Publications of Jacques Balthazart
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See detailSexual versus individual differentiation: the controversial role of avian maternal hormones
Carere, C.; Balthazart, Jacques ULg

in Trends in Endocrinology and Metabolism (2007), 18(2), 73-80

Avian embryos are exposed not only to endogenous sex steroids, which are produced by their gonads and have a key role in sexual differentiation, but also to maternal steroids transferred into the egg yolk ... [more ▼]

Avian embryos are exposed not only to endogenous sex steroids, which are produced by their gonads and have a key role in sexual differentiation, but also to maternal steroids transferred into the egg yolk, which can modulate the development of individual differences in behavior. Studies of maternal hormones have primarily focused on ultimate questions (evolutionary trade-offs, functional significance), whereas proximate mechanistic questions have been largely ignored. A central problem that must be addressed is how exposure to maternal hormones affects the individual phenotype without interfering with sexual differentiation. Separate effects could result from the action of different hormones, at different doses or at different times, on different targets. [less ▲]

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See detailNeuroanatomical specificity of sex differences in expression of aromatase mRNA in the quail brain
Voigt, C.; Ball, G. F.; Balthazart, Jacques ULg

in Journal of Chemical Neuroanatomy (2007), 33(2), 75-86

In birds and mammals, aromatase activity in the preoptic-hypothalamic region (HPOA) is usually higher in males than in females. It is, however, not known whether the enzymatic sex difference reflects the ... [more ▼]

In birds and mammals, aromatase activity in the preoptic-hypothalamic region (HPOA) is usually higher in males than in females. It is, however, not known whether the enzymatic sex difference reflects the differential activation of aromatase transcription or some other control mechanism. Although sex differences in aromatase activity are clearly documented in the HPOA of Japanese quail (Coturnix japonica), only minimal or even no differences at all were observed in the number of aromatase-immunoreactive (ARO-ir) cells in the medial preoptic nucleus (POM) and in the medial part of the bed nucleus striae terminalis (BSTM). We investigated by in situ hybridization the distribution and possible sex differences in aromatase mRNA expression in the brain of sexually active adult quail. The distribution of aromatase mRNA matched very closely the results of previous immunocytochemical studies with the densest signal being observed in the POM, BSTM and in the mediobasal hypothalamus (MBH). Additional weaker signals were detected in the rostral forebrain, arcopallium and mesencephalic regions. No sex difference in the optical density of the hybridization signal could be found in the POM and MBH but the area covered by mRNA was larger in males than in females, indicating a higher overall expression in males. In contrast, in the BSTM, similar areas were covered by the aromatase expression in both sexes but the density of the signal was higher in females than in males. The physiological control of aromatase is thus neuroanatomically specific and with regard to sex differences, these controls are at least partially different if one compares the level of transcription, translation and activity of the enzyme. These results also indirectly suggest that the sex difference in aromatase enzyme activity that is present in the quail HPOA largely results from differentiated controls of enzymatic activity rather than differences in enzyme concentration. (c) 2007 Elsevier B.V. All rights reserved. [less ▲]

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See detailSex differences in projections from preoptic area aromatase cells to the periaqueductal gray in Japanese quail
Carere, C.; Ball, G. F.; Balthazart, Jacques ULg

in Journal of Comparative Neurology (2007), 500(5), 894-907

In many vertebrate species the medial preoptic area projects to a premotor nucleus, the periaqueductal central gray (PAG). This connection plays an important role in the control of reproductive behavior ... [more ▼]

In many vertebrate species the medial preoptic area projects to a premotor nucleus, the periaqueductal central gray (PAG). This connection plays an important role in the control of reproductive behavior. In male Japanese quail (Coturnix japonica) specifically, the medial preoptic nucleus (POM), where various types of sensory inputs converge, is a critical site for the activational action of testosterone on male sexual behavior. To activate male copulatory behavior, testosterone must be aromatized to estradiol within the POM and aromatase-immunoreactive cells in the POM are the main source of projections to the PAG. The POM-PAG connection is thus an important functional circuit integrating the sensory with premotor components of sexual behavior. Contrary to what is observed in males, testosterone does not activate male-typical copulatory behavior in females and we investigated here via retrograde tracing methods whether this behavioral sexual difference is associated with a sex difference in connectivity between POM and PAG. Fluorescent microspheres were injected in the PAG of male and female quail and retrogradely labeled fluorescent cells counted in four fields of the POM in sections that had been immunolabeled for aromatase. Males had more aromatase-immunoreactive neurons projecting to the PAG than females and this difference was most prominent in the caudolateral part of the nucleus that has been specifically implicated in the control of male copulatory behavior. These data therefore support the hypothesis that sex differences in POM-PAG connectivity are causally linked to the sex difference in the behavioral response to testosterone. [less ▲]

