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See detailc-fos down-regulation inhibits testosterone-dependent male sexual behavior and the associated learning
Niessen, Neville-Andrew ULg; Balthazart, Jacques ULg; Ball, Gregory et al

in European Journal of Neuroscience (2013)

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See detailNeuroestrogens Rapidly Regulate Sexual Motivation But Not Performance
Seredynski, Aurore ULg; Balthazart, Jacques ULg; Christophe, Virginie et al

in Journal of Neuroscience (2013), 33(1), 164-174

Estrogens exert pleiotropic effects on reproductive traits, which include differentiation and activation of reproductive behaviors and the control of the secretion of gonadotropins. Estrogens also ... [more ▼]

Estrogens exert pleiotropic effects on reproductive traits, which include differentiation and activation of reproductive behaviors and the control of the secretion of gonadotropins. Estrogens also profoundly affect non-reproductive traits, such as cognition and neuroprotection. These effects are usually attributed to nuclear receptor binding and subsequent regulation of target gene transcription. Estrogens also affect neuronal activity and cell-signaling pathways via faster, membrane-initiated events. How these two types of actions that operate in distinct timescales interact in the control of complex behavioral responses is poorly understood. Here, we show that the central administration of estradiol rapidly increases the expression of sexual motivation, as assessed by several measures of sexual motivation produced in response to the visual presentation of a female but not sexual performance in male Japanese quail. This effect is mimicked by membrane-impermeable analogs of estradiol, indicating that it is initiated at the cell membrane. Conversely, blocking the action of estrogens or their synthesis by a single intracerebroventricular injection of estrogen receptor antagonists or aromatase inhibitors, respectively, decreases sexual motivation within minutes without affecting performance. The same steroid has thus evolved complementary mechanisms to regulate different behavioral components (motivation vs performance) in distinct temporal domains (long- vs short-term) so that diverse reproductive activities can be properly coordinated to improve reproductive fitness. Given the pleiotropic effects exerted by estrogens, other responses controlled by these steroids might also depend on a slow genomic regulation of neuronal plasticity underlying behavioral activation and an acute control of motivation to engage in behavior. [less ▲]

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See detailDistinct Neuroendocrine mechanisms control neural activity underlying sex differences in sexual motivation and performance
Balthazart, Jacques ULg; Corbisier de Méaultsart, Céline; Ball, Gregory et al

in European Journal of Neuroscience (2013), 37(5), 735-42

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 ... [more ▼]

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. [less ▲]

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See detailCellular mechanisms controlling rapid changes in brain aromatase activity
Charlier, Thierry; Cornil, Charlotte ULg; Ball, Gregory et al

in Balthazart, Jacques; Ball, Gregory (Eds.) Brain aromatase, estrogens and behavior (2012)

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See detailRapid modulation of aromatase activity by social and environmental stimuli in quail
Cornil, Charlotte ULg; Dickens, Molly; BAll, Gregory et al

in Balthazart, Jacques; Ball, Gregory (Eds.) Brain aromatase, estrogens and behavior (2012)

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See detailSex differences in brain aromatase activity: genomic and non-genomic controls
Balthazart, Jacques ULg; Charlier, Thierry ULg; Cornil, Charlotte ULg et al

in Frontiers in Endocrinology (2011), 2

Aromatization of testosterone into estradiol in the preoptic area plays a critical role in the activation of male copulation in quail and in many other vertebrate species. Aromatase expression in quail ... [more ▼]

Aromatization of testosterone into estradiol in the preoptic area plays a critical role in the activation of male copulation in quail and in many other vertebrate species. Aromatase expression in quail and in other birds is higher than in rodents and other mammals, which has facilitated the study of the controls and functions of this enzyme. Over relatively long time periods (days to months), brain aromatase activity (AA), and transcription are markedly (four- to sixfold) increased by genomic actions of sex steroids. Initial work indicated that the preoptic AA is higher in males than in females and it was hypothesized that this differential production of estrogen could be a critical factor responsible for the lack of behavioral activation in females. Subsequent studies revealed, however, that this enzymatic sex difference might contribute but is not sufficient to explain the sex difference in behavior. Studies of AA, immunoreactivity, and mRNA concentrations revealed that sex differences observed when measuring enzymatic activity are not necessarily observed when one measures mRNA concentrations. Discrepancies potentially reflect post-translational controls of the enzymatic activity. AA in quail brain homogenates is rapidly inhibited by phosphorylation processes. Similar rapid inhibitions occur in hypothalamic explants maintained in vitro and exposed to agents affecting intracellular calcium concentrations or to glutamate agonists. Rapid changes in AA have also been observed in vivo following sexual interactions or exposure to short-term restraint stress and these rapid changes in estrogen production modulate expression of male sexual behaviors. These data suggest that brain estrogens display most if not all characteristics of neuromodulators if not neurotransmitters. Many questions remain however concerning the mechanisms controlling these rapid changes in estrogen production and their behavioral significance. [less ▲]

