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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 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 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 detailc-fos down-regulation inhibits testosterone-dependent male sexual behavior and the associated learning
Niessen, Neville-Andrew ULiege; Balthazart, Jacques ULiege; 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 ULiege; Balthazart, Jacques ULiege; 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 ULiege; 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 ULiege; 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 ULiege; 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 ULiege; Charlier, Thierry ULiege; Cornil, Charlotte ULiege 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 ULiege; Ball, Gregory; Balthazart, Jacques ULiege

Poster (2011)

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See detailEffects of social experience on subsequent sexual performance in naïve male Japanese quail (Coturnix japonica)
Cornil, Charlotte ULiege; 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 ULiege; Cornil, Charlotte ULiege; 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 ULiege; Charlier, Thierry ULiege; Barker, Jennifer ULiege 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 ULiege; Cornil, Charlotte ULiege 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 ULiege 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 ULiege; Baillien, Michelle; Cornil, Charlotte ULiege 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 ULiege; Baillien, Michelle; Charlier, Thierry ULiege 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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