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See detailPreoptic glutamate and estradiol release during male sexual behavior
de Bournonville, Catherine ULg; de Bournonville, Marie-Pierre ULg; Aourz, Najat et al

Poster (2016, November)

Beside its long-term control by steroids, male sexual behavior is also modulated by neuroestrogens in a dynamic way (within minutes) in a number of species ranging from fishes to mammals. Studies in male ... [more ▼]

Beside its long-term control by steroids, male sexual behavior is also modulated by neuroestrogens in a dynamic way (within minutes) in a number of species ranging from fishes to mammals. Studies in male Japanese quail have also identified following exposure to a receptive female a rapid decrease in the activity of brain aromatase (AA) the enzyme responsible for the conversion of androgens into estrogens. These effects occur mainly within the medial preoptic nucleus (POM), a sexually dimorphic structure of the preoptic area that plays a key role in the activation of male sexual behavior and contains the highest AA in the brain. In vitro studies demonstrated that AA can be rapidly inhibited by calcium-dependent phosphorylations of the enzyme triggered by the activation of AMPA and kainate receptors. We confirmed here this rapid effect of glutamate on AA by injecting kainate in the POM of anesthetized males and measuring AA in the tissue after brain collection. AA in POM was inhibited in the kainate-injected hemisphere compared to the control hemisphere injected with vehicle. In a second experiment, we showed by in vivo microdialysis that glutamate is released in POM during copulation. These results thus suggest that glutamate controls dynamic changes of AA that occur in the brain during sexual interactions. To confirm that the decrease in AA leads to an actual reduction of local estradiol concentration, we quantified via microdialysis and radioimmunoassay changes in estradiol concentration in the male POM during sexual interactions with a female. Surprisingly, a dramatic elevation of estradiol was observed during copulation. Estradiol has been shown to enhance acutely male sexual motivation, therefore the function of its increase in the POM could be to maintain motivation during the entire sexual encounter. The decrease of AA observed ex vivo after copulation would then reflect a compensatory mechanism to restore baseline pre-copulatory conditions. Importantly, these results highlight that although long-term changes in AA are often used as a proxy for local estradiol concentrations, these two measures can show major short-term discrepancies possibly reflecting variations in estrogen turnover. [less ▲]

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See detailNon-ovarian aromatization is required to activate female sexual motivation in testosterone-treated ovariectomized quail
de Bournonville, Catherine; Balthazart, Jacques ULg; Ball, Gregory et al

in Hormones and Behavior (2016), 83

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See detailEstrogen Receptor β Activation Rapidly Modulates Male Sexual Motivation through the Transactivation of Metabotropic Glutamate Receptor 1a
Seredynski, Aurore L; Balthazart, Jacques ULg; Ball, Gregory F et al

in Journal of Neuroscience (2015), 35(38), 13110-23

In addition to the transcriptional activity of their liganded nuclear receptors, estrogens, such as estradiol (E2), modulate cell functions, and consequently physiology and behavior, within minutes ... [more ▼]

In addition to the transcriptional activity of their liganded nuclear receptors, estrogens, such as estradiol (E2), modulate cell functions, and consequently physiology and behavior, within minutes through membrane-initiated events. The membrane-associated receptors (mERs) underlying the acute effects of estrogens on behavior have mostly been documented in females where active estrogens are thought to be of ovarian origin. We determined here, by acute intracerebroventricular injections of specific agonists and antagonists, the type(s) of mERs that modulate rapid effects of brain-derived estrogens on sexual motivation in male Japanese quail. Brain aromatase blockade acutely inhibited sexual motivation. Diarylpropionitrile (DPN), an estrogen receptor β (ERβ)-specific agonist, and to a lesser extent 17α-estradiol, possibly acting through ER-X, prevented this effect. In contrast, drugs targeting ERα (PPT and MPP), GPR30 (G1 and G15), and the Gq-mER (STX) did not affect sexual motivation. The mGluR1a antagonist LY367385 significantly inhibited sexual motivation but mGluR2/3 and mGluR5 antagonists were ineffective. LY367385 also blocked the behavioral restoration induced by E2 or DPN, providing functional evidence that ERβ interacts with metabotropic glutamate receptor 1a (mGluR1a) signaling to acutely regulate male sexual motivation. Together these results show that ERβ plays a key role in sexual behavior regulation and the recently uncovered cooperation between mERs and mGluRs is functional in males where it mediates the acute effects of estrogens produced centrally in response to social stimuli. The presence of an ER-mGluR interaction in birds suggests that this mechanism emerged relatively early in vertebrate history and is well conserved. Significance statement: The membrane-associated receptors underlying the acute effects of estrogens on behavior have mostly been documented in females, where active estrogens are thought to be of ovarian origin. Using acute intracerebroventricular injections of specific agonists and antagonists following blockade of brain aromatase, we show here that brain-derived estrogens acutely facilitate male sexual motivation through the activation of estrogen receptor β interacting with the metabotropic glutamate receptor 1a. This behavioral effect occurring within minutes provides a mechanistic explanation of how an estrogen receptor not intrinsically coupled to intracellular effectors can signal from the membrane to govern behavior in a very rapid fashion. It suggests that different subtypes of estrogen receptors could regulate the motivation versus performance aspects of behavior. [less ▲]

