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See detailRapid changes in preoptic estradiol concentration during male sexual behavior
de Bournonville, Marie-Pierre ULiege; de Bournonville, Catherine; Ball, Gregory et al

Poster (2017, November 11)

Estrogens such as estradiol (E2) exert pleiotropic effects on physiological and behavioral responses such as neuroprotection, aggression or reproduction. Estrogens derived from local brain synthesis ... [more ▼]

Estrogens such as estradiol (E2) exert pleiotropic effects on physiological and behavioral responses such as neuroprotection, aggression or reproduction. Estrogens derived from local brain synthesis (neuroestrogens) are critical for the regulation of different functions including the control of male sexual behavior. Classically, E2 acts through effects initiated in the nucleus to regulate male sexual function. Along with these long-term effects, E2 also acts rapidly (within minutes) via membrane-initiated events. These effects are thought to depend on short-term variations in the local production of estrogens, through rapid fluctuations of the enzymatic activity of brain aromatase. In Japanese quail, rapid modulations of brain aromatase activity (AA) have been reported after sexual interactions or exposure to an acute stress. These changes take place mainly in the medial preoptic nucleus (POM), a sexually differentiated structure that plays a key role in the control of male sexual behavior and where aromatase is densely expressed. Yet, it has recently been shown that, in the short term, AA does not always reflect local E2 concentration. This study was designed to determine by in vivo microdialysis whether local E2 concentrations fluctuate during sexual interactions and test whether these changes parallel the decrease in AA observed ex vivo after copulation. We first conducted a series of experiments to validate the microdialysis and E2 assay. When dialysis probes were placed in successive baths containing known increasing amounts of E2, proportional changes in E2 concentration were measured in the dialysate. Moreover, a rise in E2 concentration was detected after in vivo retrodialysis of testosterone only if the probe was located within the POM and, after a peripheral injection of E2, a sharp rise of E2 was detected regardless of the probe location. Together these results show that in vivo microdialysis is a valid method to assess endogenous fluctuations of brain E2 concentrations in behaving animals. Two independent experiments then identified a rise in E2 concentrations in POM during sexual interactions. This increase occurred within 10 min after the initiation of the sexual interaction and was specific to the POM as there was no increase in E2 concentrations in males that had their cannula outside of this area. Together these data confirm that rapid changes in AA measured ex vivo cannot be considered as a reliable proxy for E2 concentrations. The discrepancies could originate either from the different time resolution related to the two techniques or from differences in the microenvironment in which aromatase functions in vivo and during ex vivo assays. [less ▲]

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See detailChanges in preoptic estradiol concentrations during male sexual behavior
de Bournonville, Marie-Pierre ULiege; de Bournonville, Catherine; Ball, Gregory et al

in Frontiers in Neuroscience (2017, May 30)

Besides its long-term control by steroids, male sexual behavior is also modulated by membrane-initiated effects of neuroestrogens in the short-term (within minutes). These effects are thought to depend on ... [more ▼]

Besides its long-term control by steroids, male sexual behavior is also modulated by membrane-initiated effects of neuroestrogens in the short-term (within minutes). These effects are thought to depend on short-term variations in the local production of estrogens, through rapid fluctuations of the enzymatic activity of brain aromatase, the enzyme that synthesizes estradiol (E2) from testosterone. Studies in male Japanese quail have shown that a sexual interaction with a female leads to a decrease in the activity of brain aromatase within minutes. 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 aromatase activity (AA) in the brain. However recent studies showed that AA does not always reflect local E2 concentration. For example, while an acute stress decreases AA in the POM, E2 concentration increases in the same conditions. Here we used in vivo microdialysis to quantify changes in E2 concentration in the male POM during sexual interactions with a female. A series of experiments conducted to validate the in vivo dialysis and RIA methods showed that (1) E2 concentration in the dialysate change linearly with the concentration of a bath containing known amounts of E2 in which the probe was placed, (2) an increase in preoptic E2 concentration is observed after retrodialysis of testosterone and (3) preoptic E2 levels also increase after a peripheral injection of E2. Together these results suggest that in vivo dialysis is a suitable method to assay E2 in the range of brain concentrations suspected to be present in physiological conditions. With this approach, we showed during two independent experiments that E2 concentrations increase in the POM during sexual interactions with a female. Birds that had their cannula placed outside the POM did not show any increase in E2 levels. The E2 increase in the POM could serve 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. [less ▲]