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See detailFunctional significance of the rapid regulation of brain estrogen action: Where do the estrogens come from?
Cornil, Charlotte ULg; Ball, G. F.; Balthazart, Jacques ULg

in Brain Research (2006), 1126

Estrogens exert a wide variety of actions on reproductive and non-reproductive functions. These effects are mediated by slow and long lasting genomic as well as rapid and transient non-genomic mechanisms ... [more ▼]

Estrogens exert a wide variety of actions on reproductive and non-reproductive functions. These effects are mediated by slow and long lasting genomic as well as rapid and transient non-genomic mechanisms. Besides the host of studies demonstrating the role of genomic actions at the physiological and behavioral level, mounting evidence highlights the functional significance of non-genomic effects. However, the source of the rapid changes in estrogen availability that are necessary to sustain their fast actions is rarely questioned. For example, the rise of plasma estrogens at pro-estrus that represents one of the fastest documented changes in plasma estrogen concentration appears too slow to explain these actions. Alternatively, estrogen can be synthesized in the brain by the enzyme aromatase providing a source of locally high concentrations of the steroid. Furthermore, recent studies demonstrate that brain aromatase can be rapidly modulated by afferent inputs, including glutamatergic afferents. A role for rapid changes in estrogen production in the central nervous system is supported by experiments showing that acute aromatase inhibition affects nociception as well as male sexual behavior and that preoptic aromatase activity is rapidly (within min) modulated following mating. Such mechanisms thus fulfill the gap existing between the fast actions of estrogen and their mode of production and open new avenues for the understanding of estrogenic effects on the brain. (c) 2006 Elsevier B.V. All rights reserved. [less ▲]

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See detailSocial context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria)
Boseret, Géraldine ULg; Carere, C.; Ball, G. F. et al

in Journal of Neurobiology (2006), 66(10), 1044-1060

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See detailSimultaneous pituitary-gonadal recrudescence in two Corsican populations of male blue tits with asynchronous breeding dates
Caro, S. P.; Lambrechts, M. M.; Chastel, O. et al

in Hormones & Behavior (2006), 50(3), 347-360

Animal populations living in geographically variable environments respond to different selection pressures. The adaptive character of the responses to environmental information determines the degree of ... [more ▼]

Animal populations living in geographically variable environments respond to different selection pressures. The adaptive character of the responses to environmental information determines the degree of synchrony of the breeding period with local optimal conditions. An example is provided by two populations of Mediterranean blue tits (Parus caeruleus) in Corsica, breeding in different habitats, with a 1-month difference in the onset of egg laying. This difference in the onset of lay is supposed to be adaptive because, although chicks from both populations are raised mostly on caterpillars, the timing of the appearance of caterpillars is earlier for populations of tits associated with deciduous oak trees than those associated with evergreen oak trees. Here, we show that, despite the difference in the timing of egg laying, males from these two populations start seasonal hypothalamo-hypophysial-testicular development at approximately the same time, in late winter. Specifically, the vernal recrudescence of brain GnRH-I perikarya and fibers, testes volume and song activity began around the same dates and proceeded at the same pace in late winter in both populations. Plasma testosterone and LH levels displayed seasonal variations that were shifted by less than 2 weeks compared to the 1-month difference in egg laying periods. We hypothesize that the strong selection pressures on these two populations to adapt the timing of their breeding seasons to their local environment may have acted mostly on the female egg laying dates, and not so much on the initiation and rate of seasonal recrudescence of the hypothalamo-hypophysial-testicular activity in males. (c) 2006 Elsevier Inc. All rights reserved. [less ▲]