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See detailDual actions of neuroestrogens on the regulation of behavior
Cornil, Charlotte ULg

Conference (2015, June 08)

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See detailThe dual action of estrogen hypothesis
Cornil, Charlotte ULg; Ball, Gregory F.; Balthazart, Jacques ULg

in Trends in Neurosciences (2015), 38(7), 408-16

Estradiol (E2) can act in the brain in a relatively fast manner (i.e., seconds to minutes) usually through signaling initiated at the cell membrane. Brain-derived E2 has thus been considered as another ... [more ▼]

Estradiol (E2) can act in the brain in a relatively fast manner (i.e., seconds to minutes) usually through signaling initiated at the cell membrane. Brain-derived E2 has thus been considered as another type of neurotransmitter. Recent work found that behaviors indicative of male sexual motivation are activated by estrogenic metabolites of testosterone (T) in a fast manner, while sexual performance (copulatory behavior per se) is regulated by brain E2 in a slower manner via nucleus-initiated actions. This functional division between these two types of action appears to generalize to other behavioral systems regulated by E2. We propose the dual action of estrogen hypothesis to explain this functional distinction between these two different modes of action. [less ▲]

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See detailLocal modulation of steroid action: rapid control of enzymatic activity.
Charlier, Thierry D.; Cornil, Charlotte ULg; Patte-Mensah, Christine et al

in Frontiers in neuroscience (2015), 9

Estrogens can induce rapid, short-lived physiological and behavioral responses, in addition to their slow, but long-term, effects at the transcriptional level. To be functionally relevant, these effects ... [more ▼]

Estrogens can induce rapid, short-lived physiological and behavioral responses, in addition to their slow, but long-term, effects at the transcriptional level. To be functionally relevant, these effects should be associated with rapid modulations of estrogens concentrations. 17beta-estradiol is synthesized by the enzyme aromatase, using testosterone as a substrate, but can also be degraded into catechol-estrogens via hydroxylation by the same enzyme, leading to an increase or decrease in estrogens concentration, respectively. The first evidence that aromatase activity (AA) can be rapidly modulated came from experiments performed in Japanese quail hypothalamus homogenates. This rapid modulation is triggered by calcium-dependent phosphorylations and was confirmed in other tissues and species. The mechanisms controlling the phosphorylation status, the targeted amino acid residues and the reversibility seem to vary depending of the tissues and is discussed in this review. We currently do not know whether the phosphorylation of the same amino acid affects both aromatase and/or hydroxylase activities or whether these residues are different. These processes provide a new general mechanism by which local estrogen concentration can be rapidly altered in the brain and other tissues. [less ▲]

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See detailAnatomically discrete sex differences in neuroplasticity in zebra finches as reflected by perineuronal nets.
Cornez, Gilles; Ter Haar, Sita M.; Cornil, Charlotte ULg et al

in PloS one (2015), 10(4), 0123199

Large morphological sex differences in the vertebrate brain were initially identified in song control nuclei of oscines. Besides gross differences between volumes of nuclei in males and females, sex ... [more ▼]

Large morphological sex differences in the vertebrate brain were initially identified in song control nuclei of oscines. Besides gross differences between volumes of nuclei in males and females, sex differences also concern the size and dendritic arborization of neurons and various neurochemical markers, such as the calcium-binding protein parvalbumin (PV). Perineuronal nets (PNN) of the extracellular matrix are aggregates of different compounds, mainly chondroitin sulfate proteoglycans, that surround subsets of neurons, often expressing PV. PNN develop in zebra finches song control nuclei around the end of the sensitive period for song learning and tutor deprivation, known to delay the end of the song learning sensitive period, decreases the numbers of PNN in HVC. We demonstrate here the existence in zebra finches of a major sex difference (males > females) affecting the number of PNN (especially those surrounding PV-positive cells) in HVC and to a smaller extent the robust nucleus of the arcopallium, RA, the two main nuclei controlling song production. These differences were not present in Area X and LMAN, the lateral magnocellular nucleus of the anterior nidopallium. A dense expression of material immunoreactive for chondroitin sulfate was also detected in several nuclei of the auditory and visual pathways. This material was often organized in perineuronal rings but quantification of these PNN did not reveal any sex difference with the exception that the percentage of PNN surrounding PV-ir cells in the dorsal lateral mesencephalic nucleus, MLd, was larger in females than in males, a sex difference in the opposite direction compared to what is seen in HVC and RA. These data confirm and extend previous studies demonstrating the sex difference affecting PNN in HVC-RA by showing that this sex difference is anatomically specific and does not concern visual or auditory pathways. [less ▲]