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See detailPerineuronal nets and song learning-related neuroplasticity in the songbird brain
Cornez, Gilles ULiege; Jonckers, Elisabeth; Schevchouk, Olesya et al

Conference (2017, May 22)

Perineuronal nets (PNN) are aggregations of extracellular matrix components surrounding the soma of some neurons, mainly GABAergic interneurons expressing the calcium binding protein parvalbumin (PV+). In ... [more ▼]

Perineuronal nets (PNN) are aggregations of extracellular matrix components surrounding the soma of some neurons, mainly GABAergic interneurons expressing the calcium binding protein parvalbumin (PV+). In mammals, the development of PNN limits synaptogenesis around PV+ neurons and PNN have been validated as a marker characterizing the end of critical periods for visual learning. In songbirds, song learning is limited to critical periods during ontogeny in close-ended learners such as zebra finches and to specific phases of the annual cycle in open-ended learners such as canaries that are able to modify their song seasonally. Sensitive periods for song learning are associated with neuroplasticity including morphological changes due to neurogenesis and synaptic reorganization in the song control nuclei during development and adult seasonal song modifications. The hormonal control of developmental and seasonal neuroplasticity is well documented in songbirds but little is known about the possible regulation of sensitive periods for vocal learning by PNN. First, to explore the expression of PNN throughout the development, we used zebra finches brains collected at different key ages in the song learning process (10, 20, 30, 40, 50, 60, 90, 120 days post-hatch, dph) and we quantified PNN expression and their colocalization around PV+ interneurons. The number of PNN and the % of PNN around PV+ interneurons increased progressively during developmental song learning in 3 of the main song control nuclei (HVC, RA and Area X). Moreover, we confirmed that females that never sing have fewer PNN than males in HVC and RA, two song nuclei involved in song production, at all ages after the peak in PNN numbers seen in males between 50 and 90 dph. Secondly we used adult male and female canaries (in 2 different experiments) treated with a subcutaneous implant filled with testosterone or left empty in control subjects to mimic what happens in the spring when the seasonal modification of the song ends and the song crystallizes. Testosterone significantly increased the number of PNN in the main song control nuclei in both sexes. Together these data suggest that increased expression of PNN in the songbird brain might limit neuroplasticity at the end of developmental and seasonal vocal learning [less ▲]

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See detailPerineuronal nets and vocal plasticity in songbirds: a proposed mechanism to explain the difference between closed-ended and open-ended learning
Cornez, Gilles ULiege; Madison, F.N.; Van der Linden, A. et al

in Developmental Neurobiology (2017)

Perineuronal nets (PNN) are aggregations of chondroitin sulfate proteoglycans surrounding the soma and proximal processes of neurons, mostly GABAergic interneurons expressing parvalbumin. They limit the ... [more ▼]

Perineuronal nets (PNN) are aggregations of chondroitin sulfate proteoglycans surrounding the soma and proximal processes of neurons, mostly GABAergic interneurons expressing parvalbumin. They limit the plasticity of their afferent synaptic connections. In zebra finches PNN develop in an experience-dependent manner in the song control nuclei HVC and RA (nucleus robustus arcopallialis) when young birds crystallize their song. Because songbird species that are open-ended learners tend to recapitulate each year the different phases of song learning until their song crystallizes at the beginning of the breeding season, we tested whether seasonal changes in PNN expression would be found in the song control nuclei of a seasonally breeding species such as the European starling. Only minimal changes in PNN densities and total number of cells surrounded by PNN were detected. However, comparison of the density of PNN and of PNN surrounding parvalbumin-positive cells revealed that these structures are far less numerous in starlings that show extensive adult vocal plasticity, including learning of new songs throughout the year, than in the closed-ended learner zebra finches. Canaries that also display some vocal plasticity across season but were never formally shown to learn new songs in adulthood were intermediate in this respect. Together these data suggest that establishment of PNN around parvalbumin-positive neurons in song control nuclei has diverged during evolution to control the different learning capacities observed in songbird species. This differential expression of PNN in different songbird species could represent a key cellular mechanism mediating species variation between closed-ended and open-ended learning strategies. [less ▲]

