for 10 min. After mating for 10 min (Exp.4) or overnight (Exp.5) with a female, males showed a decrease in copulatory behavior that was not reversed by access to a new female. Exp.6 and 7 confirmed that overnight copulation (Exp.6) and view of a novel female (Exp.7) respectively decreases and increases sexual behavior and motivation. Yet, these manipulations did not affect brain aromatase activity except in the tuberal hypothalamus. Together these data confirm that copulation or prolonged view of a female de- crease sexual motivation but a reactivation of sexual motivation by a new female can only be obtained if males had only seen another female but not copulated with her, which is different in some degree from the Coolidge effect described in rodents. Moreover changes in brain aromatase do not simply reflect changes in motivation and more complex mechanisms must be considered.
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 :
Effects of a novel partner and sexual satiety on the expression of male sexual behavior and brain aromatase activity in quail.
Publication date :
2019
Journal title :
Behavioural Brain Research
ISSN :
0166-4328
eISSN :
1872-7549
Publisher :
Elsevier, Netherlands
Volume :
359
Pages :
502-515
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]
Pfaff, D.W., Drive: Neurobiological and Molecular Mechanisms of Sexual Motivation. 1999, The MIT Press.
Hull, E.M., Rodriguez-Manzo, G., Male sexual behavior. Pfaff, D.W., Joëls, M., (eds.) Hormones, Brain and Behavior, 2017, 1–58.
Beach, F.A., Jordan, L., Sexual exhaustion and recovery in the male rat. Q. J. Exp, Psychol 8:3 (1956), 121–133.
Rodriguez-Manzo, G., Fernandez-Guasti, A., Reversal of sexual exhaustion by serotonergic and noradrenergic agents. Behav. Brain Res. 62:2 (1994), 127–134.
Rodriguez-Manzo, G., Guadarrama-Bazante, I.L., Morales-Calderon, A., Recovery from sexual exhaustion-induced copulatory inhibition and drug hypersensitivity follow a same time course: two expressions of a same process?. Behav. Brain Res. 217:2 (2011), 253–260.
Fisher, A.E., Effects of stimulus variation on sexual satiation in the male rat. J. Comp. Physiol. Psychol. 55 (1962), 614–620.
Wilson, J.R., Kuehn, R.E., Beach, F.A., Modification in the sexual behavior of male rats produced by changing the stimulus female. J. Comp. Physiol. Psychol. 56 (1963), 636–644.
Fowler, H., Whalen, R.E., Variation in incentive stimulus and sexual behavior in the male rat. J. Comp. Physiol. Psychol. 54 (1961), 68–71.
Dewsbury, D.A., Effects of novelty on copulatory behavior: the coolidge effect and related phenomena. Psychol. Bull. 89:3 (1981), 464–482.
Ventura-Aquino, E., Fernandez-Guasti, A., Paredes, R.G., Hormones and the Coolidge Effect, Molecular and Cellular Endocrinology. 2017.
Pizzari, T., Cornwallis, C.K., Lovlie, H., Jakobsson, S., Birkhead, T.R., Sophisticated sperm allocation in male fowl. Nature 426:6962 (2003), 70–74.
Tlachi-Lopez, J.L., Eguibar, J.R., Fernandez-Guasti, A., Lucio, R.A., Copulation and ejaculation in male rats under sexual satiety and the Coolidge effect. Physiol. Behav. 106:5 (2012), 626–630.
Lucio, R.A., Rodriguez-Piedracruz, V., Tlachi-Lopez, J.L., Garcia-Lorenzana, M., Fernandez-Guasti, A., Copulation without seminal expulsion: the consequence of sexual satiation and the Coolidge effect. Andrology 2:3 (2014), 450–457.
Pfaus, J.G., Homologies of animal and human sexual behaviors. Horm. Behav. 30:3 (1996), 187–200.
Ball, G.F., Balthazart, J., How useful is the appetitive and consummatory distinction for our understanding of the neuroendocrine control of sexual behavior?. Horm. Behav. 53 (2008), 307–311.