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See detailRapid effects of estrogens on sexual appetite and consummation in quail
Balthazart, Jacques ULg

in Journal of Ornithology (2006, August), 147(5, Suppl. 1), 56

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See detailThe proximate basis of adaptive micro-geographic variation in reproductive phenology in male and female Blue Tits
Caro, S.; Balthazart, Jacques ULg; Lambrechts, M.

in Journal of Ornithology (2006, August), 147(5, Suppl. 1), 47-48

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See detailIn vivo MR imaging of the seasonal volumetric and functional plasticity of song control nuclei in relation to song output in a female songbird
Van Meir, V.; Pavlova, D.; Verhoye, M. et al

in Neuroimage (2006), 31(3), 981-992

In temperate zone songbird species, seasonal plasticity in the morphological and functional state of brain regions involved in song production occurs in association with seasonal changes in song output ... [more ▼]

In temperate zone songbird species, seasonal plasticity in the morphological and functional state of brain regions involved in song production occurs in association with seasonal changes in song output. Following MHCl2-injections in HVC (used as proper name) of female starlings, in vivo tract-tracing by Manganese Enhanced-Magnetic Resonance Imaging (ME-MRI) provided repeated measures of the volume of two HVC targets, the nucleus robustus arcopallii (RA) and area X, along with measures of the activity of the caudal motor pathway and rostral basal-ganglia pathway that control singing. Mn2+- labeling (volume labeled and signal intensity) of both nuclei was dramatically reduced in July (post-breeding season) when birds did not sing, compared to March (breeding season) when birds produced song. Seasonal changes in telencephalon volume did not exceed 4% and were not significant but were surprisingly correlated with individual measures of song rate and song bout length. Although individual song rates were variable in March, all MnCl2-injections led to a reliable labeling of area X and RA. In July, delineation of area X was only possible in two birds and RA could be delineated in 50% of the population; its volume had decreased by 46% as compared to March. The birds in which RA could be delineated in July had in March a higher activity of the HVC to area X projection as reflected by the total amount of Mn2+ accumulated in area X, which suggests unexpected relationships between the two types of HVC projection neurons. (c) 2006 Elsevier Inc. All rights reserved. [less ▲]

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See detailIs brain estradiol a hormone or a neurotransmitter?
Balthazart, Jacques ULg; Ball, G. F.

in Trends in Neurosciences (2006), 29(5), 241-249

Mounting evidence indicates that, besides their well-known hormonal mode of action at the genetic level, estrogens such as 17 beta-estradiol also influence brain function by direct effects on neuronal ... [more ▼]

Mounting evidence indicates that, besides their well-known hormonal mode of action at the genetic level, estrogens such as 17 beta-estradiol also influence brain function by direct effects on neuronal membranes. Experimentally induced rapid changes in estradiol bioavailability in the brain have been shown to alter the expression of male sexual behavior significantly within minutes - probably too quickly to be accounted for by conventional genetic mechanisms. In parallel, recent studies indicate that aromatase, the enzyme that converts testosterone to estradiol in the brain, is expressed in presynaptic terminals and modulated within minutes by Ca2+-dependent phosphorylation. In this article, we develop the hypothesis that brain estrogens display many, if not all, functional characteristics of neuromodulators or even neurotransmitters. [less ▲]

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See detailNeuroanatomical specificity in the expression of the immediate early gene c-fos following expression of appetitive and consummatory male sexual behaviour in Japanese quail
Taziaux, Mélanie ULg; Cornil, Charlotte ULg; Dejace, C. et al

in European Journal of Neuroscience (2006), 23(7), 1869-1887

We investigated the neural sites related to the occurrence of appetitive (ASB) and consummatory (CSB) aspects of male sexual behaviour in Japanese quail. Castrated males treated with testosterone were ... [more ▼]