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See detailStudies of HVC Plasticity in Adult Canaries Reveal Social Effects and Sex Differences as Well as Limitations of Multiple Markers Available to Assess Adult Neurogenesis.
Shevchouk, Olesya ULiege; Ball, G.F.; Cornil, Charlotte ULiege et al

in PLoS ONE (2017), 12(1), 0170938

In songbirds, neurogenesis in the song control nucleus HVC is sensitive to the hormonal and social environment but the dynamics of this process is difficult to assess with a single exogenous marker of new ... [more ▼]

In songbirds, neurogenesis in the song control nucleus HVC is sensitive to the hormonal and social environment but the dynamics of this process is difficult to assess with a single exogenous marker of new neurons. We simultaneously used three independent markers to investigate HVC neurogenesis in male and female canaries. Males were castrated, implanted with testosterone and housed either alone (M), with a female (M-F) or with another male (M-M) while females were implanted with 17β- estradiol and housed with a male (F-M). All subjects received injections of the two thymidine analogues, BrdU and of EdU, respectively 21 and 10 days before brain collection. Cells containing BrdU or EdU or expressing doublecortin (DCX), which labels newborn neurons, were quantified. Social context and sex differentially affected total BrdU+, EdU+, BrdU+EdU- and DCX+ populations. M-M males had a higher density of BrdU+ cells in the ventricular zone adjacent to HVC and of EdU+ in HVC than M-F males. M birds had a higher ratio of BrdU+EdU- to EdU+ cells than M-F subjects suggesting higher survival of newer neurons in the former group. Total number of HVC DCX+ cells was lower in M-F than in M-M males. Sex differences were also dependent of the type of marker used. Several technical limitations associated with the use of these multiple markers were also identified. These results indicate that proliferation, recruitment and survival of new neurons can be independently affected by environmental conditions and effects can only be fully discerned through the use of multiple neurogenesis markers. [less ▲]

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See detailTopography and Lateralized Effect of Acute Aromatase Inhibition on Auditory Processing in a Seasonal Songbird
de groof, Geert; Balthazart, Jacques ULiege; Cornil, Charlotte ULiege et al

in Journal of Neuroscience (2017), 37(16), 4243-4254

It is increasingly recognized that brain-derived estrogens (neuroestrogens) can regulate brain physiology and behavior much faster than what was previously known from the transcriptional action of ... [more ▼]

It is increasingly recognized that brain-derived estrogens (neuroestrogens) can regulate brain physiology and behavior much faster than what was previously known from the transcriptional action of estrogens on nuclear receptors. One of the best examples of such neuro- modulation by neuroestrogens concerns the acute regulation of sensory coding by the auditory cortex as demonstrated by electrophys- iological studies of selected neurons in zebra finches. Yet, the spatial extent of such modulation by neuroestrogens is not known. Using functional magnetic resonance imaging, we demonstrate here that acute estrogen depletion alters within minutes auditory processing in male European starlings. These effects are confined to very specific but large areas of the auditory cortex. They are also specifically lateralized to the left hemisphere. Interestingly, the modulation of auditory responses by estrogens was much larger (both in amplitude and in topography) in March than in December or May/June. This effect was presumably independent from changes in circulating testosterone concentrations since levels of the steroid were controlled by subcutaneous implants, thus suggesting actions related to other aspects of the seasonal cycle or photoperiodic manipulations. Finally, we also show that estrogen production specifically modulates selectivity for behaviorally relevant vocalizations in a specific part of the caudomedial nidopallium. These findings confirm and extend previous conclusions that had been obtained by electrophysiological techniques. This approach provides a new very powerful tool to investigate auditory responsiveness in songbirds and its fast modulation by sex steroids. [less ▲]