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See detailRapid regulation by glutamate of aromatase activity
Charlier, Thierry ULg; Ball, Gregory; Balthazart, Jacques ULg

Poster (2011)

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See detailEffects of social experience on subsequent sexual performance in naïve male Japanese quail (Coturnix japonica)
Cornil, Charlotte ULg; Ball, Gregory

in Hormones & Behavior (2010), 57

On their first sexual encounter, naïve male Japanese quail will attend to and approach a female; they sometimes mount but they do not always copulate. During the second encounter, most males successfully ... [more ▼]

On their first sexual encounter, naïve male Japanese quail will attend to and approach a female; they sometimes mount but they do not always copulate. During the second encounter, most males successfully copulate. Although sexual experience facilitates subsequent sexual interactions, sensory cues provided by females, independent of any sexual encounter, may also enhance sexual performance. To investigate whether previous exposure to a conspecific affects subsequent sexual behavior, we allowed inexperienced males to observe an empty box, or a conspecific consisting of either an experienced female or male for 2.5 min/day on 7 days. Measures of appetitive sexual behavior were recorded during these tests. On day 8, subjects were allowed to copulate with a novel female for 5 min. On the following days, all subjects were repeatedly provided with visual access to a female and allowed to mate. In the pre-copulatory trials males initially exhibited a high frequency of appetitive responses that dissipated with repetition. Pre-copulatory experience also significantly affected motivation to mate with subjects exposed to females copulating more quickly than other subjects. Post-copulatory appetitive behavior also differed between groups: control subjects showed the highest behavioral frequency followed by males exposed to females and finally males exposed to males. These data indicate that pre-copulatory social experience profoundly influences subsequent sexual behavior and probably reproductive success. This experience effect is independent of any hormonal effect (such as one resulting from changes in secretion following different social interactions) given that the subjects were castrates chronically treated with testosterone. [less ▲]

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See detailDiversity of mechanisms involved in aromatase regulation and estrogen action in the brain
Charlier, Thierry ULg; Cornil, Charlotte ULg; Ball, Gregory et al

in Biochimica et Biophysica Acta - General Subjects (2010)

Background In recent years, the mechanisms through which estrogens modulate neuronal physiology, brain morphology, and behavior have proven to be far more complex than previously thought. For example, a ... [more ▼]

Background In recent years, the mechanisms through which estrogens modulate neuronal physiology, brain morphology, and behavior have proven to be far more complex than previously thought. For example, a second nuclear estrogen receptor has been identified, a new family of coregulatory proteins regulating steroid-dependent gene transcriptions was discovered and, finally, it has become clear that estrogens have surprisingly rapid effects based on their actions on cell membranes, which in turn result in the modulation of intracellular signaling cascades. Scope of review This paper presents a selective review of new findings in this area related to work in our laboratories, focusing on the role of estrogens in the activation of male sexual behavior. Two separate topics are considered. We first discuss functions of the steroid receptor coactivator-1 (SRC-1) that has emerged as a key limiting factor for behavioral effects of estradiol. Knocking-down its expression by antisense oligonucleotides drastically inhibits male-typical sexual behaviors. Secondly, we describe rapid regulations of brain estradiol production by calcium-dependent phosphorylations of the aromatase enzyme, themselves under the control of neurotransmitter activity. These rapid changes in estrogen bioavailability have clear behavioral consequences. Increases or decreases in estradiol concentrations respectively obtained by an acute injection of estradiol itself or of an aromatase inhibitor lead within 15–30 min to parallel changes in sexual behavior frequencies. These new controls of estrogen action offer a vast array of possibilities for discrete local controls of estrogen action. They also represent a formidable challenge for neuroendocrinologists trying to obtain an integrated view of brain function in relation to behavior. [less ▲]