We investigated the neural sites related to the occurrence of appetitive (ASB) and consummatory (CSB) aspects of male sexual behaviour in Japanese quail. Castrated males treated with testosterone were exposed for 5 min to one of four experimental conditions: (i) free interaction with a female (CSB group); (ii) expression of rhythmic cloacal sphincter movements in response to the visual presentation of a female (ASB-F group); (iii) or a male (ASB-M group), and (iv) handling as a control manipulation. Brains were collected 90 min after the start of behavioural tests and stained by immunocytochemistry for the FOS protein. An increase in FOS expression was observed throughout the rostro-caudal extent of the medial preoptic nucleus (POM) in CSB males, whereas the view of a female (ASB-F) induced an increased FOS expression in the rostral POM only. In the CSB group, there was also an increase in FOS expression in the bed nucleus striae terminalis, and both the CSB and ASB-F groups exhibited increased FOS expression in aspects of the ventro-lateral thalamus (VLT) related to visual processing. Moreover, both the CSB and ASB-M groups showed increased FOS expression in the lateral septum. These data provide additional support to the idea that there is a partial anatomical dissociation between structures involved in the control of both aspects of male sexual behaviour and independently provide data consistent with a previous lesion study that indicated that the rostral and caudal POM differentially control the expression of ASB and CSB in quail. [less ▲]

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See detailAlpha-fetoprotein protects the developing female mouse brain from masculinization and defeminization by estrogens
Bakker, Julie ULg; De Mees, C.; Douhard, Quentin ULg et al

in Nature Neuroscience (2006), 9(2), 220-226

Two clearly opposing views exist on the function of alpha-fetoprotein (AFP), a fetal plasma protein that binds estrogens with high affinity, in the sexual differentiation of the rodent brain. AFP has been ... [more ▼]

Two clearly opposing views exist on the function of alpha-fetoprotein (AFP), a fetal plasma protein that binds estrogens with high affinity, in the sexual differentiation of the rodent brain. AFP has been proposed to either prevent the entry of estrogens or to actively transport estrogens into the developing female brain. The availability of Afp mutant mice (Afp(-/-)) now finally allows us to resolve this longstanding controversy concerning the role of AFP in brain sexual differentiation, and thus to determine whether prenatal estrogens contribute to the development of the female brain. Here we show that the brain and behavior of female Afp(-/-) mice were masculinized and defeminized. However, when estrogen production was blocked by embryonic treatment with the aromatase inhibitor 1,4,6-androstatriene-3,17-dione, the feminine phenotype of these mice was rescued. These results clearly demonstrate that prenatal estrogens masculinize and defeminize the brain and that AFP protects the female brain from these effects of estrogens. [less ▲]

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See detailEstradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain
Cornil, Charlotte ULg; Dalla, C.; Papadopoulou-Daifoti, Z. et al

in Behavioural Brain Research (2006), 166(1), 110-123

Steroids are generally viewed as transcription factors binding to intracellular receptors and activating gene transcription. Rapid cellular effects mediated via non-genomic mechanisms have however been ... [more ▼]

Steroids are generally viewed as transcription factors binding to intracellular receptors and activating gene transcription. Rapid cellular effects mediated via non-genomic mechanisms have however been identified and one report showed that injections of estradiol rapidly stimulate chemoinvestigation and mounting behavior in castrated male rats. It is not known whether such effects take place in other species and what are the cellular underlying mechanisms. We show here that a single injection of estradiol (500 wg/kg) rapidly and transiently activates copulatory behavior in castrated male quail pre-treated with a dose of testosterone behaviorally ineffective by itself. The maximal behavioral effect was observed after 15 min. In a second experiment, the brain of all subjects was immediately collected after behavioral tests performed 15 min after injection. The preoptic area-hypothalamus (HPOA), hindbrain, telencephalon and cerebellum were isolated and monoamines measured by HPLC-ED. Estradiol increased levels of the serotonin metabolite 5-hydroxyindoleacetic acid (5-HIAA) and 5-HIAA/serotonin ratios in the telencephalon and hindbrain independently of whether animals had mated or not. Estradiol also affected these measures in HPOA and cerebellum but this effect was correlated with the level of sexual activity so that significant effects of the treatment only appeared when sexual activity was used as a covariate. Interactions between estradiol effects and sexual activity were also observed for dopamine in the HPOA and for serotonin in the hindbrain and cerebellum. Together, these data demonstrate that a single estradiol injection rapidly activates male sexual behavior in quail and that this behavioral effect is correlated with changes in monoaminergic activity. (c) 2005 Elsevier B.V. All rights reserved. [less ▲]