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See detailTestosterone-induced neuroendocrine changes in the medial preoptic area precede song activation and plasticity in song control nuclei of female canaries
Shevchouk, Olesya ULiege; Ghorbanpoor, Samar; Ball, Gregory F et al

in European Journal of Neuroscience (2017), 45(7), 886-900

Testosterone plays a key role in the control of seasonal changes in singing behavior and its underlying neural circuitry. After administration of exogenous testosterone, song quality and song control ... [more ▼]

Testosterone plays a key role in the control of seasonal changes in singing behavior and its underlying neural circuitry. After administration of exogenous testosterone, song quality and song control nuclei volumes change over the course of weeks, but song rate increases within days. The medial preoptic nucleus (POM) controls sexual motivation and testosterone action in POM increases sexually motivated singing. Here, we investigated the time course of testosterone action in the song control nuclei and POM, at the gross anatomical and cellular level. Photosensitive female canaries were injected with BrdU to label newborn neurons. One day later they were transferred to a long day photoperiod and implanted with testosterone-filled or empty implants. Brains and blood were collected 1, 2, 9 or 21 days later. Testosterone increased POM volume within one day, whereas the volume of song control nuclei increased significantly only on day 21 even if a trend was already observed for HVC on day 9. The density of newborn neurons in HVC, labeled by Bromodeoxyuridine (BrdU) and doublecortin, was increased by testosterone on days 9 and 21 although a trend was already detectable on day 2. In POM testosterone increased the number and size of aromatase-immunoreactive neurons already after one day. This rapid action of testosterone in POM supports its proposed role in controlling singing motivation. Although testosterone increased the number of newborn neurons in HVC rapidly (9, possibly 2 days), it is unlikely that these new neurons affect singing behavior before they mature and integrate into functional circuits. [less ▲]

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See detailA dynamic, sex-specific expression pattern of genes regulating thyroid hormone action in the developing zebra finch song control system
Raymaekers, S.R.; Verbeure, W.; Ter Haar, S.M. et al

in General and Comparative Endocrinology (2017), 240

The zebra finch (Taeniopygia guttata) song control system consists of several series of interconnected brain nuclei that undergo marked changes during ontogeny and sexual development, making it an excel ... [more ▼]

The zebra finch (Taeniopygia guttata) song control system consists of several series of interconnected brain nuclei that undergo marked changes during ontogeny and sexual development, making it an excel- lent model to study developmental neuroplasticity. Despite the demonstrated influence of hormones such as sex steroids on this phenomenon, thyroid hormones (THs) – an important factor in neural devel- opment and maturation – have not been studied in this regard. We used in situ hybridization to compare the expression of TH transporters, deiodinases and receptors between both sexes during all phases of song development in male zebra finch. Comparisons were made in four song control nuclei: Area X, the lateral magnocellular nucleus of the anterior nidopallium (LMAN), HVC (used as proper name) and the robust nucleus of the arcopallium (RA). Most genes regulating TH action are expressed in these four nuclei at early stages of development. However, while general expression levels decrease with age, the activating enzyme deiodinase type 2 remains highly expressed in Area X, HVC and RA in males, but not in females, until 90days post-hatch (dph), which marks the end of sensorimotor learning. Furthermore, the L-type amino acid transporter 1 and TH receptor beta show elevated expression in male HVC and RA respectively compared to surrounding tissue until adulthood. Differences compared to sur- rounding tissue and between sexes for the other TH regulators were minor. These developmental changes are accompanied by a strong local increase in vascularization in the male RA between 20 and 30 dph but not in Area X or HVC. Our results suggest that local regulation of TH signaling is an important factor in the development of the song control nuclei during the song learning phase and that TH activation by DIO2 is a key player in this process. [less ▲]

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See detailPreoptic glutamate and estradiol release during male sexual behavior
de Bournonville, Catherine ULiege; de Bournonville, Marie-Pierre ULiege; 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 detailSeasonal changes and steroid control of perineuronal nets in the song control system
Cornez, Gilles ULiege; Shevchouk, Olesya ULiege; Madison, Farrah et al

Conference (2016, October 14)