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See detailGlutamate controls brain estrogen synthesis during sexual interactions
de Bournonville, Catherine ULg; Aourz, Najat; Van Eeckhaut, Ann et al

Poster (2014, November 17)

Besides their long-lasting effects mediated by a modulation of gene transcription, brain-derived estrogens can rapidly regulate (within minutes) reproductive behaviors. In vitro, the activity of aromatase ... [more ▼]

Besides their long-lasting effects mediated by a modulation of gene transcription, brain-derived estrogens can rapidly regulate (within minutes) reproductive behaviors. In vitro, the activity of aromatase (AA), the enzyme responsible for the conversion of androgens into estrogens, is also regulated on a similar short time-scale, via phosphorylation of the enzyme resulting from changes in neuronal activity or glutamate release. Acute changes in AA have been documented ex vivo in specific brain regions following exposure to social or stressful stimuli but the mechanism underlying these regulations is not known. To investigate whether glutamate is implicated in these rapid changes in AA, male quail received a unilateral injection of kainate in the medial preoptic nucleus (POM). The left and right preoptic areas were collected 20 min later and assayed separately by the tritiated water technique for AA. As shown previously in preoptic explants maintained in vitro, AA was downregulated in the kainate-injected hemisphere as compared to the non-injected side. To determine whether the decline in AA detected in the POM after a sexual interaction could be mediated by an increased release of glutamate in this region, extracellular glutamate concentration was measured by in vivo microdialysis with a probe implanted in the POM of sexually mature males. Dialysate was collected every 3 minutes over three periods of 15 min when the male was (1) alone, (2) allowed to freely copulate with a female and (3) alone again. A transient rise in extracellular glutamate concentration was observed specifically and immediately after the expression of cloacal contact movements, when semen is transferred to the female. Glutamate returned to a basal level after the female was removed. Together, these results indicate that the mechanism of acute regulation of aromatase activity by glutamate identified in vitro is potentially responsible for the acute regulation of the enzyme observed in vivo following copulation. As rapid changes in brain estrogen synthesis and its actions are apparently related to the control of sexual motivation rather than sexual performance, follow up experiments should now determine whether the release of glutamate in the POM occurs in parallel with an increase in motivation or follows the termination of the copulatory sequence. [less ▲]

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See detailAge-dependent and age-independent effects of testosterone in male quail
Cornil, Charlotte ULg; Schmit, Mélanie; de Bournonville, Catherine ULg et al

in General and Comparative Endocrinology (2014), 208C

Various studies in rodents recently concluded that puberty should be considered as a second period of organization of brain and behavior and that action of sex steroids at that time is long lasting and ... [more ▼]

Various studies in rodents recently concluded that puberty should be considered as a second period of organization of brain and behavior and that action of sex steroids at that time is long lasting and possibly permanent. We tested this notion in male Japanese quail that had been castrated before 3 weeks post- hatch by analyzing whether a similar treatment with exogenous testosterone initiated at 3, 5 or 7 weeks post-hatch has a differential influence on the development of testosterone-dependent morphological, behavioral and neural characteristics that are known to be sexually differentiated. The growth of the androgen-dependent cloacal gland was significantly faster when testosterone treatment was initiated later in life indicating that the target tissue is not ready to fully respond to androgens at 3 weeks post- hatch. The three groups of birds nevertheless developed a gland of the same size typical of intact sexually mature birds. When adults, all birds expressed copulatory behavior with the same frequencies and laten- cies and they displayed the same level of aromatase activity and of vasotocinergic innervation in the pre- optic area as gonadally intact males despite the fact that they had been treated with testosterone for different durations starting at different ages. Surprisingly, the frequency of cloacal sphincter contractions, a measure of appetitive sexual behavior, was significantly higher when testosterone treatment had been initiated later. Together these data provide no clear evidence for an organizational action of testosterone during sexual maturation of male quail but additional experiments should investigate whether estrogens have such an action in females. [less ▲]