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See detailAndrogen metabolism and the activation of male sexual behavior: It's more complicated than you think!
Ball, G. F.; Balthazart, Jacques ULg

in Hormones & Behavior (2006), 49(1), 1-3

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See detailRapid control of brain aromatase activity by glutamatergic inputs
Balthazart, Jacques ULg; Baillien, M.; Ball, G. F.

in Endocrinology (2006), 147(1), 359-366

Estrogens derived from the neural aromatization of testosterone play a key role in the activation of male sexual behavior in many vertebrates and have now been recognized to have rapid membrane effects on ... [more ▼]

Estrogens derived from the neural aromatization of testosterone play a key role in the activation of male sexual behavior in many vertebrates and have now been recognized to have rapid membrane effects on brain function. Such changes in aromatase activity and hence in local estrogen concentrations could rapidly modulate behavioral responses. We show here that there is a very rapid (within minutes) decrease in aromatase activity in quail hypothalamic explants exposed to treatments affecting intracellular Ca2+ concentrations, such as the addition of glutamate agonists (kainate, alpha-amino-3-hydroxymethyl-4-isoxazole propionic acid, and, to a much lesser extent, N-methyl-D-aspartate), but not of gamma-aminobutyric acid. The kainate effects, which reduce aromatase activity by 25-50%, are observed within 5 min, are completely blocked in explants exposed to specific kainate antagonists (6-cyano-7-nitroquinoxaline-2,3-dione disodium or 1,2,3,4-tetrahydro-6-nitro-2,3-dioxo-benzo[f]quinoxaline-7-sulfonamide disodium), and are also rapidly reversible when effectors are washed out. Together, these data support the idea that the synthesis of estrogen can be rapidly regulated in the brain, thus producing rapid changes in local estrogen bioavailability that could rapidly modify brain function with a time course similar to what has previously been described for neurotransmitters and neuromodulators. [less ▲]

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See detailAttraction thresholds and sex discrimination of urinary odorants in male and female aromatase knockout (ArKO) mice
Pierman, S.; Douhard, Quentin ULg; Balthazart, Jacques ULg et al

in Hormones & Behavior (2006), 49(1), 96-104

We previously found that both male and female aromatase knockout (ArKO) mice, which cannot synthesize estrogens due to a targeted mutation of the aromatase gene, showed less investigation of volatile body ... [more ▼]

We previously found that both male and female aromatase knockout (ArKO) mice, which cannot synthesize estrogens due to a targeted mutation of the aromatase gene, showed less investigation of volatile body odors from anesthetized conspecifics of both sexes in Y-maze tests. We now ask whether ArKO mice are in fact capable of discriminating between and/or responding to volatile odors. Using habituation/dishabituation tests, we found that gonadectomized ArKO and wild-type (WT) mice of both sexes, which were tested without any sex hormone replacement, reliably distinguished between undiluted volatile urinary odors of either adult males or estrous females versus deionized water as well as between these two urinary odors themselves. However, ArKO mice of both sexes were less motivated than WT controls to investigate same-sex odors when they were presented last in the sequence of stimuli. In a second experiment, we compared the ability of ArKO and WT mice to respond to decreasing concentrations of either male or female urinary odors. We found a clear-cut sex difference in urinary odor attraction thresholds among WT mice: WT males failed to respond to urine dilutions higher than 1:20 by volume, whereas WT females continued to respond to urine dilutions up to 1:80. Male ArKO mice resembled WT females in their ability to respond to lower concentrations of urinary odors, raising the possibility that the observed sex difference among WT mice in urine attraction thresholds results from the perinatal actions of estrogen in the male nervous system. Female ArKO mice failed to show significant dishabituation responses to two (1:20 and 1:80) dilutions of female urine, perhaps, again, because of a reduced motivation to investigate less salient, same-sex urinary odors. Previously observed deficits in the preference of ArKO male and female mice to approach volatile body odors from conspecifics of either sex cannot be attributed to an inability of ArKO subjects to discriminate these odors according to sex but instead may reflect a deficient motivation to approach same-sex odors, especially when their concentration is low. [less ▲]