Perineuronal nets (PNNs) are aggregations of extracellular matrix components surrounding the soma of some neurons, mainly GABAergic interneurons expressing the calcium binding protein parvalbumin (PV ... [more ▼]

Perineuronal nets (PNNs) are aggregations of extracellular matrix components surrounding the soma of some neurons, mainly GABAergic interneurons expressing the calcium binding protein parvalbumin (PV+). In mammals, the development of PNNs limits synaptogenesis around PV+ neurons and PNNs have been validated as a marker characterizing the end of critical periods for some types of learning. In oscines, song learning is limited to critical periods either during ontogeny in close-ended learners such as zebra finches or during specific phases of the annual cycle in open-ended learners such as canaries or starlings. In zebra finches, PNN expression increases when the song crystalizes and this increase is markedly inhibited if juveniles are deprived from a tutor, which is known to delay the closure of the critical period for song learning. Nothing is known however about a possible role of PNNs in adult seasonal plasticity of open-ended learners. We compared PNNs expression and their colocalization with PV+ neurons in photosensitive, photostimulated, and photorefractory starlings. Although this treatment affected as expected the testes volumes, testosterone concentrations and volumes of song control nuclei, it did not markedly change the expression of PNNs or PV+ neurons in song control or auditory nuclei. In a second experiment, brains of female canaries implanted with testosterone for 1, 2, 9, or 21 days displayed an increase of the total numbers of PV+ neurons and PNNs in HVC, the total number of PNNs in nucleus robustusarcopallialis (RA), the density of PNNs in Area X and the %PV+ neurons surrounded by PNNs in RA and Area X. Interestingly the density of PNNs in song control nuclei progressively decreases from zebra finches to canaries to starlings in parallel with the increased song plasticity in these species supporting the notion that PNNs may limit brain and thus song plasticity in a species-typical manner. [less ▲]

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See detailAromatase inhibition rapidly affects in a reversible manner distinct features of birdsong
Alward, Beau A.; de Bournonville, Catherine; Chan, Trevor T. et al

in Scientific Reports (2016)

Recent evidence has implicated steroid hormones, specifically estrogens, in the rapid modulation of cognitive processes. Songbirds have been a useful model system in the study of complex cognitive ... [more ▼]

Recent evidence has implicated steroid hormones, specifically estrogens, in the rapid modulation of cognitive processes. Songbirds have been a useful model system in the study of complex cognitive processes including birdsong, a naturally learned vocal behavior regulated by a discrete steroid-sensitive telencephalic circuitry. Singing behavior is known to be regulated by long-term actions of estrogens but rapid steroid modulation of this behavior has never been examined. We investigated if acute actions of estrogens regulate birdsong in canaries (Serinus canaria). In the morning, male canaries sing within minutes after light onset. Birds were injected with fadrozole, a potent aromatase inhibitor, or vehicle within 2-5 minutes after lights on to implement a within-subjects experimental design. This single injection of fadrozole reduced the motivation to sing as well as song acoustic stereotypy, a measure of consistency over song renditions, on the same day. By the next day, however, all song measures that were affected had returned to baseline. This study indicates that estrogens also act in a rapid fashion to regulate two distinct features of song, a learned vocal behavior. [less ▲]

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See detailEndocrine and social regulation of adult neurogenesis in songbirds.
Balthazart, Jacques ULiege; Ball, Gregory F.

in Frontiers in neuroendocrinology (2016)

The identification of pronounced seasonal changes in the volume of avian song control nuclei stimulated the discovery of adult neurogenesis in songbirds as well as renewed studies in mammals including ... [more ▼]