Cornil, C.A., Ball, G.F., Balthazart, J., Differential control of appetitive and consummatory sexual behavior by neuroestrogens in male quail. Horm. Behav., 2018.
Fiorino, D.F., Coury, A., Phillips, A.G., Dynamic changes in nucleus accumbens dopamine efflux during the Coolidge effect in male rats. J. Neurosci. 17:12 (1997), 4849–4855.
Ball, G.F., Balthazart, J., Japanese quail as a model system for studying the neuroendocrine control of reproductive and social behaviors. ILAR J. Natl. Res. Council Inst. Lab. Anim. Resour. 51:4 (2010), 310–325.
Cornil, C.A., de Bournonville, C., Dual action of neuro-estrogens in the regulation of male sexual behavior. Gen. Comp. Endocrinol. 256 (2018), 57–62.
Cornil, C.A., Dalla, C., Papadopoulou-Daifoti, Z., Baillien, M., Balthazart, J., Estradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain. Behav. Brain Res. 66:1 (2006), 110–123.
Cornil, C.A., Taziaux, M., Baillien, M., Ball, G.F., Balthazart, J., Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail. Horm. Behav. 49:1 (2006), 45–67.
Seredynski, A.L., Balthazart, J., Christophe, V.J., Ball, G.F., Cornil, C.A., Neuroestrogens rapidly regulate sexual motivation but not performance. J. Neurosci. 33:1 (2013), 164–174.
Seredynski, A.L., Balthazart, J., Ball, G.F., Cornil, C.A., Estrogen receptor beta activation rapidly modulates male sexual motivation through the transactivation of metabotropic glutamate receptor 1a. J. Neurosci. 35:38 (2015), 13110–13123.
Charlier, T.D., Ball, G.F., Balthazart, J., Inhibition of steroid receptor coactivator-1 blocks estrogen and androgen action on male sex behavior and associated brain plasticity. J. Neurosci. 25:4 (2005), 906–913.
Niessen, N.A., Balthazart, J., Ball, G.F., Charlier, T.D., Steroid receptor coactivator 2 modulates steroid-dependent male sexual behavior and neuroplasticity in Japanese quail (Coturnix japonica). J. Neurochem. 119:3 (2011), 579–593.
Seredynski, A.L., Ball, G.F., Balthazart, J., Charlier, T.D., Specific activation of estrogen receptor alpha and beta enhances male sexual behavior and neuroplasticity in male Japanese quail. PLoS One, 6(4), 2011 e18627.
Balthazart, J., Foidart, A., Hendrick, C., The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior. Physiol. Behav. 47 (1990), 83–94.
Balthazart, J., Schumacher, M., Evrard, L., Sex differences and steroid control of testosterone-metabolizing enzyme activity in the quail brain. J. Neuroendocrinol. 2:5 (1990), 675–683.
Balthazart, J., Tlemcani, O., Harada, N., Localization of testosterone-sensitive and sexually dimorphic aromatase-immunoreactive cells in the quail preoptic area. J. Chem. Neuroanat. 11:3 (1996), 147–171.
Balthazart, J., Baillien, M., Ball, G.F., Rapid and reversible inhibition of brain aromatase activity. J. Neuroendocrinol. 13 (2001), 63–73.
Balthazart, J., Baillien, M., Charlier, T.D., Ball, G.F., Calcium-dependent phosphorylation processes control brain aromatase in quail. Eur. J. Neurosci. 17:8 (2003), 1591–1606.
Balthazart, J., Baillien, M., Ball, G.F., Rapid control of brain aromatase activity by glutamatergic inputs. Endocrinology 147:1 (2006), 359–366.