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See detailSex steroid-induced neuroplasticity and behavioral activation in birds
Balthazart, Jacques ULg; Charlier, Thierry ULg; Barker, Jennifer ULg et al

in European Journal of Neuroscience (2010), 32

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See detailRapid regulation of aromatase activity and the role of stress
Dickens, Molly; Charlier, Thierry ULg; Cornil, Charlotte ULg et al

Poster (2010)

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See detailIs sexual motivational state linked to dopamine release in the medial preoptic area?
Kleitz-Nelson, Hayley; Dominguez, Juan; Cornil, Charlotte ULg et al

in Behavioral Neuroscience (2010)

The medial preoptic area (mPOA) is a key site for the dopaminergic enhancement of male sexual behavior. Dopamine release increases in the rat mPOA with mating, supporting the critical stimulatory role ... [more ▼]

The medial preoptic area (mPOA) is a key site for the dopaminergic enhancement of male sexual behavior. Dopamine release increases in the rat mPOA with mating, supporting the critical stimulatory role played by preoptic dopamine on male sexual behavior. However, it has been questioned whether dopamine is specifically related to the occurrence of male sexual behavior and not simply involved in general arousal. To address this question, we ask whether dopamine release in the mPOA is linked to the production of male sexual behavior in Japanese quail, a species that exhibits a much shorter temporal pattern of copulation than rats and does not have an intromittent organ, resulting in a very different topography of their sexual response. Extracellular samples from the mPOA of adult sexually experienced male quail were collected every six minutes before, during, and after exposure to a female using in vivo microdialysis and analyzed using HPLC-EC. Extracellular dopamine significantly increased in the presence of a female and returned to baseline after removal of the female. However, subjects who failed to copulate did not display this increased release. These findings indicate that it is not solely the presence of a female that drives dopamine release in males, but how a male responds to her. Further, in subjects that copulated, dopamine release did not change in samples collected during periods of no copulation. Together, these findings support the hypothesis that dopamine action in the mPOA is specifically linked to sexual motivation and not only copulatory behavior or physical arousal. [less ▲]

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See detailBehavioral effects of rapid changes in aromatase activity in the central nervous system
Balthazart, Jacques ULg; Baillien, Michelle; Cornil, Charlotte ULg et al

in Kordon, C.; Gaillard, R. C.; Christen, Y. (Eds.) Research and perspectives in endocrine action (2004)

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See detailCalcium-dependent phosphorylation processes control brain aromatase in quail
Balthazart, Jacques ULg; Baillien, Michelle; Charlier, Thierry ULg et al

in European Journal of Neuroscience (2003), 17(8), 1591-1606

Increased gene transcription activated by the binding of sex steroids to their cognate receptors is one important way in which oestrogen synthase (aromatase) activity is regulated in the brain. This ... [more ▼]

Increased gene transcription activated by the binding of sex steroids to their cognate receptors is one important way in which oestrogen synthase (aromatase) activity is regulated in the brain. This control mechanism is relatively slow (hours to days) but recent data indicate that aromatase activity in quail preoptic-hypothalamic homogenates is also rapidly (within minutes) affected by exposure to conditions that enhance Ca2+-dependent protein phosphorylation. We demonstrate here that Ca2+-dependent phosphorylations controlled by the activity of multiple protein kinases including PKC, and possibly also PKA and CAMK, can rapidly down-regulate aromatase activity in brain homogenates. These phosphorylations directly affect the aromatase molecule itself. Western blotting experiments on aromatase purified by immunoprecipitation reveal the presence on the enzyme of phosphorylated serine, threonine and tyrosine residues in concentrations that are increased by phosphorylating conditions. Cloning and sequencing of the quail aromatase identified a 1541-bp open reading frame that encodes a predicted 490-amino-acid protein containing all the functional domains that have been previously described in the mammalian and avian aromatase. Fifteen predicted consensus phosphorylation sites were identified in this sequence, but only two of these (threonine 455 and 486) match the consensus sequences corresponding to the protein kinases that were shown to affect aromatase activity during the pharmacological experiments (i.e. PKC and PKA). This suggests that the phosphorylation of one or both of these residues represents the mechanism underlying, at least in part, the rapid changes in aromatase activity. [less ▲]