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See detailRapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail
Cornil, Charlotte ULg; Taziaux, Mélanie ULg; Baillien, M. et al

in Hormones & Behavior (2006), 49(1), 45-67

Non-genomic effects of steroid hormones on cell physiology have been reported in the brain. However, relatively little is known about the behavioral significance of these actions. Male sexual behavior is ... [more ▼]

Non-genomic effects of steroid hormones on cell physiology have been reported in the brain. However, relatively little is known about the behavioral significance of these actions. Male sexual behavior is activated by testosterone partly through its conversion to estradiol via the enzyme aromatase in the preoptic area (POA). Brain aromatase activity (AA) changes rapidly which might in turn be important for the rapid regulation of behavior. Here, acute effects of Vorozole (TM), an aromatase inhibitor, injected IP at different doses and times before testing (between 15 and 60 min), were assessed on male sexual behavior in quail. To limit the risk of committing both types of statistical errors (I and II), data of all experiments were entered into a meta-analysis. Vorozole (TM) significantly inhibited mount attempts (P < 0.05, size effect [g] = 0.527) and increased the latency to first copulation (P < 0.05, g = 0.251). The treatment had no effect on the other measures of copulatory behavior. Vorozole (TM) also inhibited appetitive sexual behavior measured by the social proximity response (P < 0.05, g = 0.534) or rhythmic cloacal sphincter movements (P < 0.001, g = 0.408). Behavioral inhibitions always reached a maximum at 30 min. Another aromatase inhibitor, androstatrienedione, induced a similar rapid inhibition of sphincter movements. Radioenzyme assays demonstrated that within 30 min Vorozole (TM) had reached the POA and completely blocked AA measured in homogenates. When added to the extracellular milieu, Vorozole (TM) also blocked within 5 min the AA in POA explants maintained in vitro. Together, these data demonstrate that aromatase inhibition rapidly decreases both consummatory and appetitive aspects of male sexual behavior. (c) 2005 Elsevier Inc. All rights reserved. [less ▲]

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See detailPlasticity in the expression of the steroid receptor coactivator 1 in the Japanese quail brain: effect of sex, testosterone, stress and time of the day.
Charlier, Thierry ULg; Ball, G. F.; Balthazart, Jacques ULg

in Neuroscience (2006), 140(4), 1381-94

Analysis of nuclear receptor action on the eukaryotic genome highlights the importance of coactivators on gene transcription. The steroid receptor coactivator-1 in particular is the focus of an intense ... [more ▼]

Analysis of nuclear receptor action on the eukaryotic genome highlights the importance of coactivators on gene transcription. The steroid receptor coactivator-1 in particular is the focus of an intense research and physiological or behavioral studies have confirmed that it plays a major role in the modulation of steroid and thyroid receptors activity. However, little is known about the regulation of steroid receptor coactivator-1 expression the brain. The goal of this study was to determine the potential factors modulating steroid receptor coactivator-1 synthesis in Japanese quail by quantification of its mRNA with real time quantitative polymerase chain reaction and of the corresponding protein via Western blotting. Contrary to previously published results from our laboratory [Charlier TD, Lakaye B, Ball GF, Balthazart J (2002) The steroid receptor coactivator SRC-1 exhibits high expression in steroid-sensitive brain areas regulating reproductive behaviors in the quail brain. Neuroendocrinology 76:297-315], we found here that sexually mature females had a higher concentration of steroid receptor coactivator-1 in the preoptic area/hypothalamus compared with males. Steroid receptor coactivator-1 expression in the male preoptic area/hypothalamus was up-regulated by testosterone and tended to be decreased by stress. We also identified a significant correlation between the time of the day and the expression of the coactivator in the optic lobes, hippocampus, telencephalon and hindbrain but the pattern of changes in expression as a function of the time of the day varied from one brain area to another. Together, these data support the idea that steroid receptor coactivator-1 is not constitutively expressed but rather is finely regulated by steroids, stress and possibly other unidentified factors. [less ▲]

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