The identification of pronounced seasonal changes in the volume of avian song control nuclei stimulated the discovery of adult neurogenesis in songbirds as well as renewed studies in mammals including humans. Neurogenesis in songbirds is modulated by testosterone and other factors such as photoperiod, singing activity and social environment. Adult neurogenesis has been widely studied by labeling, with tritiated thymidine or its analog BrdU, cells duplicating their DNA in anticipation of their last mitotic division and following their fate as new neurons. New methods based on endogenous markers of cell cycling or of various stages of neuronal life have allowed for additional progress. In particular immunocytochemical visualization of the microtubule-associated protein doublecortin has provided an integrated view of neuronal replacement in the song control nucleus HVC. Multiple questions remain however concerning the specific steps in the neuronal life cycle that are modulated by various factors and the underlying cellular mechanisms. [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 ULiege; Ball, Gregory et al

in Hormones and Behavior (2016), 83

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See detailPleiotropic Control by Testosterone of a Learned Vocal Behavior and Its Underlying Neuroplasticity(1,2,3).
Alward, Beau A.; Madison, Farrah N.; Parker, Shannon E. et al

in eNeuro (2016), 3(1),

Steroid hormones coordinate multiple aspects of behavior and physiology. The same hormone often regulates different aspects of a single behavior and its underlying neuroplasticity. This pleiotropic ... [more ▼]

Steroid hormones coordinate multiple aspects of behavior and physiology. The same hormone often regulates different aspects of a single behavior and its underlying neuroplasticity. This pleiotropic regulation of behavior and physiology is not well understood. Here, we investigated the orchestration by testosterone (T) of birdsong and its neural substrate, the song control system. Male canaries were castrated and received stereotaxic implants filled with T in select brain areas. Implanting T solely in the medial preoptic nucleus (POM) increased the motivation to sing, but did not enhance aspects of song quality such as acoustic structure and stereotypy. In birds implanted with T solely in HVC (proper name), a key sensorimotor region of the song control system, little or no song was observed, similar to castrates that received no T implants of any sort. However, implanting T in HVC and POM simultaneously rescued all measures of song quality. Song amplitude, though, was still lower than what was observed in birds receiving peripheral T treatment. T in POM enhanced HVC volume bilaterally, likely due to activity-dependent changes resulting from an enhanced song rate. T directly in HVC, without increasing song rate, enhanced HVC volume on the ipsilateral side only. T in HVC enhanced the incorporation and recruitment of new neurons into this nucleus, while singing activity can independently influence the incorporation of new neurons into HVC. These results have broad implications for how steroid hormones integrate across different brain regions to coordinate complex social behaviors. [less ▲]

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See detailSex differences in partner preferences in humans and animals.
Balthazart, Jacques ULiege

in Philosophical transactions of the Royal Society of London. Series B, Biological sciences (2016), 371(1688),

A large number of morphological, physiological and behavioural traits are differentially expressed by males and females in all vertebrates including humans. These sex differences, sometimes, reflect the ... [more ▼]

A large number of morphological, physiological and behavioural traits are differentially expressed by males and females in all vertebrates including humans. These sex differences, sometimes, reflect the different hormonal environment of the adults, but they often remain present after subjects of both sexes are placed in the same endocrine conditions following gonadectomy associated or not with hormonal replacement therapy. They are then the result of combined influences of organizational actions of sex steroids acting early during development, or genetic differences between the sexes, or epigenetic mechanisms differentially affecting males and females. Sexual partner preference is a sexually differentiated behavioural trait that is clearly controlled in animals by the same type of mechanisms. This is also probably true in humans, even if critical experiments that would be needed to obtain scientific proof of this assertion are often impossible for pragmatic or ethical reasons. Clinical, epidemiological and correlative studies provide, however, converging evidence strongly suggesting, if not demonstrating, that endocrine, genetic and epigenetic mechanisms acting during the pre- or perinatal life control human sexual orientation, i.e. homosexuality versus heterosexuality. Whether they interact with postnatal psychosexual influences remains, however, unclear at present. [less ▲]

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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 ULiege; 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 detailAnatomically discrete sex differences in neuroplasticity in zebra finches as reflected by perineuronal nets.
Cornez, Gilles ULiege; Ter Haar, Sita M.; Cornil, Charlotte ULiege 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 detailThe dual action of estrogen hypothesis
Cornil, Charlotte ULiege; Ball, Gregory F.; Balthazart, Jacques ULiege

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 ULiege; 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 detailMate selection, Sexual orientation and Pair bonding
Balthazart, Jacques ULiege; Young, Larry J.

in Plant, Tony M.; Zelenik, Anthony J. (Eds.) Knobil and Neill's Physiology of Reproduction (2015)

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