Charlier, T.D., Harada, N., Balthazart, J., Cornil, C.A., Human and quail aromatase activity is rapidly and reversibly inhibited by phosphorylating conditions. Endocrinology 152:11 (2011), 4199–4210.
de Bournonville, C., Smolders, I., Van Eeckhaut, A., Ball, G.F., Balthazart, J., Cornil, C.A., Glutamate released in the preoptic area during sexual behavior controls local estrogen synthesis in male quail. Psychoneuroendocrinology 79 (2017), 49–58.
Cornil, C.A., Dalla, C., Papadopoulou-Daifoti, Z., Baillien, M., Dejace, C., Balthazart, J., Sexual behavior affects preoptic aromatase activity and brain monoamines’ levels. Endocrinology 146:9 (2005), 3809–3820.
de Bournonville, C., Dickens, M.J., Ball, G.F., Balthazart, J., Cornil, C.A., Dynamic changes in brain aromatase activity following sexual interactions in males: where, when and why?. Psychoneuroendocrinology 38:6 (2013), 789–799.
Dickens, M.J., de Bournonville, C., Balthazart, J., Cornil, C.A., Relationships between rapid changes in local aromatase activity and estradiol concentrations in male and female quail brain. Horm. Behav. 65:2 (2014), 154–164.
Seiwert, C.M., Adkins-Regan, E., The foam production system of the male japanese quail: characterization of structure and function. Brain Behav.Evol. 52 (1998), 61–80.
Thompson, R.R., Goodson, J.L., Ruscio, M.G., Adkins-Regan, E., Role of the archistriatum 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.
Cornil, C.A., Holloway, K.S., Taziaux, M., Balthazart, J., The effects of aromatase inhibition on testosterone-dependent conditioned rhythmic cloacal sphincter movement in male Japanese quail. Physiol. Behav. 83:1 (2004), 99–105.
Holloway, K.S., Balthazart, J., Cornil, C.A., Androgen mediation of conditioned rhythmic cloacal sphincter movements in Japanese quail (Coturnix japonica). J. Comp. Psychol. 119:1 (2005), 49–57.
Cornil, C.A., Ball, G.F., Effects of social experience on subsequent sexual performance in naive male Japanese quail (Coturnix japonica). Horm. Behav. 57:4-5 (2010), 515–522.
Balthazart, J., Absil, P., Gérard, M., Appeltants, D., Ball, G.F., Appetitive and consummatory male sexual behavior in japanese quail are differentialy regulated by subregions of the preoptic medial nucleus. J. Neurosci. 18:16 (1998), 6512–6527.
Taziaux, M., Cornil, C.A., Balthazart, J., Aromatase inhibition blocks the expression of sexually-motivated cloacal gland movements in male quail. Behav. Process. 67:3 (2004), 461–469.
Adkins, E.K., Adler, N.T., Hormonal control of behavior in the japanese quail. J. Comp. Physiol. Psychol. 81:1 (1972), 27–36.
Hutchison, R.E., Hormonal differentiation of sexual behavior in Japanese quail. Horm. Behav. 11 (1978), 363–387.
Palkovits, M., Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res. 59 (1973), 449–450.
Cornil, C.A., Ball, G.F., Balthazart, J., Charlier, T.D., Organizing effects of sex steroids on brain aromatase activity in quail. PLoS One, 6(4), 2011 e19196.
Kuenzel, W.J., Masson, M., A Stereotaxic Atlas of the Brain of the Chick (Gallus Domesticus). 1988, The Johns Hopkins University Press, Baltimore and London.
Roselli, C.E., Resko, J.A., In vitro assay of aromatase activity in the central nervous system. Greenstein, B., (eds.) Neuroendocrine Research Methods, Vol 2, 1991, Harwood Academic Publishers, Chur, Switzerland pp. 937-951-0.
Baillien, M., Balthazart, J., A direct dopaminergic control of aromatase activity in the quail preoptic area. J. Steroid Biochem. Mol. Biol. 63:1-3 (1997), 99–113.
Schumacher, M., Balthazart, J., The postnatal demasculinization of sexual behavior in the Japanese quail (Coturnix coturnix japonica). Horm. Behav. 18:3 (1984), 298–312.