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See detailMultiple mechanisms control brain aromatase activity at the genomic and non-genomic level
Balthazart, Jacques ULg; Baillien, Michelle; Charlier, Thierry ULg et al

in Journal of Steroid Biochemistry & Molecular Biology (2003), 86

Evidence has recently accumulated indicating that aromatase activity in the preoptic area is modulated in parallel by both slow (hours to days) genomic and rapid (minutes to hours) non-genomic mechanisms ... [more ▼]

Evidence has recently accumulated indicating that aromatase activity in the preoptic area is modulated in parallel by both slow (hours to days) genomic and rapid (minutes to hours) non-genomic mechanisms. We review here these two types of control mechanisms and their potential contribution to various aspects of brain physiology in quail. High levels of aromatase mRNA, protein and activity (AA) are present in the preoptic area of this species where the transcription of aromatase is controlled mainly by steroids. Estrogens acting in synergy with androgens play a key role in this control and both androgen and estrogen receptors (ER; alpha and beta subtypes) are present in the preoptic area even if they are not necessarily co-localized in the same cells as aromatase. Steroids have more pronounced effects on aromatase transcription in males than in females and this sex difference could be caused, in part, by a sexually differentiated expression of the steroid receptor coactivator 1 in this area. The changes in aromatase concentration presumably control seasonal variations as well as sex differences in brain estrogen production. Aromatase activity in hypothalamic homogenates is also rapidly (within minutes) down-regulated by exposure to conditions that enhance protein phosphorylation such as the presence of high concentrations of calcium, magnesium and ATP. Similarly, pharmacological manipulations such as treatment with thapsigargin or stimulation of various neurotransmitter receptors (alpha-amino-3-hydroxy-methyl-4-isoxazole propionic acid (AMPA), kainate, and N-methyl-d-aspartate (NMDA)) leading to enhanced intracellular calcium concentrations depress within minutes the aromatase activity measured in quail preoptic explants. The effects of receptor stimulation are presumably direct: electrophysiological data confirm the presence of these receptors in the membrane of aromatase-expressing cells. Inhibitors of protein kinases interfere with these processes andWestern blotting experiments on brain aromatase purified by immunoprecipitation confirm that the phosphorylations regulating aromatase activity directly affect the enzyme rather than another regulatory protein. Accordingly, several phosphorylation consensus sites are present on the deduced amino acid sequence of the recently cloned quail aromatase. Fast changes in the local availability of estrogens in the brain can thus be caused by aromatase phosphorylation so that estrogen could rapidly regulate neuronal physiology and behavior. The rapid as well as slower processes of local estrogen production in the brain thus match well with the genomic and non-genomic actions of steroids in the brain. These two processes potentially provide sufficient temporal variation in the bio-availability of estrogens to support the entire range of established effects for this steroid. [less ▲]

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See detailThe neuroendocrinology of reproductive behavior in Japanese quail
Balthazart, Jacques ULg; Baillien, Michelle; Charlier, Thierry ULg et al

in Domestic Animal Endocrinology (2003), 25

Sex steroid hormones such as testosterone have widespread effects on brain physiology and function but one of their best characterized effects arguably involves the activation of male sexual behavior ... [more ▼]

Sex steroid hormones such as testosterone have widespread effects on brain physiology and function but one of their best characterized effects arguably involves the activation of male sexual behavior. During the past 20 years we have investigated the testosterone control of male sexual behavior in an avian species, the Japanese quail (Coturnix japonica).We briefly reviewhere the main features and advantages of this species relating to the investigation of fundamental questions in the field of behavioral neuroendocrinology, a field that studies inter-relationship among hormones, brain and behavior. Special attention is given to the intracellular metabolism of testosterone, in particular its aromatization into an estrogen, which plays a critical limiting role in the mediation of the behavioral effects of testosterone. Brain aromatase activity is controlled by steroids which increase the transcription of the enzyme, but afferent inputs that affect the intraneuronal concentrations of calcium also appear to have a pronounced effect on the enzyme activity through rapid changes in its phosphorylation status. The physiological significance of these slowgenomic and rapid, presumably non-genomic, changes in brain aromatase activity are also briefly discussed. [less ▲]

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