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See detailRelationships between rapid changes in local aromatase activity and estradiol concentrations in male and female quail brain.
Dickens, M. J.; de Bournonville, Catherine ULg; Balthazart, Jacques ULg et al

in Hormones and behavior (2014), 65(2), 154-164

Estradiol-17beta (E2) synthesized in the brain plays a critical role in the activation of sexual behavior in many vertebrate species. Because E2 concentrations depend on aromatization of testosterone ... [more ▼]

Estradiol-17beta (E2) synthesized in the brain plays a critical role in the activation of sexual behavior in many vertebrate species. Because E2 concentrations depend on aromatization of testosterone, changes in aromatase enzymatic activity (AA) are often utilized as a proxy to describe E2 concentrations. Utilizing two types of stimuli (sexual interactions and acute restraint stress) that have been demonstrated to reliably alter AA within minutes in opposite directions (sexual interactions=decrease, stress=increase), we tested in Japanese quail whether rapid changes in AA are paralleled by changes in E2 concentrations in discrete brain areas. In males, E2 in the pooled medial preoptic nucleus/medial portion of the bed nucleus of the stria terminalis (POM/BST) positively correlated with AA following sexual interactions. However, following acute stress, E2 decreased significantly (approximately 2-fold) in the male POM/BST despite a significant increase in AA. In females, AA positively correlated with E2 in both the POM/BST and mediobasal hypothalamus supporting a role for local, as opposed to ovarian, production regulating brain E2 concentrations. In addition, correlations of individual E2 in POM/BST and measurements of female sexual behavior suggested a role for local E2 synthesis in female receptivity. These data demonstrate that local E2 in the male brain changes in response to stimuli on a time course suggestive of potential non-genomic effects on brain and behavior. Overall, this study highlights the complex mechanisms regulating local E2 concentrations including rapid stimulus-driven changes in production and stress-induced changes in catabolism. [less ▲]

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See detailSex in the brain
Cornil, Charlotte ULg

in International innovation (2014), 157

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See detailMechanism of the medium-duration afterhyperpolarization in rat serotonergic neurons
Alix, Philippe ULg; Venkatesan, Kumar; Scuvée-Moreau, Jacqueline et al

in European Journal of Neuroscience (2014), 39(2), 186-196

Most serotonergic neurons display a prominent medium-duration afterhyperpolarization (mAHP), which is mediated by small conductance Ca2+-activated K+ (SK) channels. Recent ex vivo and in vivo experiments ... [more ▼]

Most serotonergic neurons display a prominent medium-duration afterhyperpolarization (mAHP), which is mediated by small conductance Ca2+-activated K+ (SK) channels. Recent ex vivo and in vivo experiments have suggested that SK channel blockade increases the firing rate and/or bursting in these neurons. The purpose of this study was therefore to characterize the source of Ca2+ which activates the mAHP channels in serotonergic neurons. In voltage clamp experiments, an outward current was recorded at -60 mV after a depolarizing pulse to + 100 mV. A supra-maximal concentration of the SK channel blockers apamin or (-)- bicuculline methiodide blocked this outward current. This current was also sensitive to the broad Ca2+ channel blocker Co2+ and was partially blocked by both ω-conotoxin and mibefradil, which are blockers of N-type and T-type Ca2+ channels, respectively. Neither blockers of other voltage-gated Ca2+ channels nor DBHQ, an inhibitor of Ca2+-induced Ca2+ release, had any effect on the SK current. [less ▲]

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See detailEstrogens control female sexual motivation and receptivity in quail.
de Bournonville, Catherine ULg; Ball, Gregory, F.; Balthazart, Jacques ULg et al

Poster (2013, November 10)

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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 detailFemale sexual and social behaviors are controlled by estrogens
de Bournonville, Catherine ULg; Ball, Gregory F; Balthazart, Jacques ULg et al

Poster (2013)

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See detailFemale sexual motivation is controlled by estrogens in quail
de Bournonville, Catherine ULg; Ball, Gregory F; Balthazart, Jacques ULg et al

Poster (2013)

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See detailLocal estradiol synthesis in the brain and its implication in male and female sexual motivation of Japanese quail
de Bournonville, Catherine ULg; Schmit, Mélanie; Ball, Gregory F et al

in Trabajos del Instituto Cajal (2013)

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See detailAre neuroestrogens implicated in sexual motivation? Development of experimental protocols.
de Bournonville, Catherine ULg; Schmit, Mélanie; Ball, Gregory F et al

Poster (2013)

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