Balthazart, J., Hirschberg, D., Testosterone metabolism and sexual behavior in the chick. Horm. Behav. 12 (1979), 253–263.
Balthazart, J., Malacarne, G., Deviche, P., Stimulatory effects of 5β-dihydrotestosterone on the sexual behavior in the domestic chick. Horm. Behav. 15:3 (1981), 246–258.
Romano-Torres, M., Phillips-Farfan, B.V., Chavira, R., Rodriguez-Manzo, G., Fernandez-Guasti, A., Relationship between sexual satiety and brain androgen receptors. Neuroendocrinology 85:1 (2007), 16–26.
Brennan, P.L., Adkins-Regan, E., Endocrine regulation and sexual differentiation of avian copulatory sexually selected characters. Neurosci. Biobehav. Rev. 46 Pt:4 (2014), 557–566.
Ottinger, M.A., Schleidt, W.M., Russek, E., Daily patterns of courtship and mating behavior in the male Japanese quail. Behav. Process. 7:3 (1982), 223–233.
Schein, M.W., Carter, C.S., Sexual behaviour and novel stimuli in male Japanese quail (Coturnix coturnix japonica). Anim. Behav. 20 (1972), 383–385.
Domjan, M., Kurth, S., Effects of novelty on the reproductive behavior of male Japanese quail (Coturnix coturnix japonica). J. Comp. Psychol. 100 (1986), 203–207.
Lovlie, H., Cornwallis, C.K., Pizzari, T., Male mounting alone reduces female promiscuity in the fowl. Curr. Biol. 15 (2005), 1222–1227.
Bateson, P., Optimal outbreeding and the development of sexual preferences in Japanese quail. Z. Tierpsychol. 53 (1980), 231–244.
Riters, L.V., Balthazart, J., Behavioral evidence for individual recognition in Japanese quail. Behaviour 135 (1998), 551–578.
Schein, M.W., Diamond, M., Carter, C.S., Sexual performance levels of male japanese quail (Coturnix coturnix japonica). Anim. Behav. 20 (1972), 61–67.
Dickens, M.J., Balthazart, J., Cornil, C.A., Brain aromatase and circulating corticosterone are rapidly regulated by combined acute stress and sexual interaction in a sex-specific manner. J. Neuroendocrinol. 24:10 (2012), 1322–1334.
Dickens, M.J., Cornil, C.A., Balthazart, J., Acute stress differentially affects aromatase activity in specific brain nuclei of adult male and female quail. Endocrinology 152:11 (2011), 4242–4251.
Dickens, M.J., Cornil, C.A., Balthazart, J., Neurochemical control of rapid stress-induced changes in brain aromatase activity. J. Neuroendocrinol. 25:4 (2013), 329–339.
Ubuka, T., Haraguchi, S., Tobari, Y., Narihiro, M., Ishikawa, K., Hayashi, T., Harada, N., Tsutsui, K., Hypothalamic inhibition of socio-sexual behaviour by increasing neuroestrogen synthesis. Nat. Commun., 5, 2014, 3061.
Domjan, M., Pavlovian conditioning : a functional perspective. Annu. Rev. Psychol. 56 (2005), 179–206.
Charlier, T.D., Newman, A.E., Heimovics, S.A., Po, K.W., Saldanha, C.J., Soma, K.K., Rapid effects of aggressive interactions on aromatase activity and oestradiol in discrete brain regions of wild male white-crowned sparrows. J. Neuroendocrinol. 23:8 (2011), 742–753.
Remage-Healey, L., Maidment, N.T., Schlinger, B.A., Forebrain steroid levels fluctuate rapidly during social interactions. Nat. Neurosci. 11:11 (2008), 1327–1334.
de Bournonville, M.P., de Bournonville, C., Ball, G.F., Balthazart, J., Cornil, C.A., Rapid changes in preoptic estradiol concentration during male sexual behavior. Abstr. - Soc. Neurosci., 2017 (67.04/HH10).
