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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 ULg; Ghorbanpoor, Samar; Ball, Gregory F et al

in European Journal of Neuroscience (in press)

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 detailMultiple markers of HVC neurogenesis in the canary
Shevchouk, Olesya ULg; Ball, G.F.; Cornil, Charlotte ULg et al

in PLoS ONE (in press)

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 detailPerineuronal nets and vocal plasticity in songbirds: a proposed mechanism to explain the difference between closed-ended and open-ended learning
Cornez, Gilles ULg; 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 detailExploring sex differences in the adult zebra finch brain: in vivo diffusion tensor imaging and ex vivo super-resolution track density imaging
Hamaide, J.; De Groof, G.; Van Steenkiste, G. et al

in NeuroImage (2017)

Zebra finches are an excellent model to study the process of vocal learning, a complex socially-learned tool of communication that forms the basis of spoken human language. So far, structural ... [more ▼]

Zebra finches are an excellent model to study the process of vocal learning, a complex socially-learned tool of communication that forms the basis of spoken human language. So far, structural investigation of the zebra finch brain has been performed ex vivo using invasive methods such as histology. These methods are highly specific, however, they strongly interfere with performing whole-brain analyses and exclude longitudinal studies aimed at establishing causal correlations between neuroplastic events and specific behavioral performances. Therefore, the aim of the current study was to implement an in vivo Diffusion Tensor Imaging (DTI) protocol sensitive enough to detect structural sex differences in the adult zebra finch brain. Voxel-wise comparison of male and female DTI parameter maps shows clear differences in several components of the song control system (i.e. Area X surroundings, the high vocal center (HVC) and the lateral magnocellular nucleus of the anterior nidopallium (LMAN)), which corroborate previous findings and are in line with the clear behavioral difference as only males sing. Furthermore, to obtain additional insights into the 3-dimensional organization of the zebra finch brain and clarify findings obtained by the in vivo study, ex vivo DTI data of the male and female brain were acquired as well, using a recently established super-resolution reconstruction (SRR) imaging strategy. Interestingly, the SRR-DTI approach led to a marked reduction in acquisition time without interfering with the (spatial and angular) resolution and SNR which enabled to acquire a data set characterized by a 78μm isotropic resolution including 90 diffusion gradient directions within 44h of scanning time. Based on the reconstructed SRR-DTI maps, whole brain probabilistic Track Density Imaging (TDI) was performed for the purpose of super resolved track density imaging, further pushing the resolution up to 40μm isotropic. The DTI and TDI maps realized atlas-quality anatomical maps that enable a clear delineation of most components of the song control and auditory systems. In conclusion, this study paves the way for longitudinal in vivo and high-resolution ex vivo experiments aimed at disentangling [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 detailRapid Effects of Estrogens on Avian Brain and Social Behavior
Remage-Healey, Luke; Heimovics, Sarah A.; Soma, Kiran K et al

in Pfaff, Donald W; Arnold, Arthur P; Etgen, Anne M (Eds.) et al Hormones, Brain and Behavior (2017)

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See detailAcute regulation of male sexual behavior by brain-derived estrogens
Cornil, Charlotte ULg

Conference (2016, November 15)

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

Poster (2016, November)

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

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

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See detailSeasonal changes and steroid control of perineuronal nets in the song control system
Cornez, Gilles ULg; Shevchouk, Olesya ULg; 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 detailDual action of neuro-estrogens in the regulation of male sexual behavior
Cornil, Charlotte ULg

Conference (2016, October 13)

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See detailThe dual action of neuroestrogens on sexual behavior
Cornil, Charlotte ULg

Conference (2016, August)

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See detailActions of steroids: New Neurotransmitters
Rudolph, L.M.; Cornil, Charlotte ULg; Mittelman-Smith, M.A. et al

in Journal of Neuroscience (2016), 36(45), 11449-11458

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

in Hormones and Behavior (2016), 83

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See detailThe dual action of neuroestrogens on behavior
Cornil, Charlotte ULg

Scientific conference (2015, October 09)

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

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

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

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

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

Conference (2015, June 08)

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

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

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

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

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

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

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

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

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