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See detailMEMBRANE ESTROGEN RECEPTOR ALPHA PARTICIPATES IN THE ORGANIZATION OF THE BRAIN BY PERINATAL ESTROGENS
Cornil, Charlotte ULiege; Khbouz, Badr ULiege; Court, Lucas ULiege et al

Conference (2019, May 21)

Estrogens exert pleiotropic effects on multiple physiological and behavioral responses. Male and female sexual behaviors in rodents constitute some of the best characterized responses activated by ... [more ▼]

Estrogens exert pleiotropic effects on multiple physiological and behavioral responses. Male and female sexual behaviors in rodents constitute some of the best characterized responses activated by estrogens in adulthood and largely depend on estrogen receptor alpha (ERα). Evidence exists that nucleus- and membrane-initiated estrogen signaling cooperate to orchestrate the activation of these behaviors both short- and long-term. However questions remain regarding the mechanism(s) and receptor(s) involved in the early brain programming during development to organize the circuits underlying sexually differentiated endpoints. Taking advantage of a mouse model harboring a mutation of the ERα palmitoylation site which invalidates membrane ER signaling (mERα), this study investigated the role of mERα on the expression of male and female sexual behavior and neuronal populations that differ between sexes. The results revealed no effect of genotype on the expression of female sexual behavior while male sexual behavior was significantly reduced but not impaired in males homozygous for the mutation. Similarly, the number of kisspeptin- (Kp-ir) and calbindin-immunoreactive (Cb-ir) neurons in the anteroventral periventricular nucleus (AVPv) and the sexually-dimorphic nucleus of the preoptic area (SDN-POA) respectively were not different between genotypes in females, while homozygous males showed an increased number of Kp-ir and a decreased number of Cb-ir neurons compared to their wild-type littermates thus leading to an intermediate phenotype between females and wild-type males. Importantly, females treated with estrogens between post-natal day 0 and 5 exhibited the same neurochemical phenotype as their corresponding genotype in males. Together, these data provide evidence that mERα is involved in the perinatal programming of the male brain. [less ▲]

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See detailNEUROESTROGENS AND FEMALE SEXUAL BEHAVIOR
Cornil, Charlotte ULiege

Conference (2019, January 17)

The ovaries are often thought of as the main and only source of estrogens involved in the regulation of female behavior. Estrogens are produced by the aromatization of testosterone. Although this enzyme ... [more ▼]

The ovaries are often thought of as the main and only source of estrogens involved in the regulation of female behavior. Estrogens are produced by the aromatization of testosterone. Although this enzyme is less abundant than in males, this enzyme is expressed and active in the brain of females where it is regulated by similar mechanisms as in males. Early work had shown that estrogens produced in the ventromedial hypothalamus are involved in the regulation of female sexual behavior in musk shrews. Yet the question of the role of central aromatase in general had not received much attention until recently. In this talk, I will first review early work and recent evidence supporting a role for central aromatization in the regulation of physiological and behavioral processes in females. Then I will present recent data from our lab supporting a role for non-ovarian estrogens in the regulation of female sexual behavior in Japanese quail. Together, these data support the notion that in females brain aromatase is not simply a non-functional vestige of evolution and provide support for the importance of locally produced estrogens for brain function in females. [less ▲]

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See detailRole of membrane-initiated effects of estrogens in brain programming
Cornil, Charlotte ULiege

Scientific conference (2019, January 17)

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See detailSite-specific effects of aromatase inhibition on the activation of male sexual behavior in male Japanese quail (Coturnix japonica)
de Bournonville, Marie-Pierre ULiege; Vandries, Laura ULiege; Ball, Gregory et al

in Hormones and Behavior (2019), 108

Aromatization within the medial preoptic nucleus (POM) is essential for the expression of male copulatory behavior in Japanese quail. However, several nuclei within the social behavior network (SBN) also ... [more ▼]

Aromatization within the medial preoptic nucleus (POM) is essential for the expression of male copulatory behavior in Japanese quail. However, several nuclei within the social behavior network (SBN) also express aromatase. Whether aromatase in these loci participates in the behavioral activation is not known. Castrated male Japanese quail were implanted with 2 subcutaneous Silastic capsules filled with crystalline testosterone and with bilateral stereotaxic implants filled with the aromatase inhibitor Vorozole targeting the POM, the bed nucleus of the stria terminalis (BST) or the ventromedial nucleus of the hypothalamus (VMN). Control animals were implanted with testosterone and empty bilateral stereotaxic implants. Starting 2 days after the surgery, subjects were tested for the expression of consummatory sexual behavior (CSB) every other day for a total of 10 tests. They were also tested once for appetitive sexual behavior (ASB) as measured by the rhythmic cloacal sphincter movements displayed in response to the visual presentation of a female. CSB was drastically reduced when the Vorozole implants were localized in the POM, but not in the BST nor in the VMN. Birds with implants in the BST showed a longer latency to show CSB in the first 6 tests than controls, suggesting a role of the BST in the acquisition of the full copulatory ability. ASB was not significantly affected by aromatase blockade in any region. These data confirm the key role played by the POM in the control of male sexual behavior and suggest a minor role for aromatization in the BST or VMN. [less ▲]

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See detailPersonality and gonadal development as sources of individual variation in response to GnRH challenge in female great tits
Caro, Samuel; Cornil, Charlotte ULiege; van Oers, Kees et al

in Proceedings of the Royal Society of London. Series B, Biological Sciences (2019), 286(1902), 20190142

Seasonal timing of reproduction is a key life-history trait, but we know little about the mechanisms underlying individual variation in female endocrine profiles associated with reproduction. In birds ... [more ▼]

Seasonal timing of reproduction is a key life-history trait, but we know little about the mechanisms underlying individual variation in female endocrine profiles associated with reproduction. In birds, 17b-oestradiol is a key repro- ductive hormone that links brain neuroendocrine mechanisms, involved in information processing and decision-making, to downstream mechanisms in the liver, where egg-yolk is produced. Here, we test, using a simulated induction of the reproductive system through a GnRH challenge, whether the ovary of pre-breeding female great tits responds to a brain stimulation by increasing oestradiol. We also assess how this response is modified by individual-specific traits like age, ovarian follicle size and personality, using females from lines artificially selected for divergent levels of explora- tory behaviour. We show that a GnRH injection leads to a rapid increase in circulating concentrations of oestradiol, but responses varied among individ- uals. Females with more developed ovarian follicles showed stronger responses and females from lines selected for fast exploratory behaviour showed stronger increases compared to females from the slow line, indicat- ing a heritable component. This study shows that the response of the ovary to a reproductive stimulation from the brain greatly varies among individ- uals and that this variation can be attributed to several commonly measured individual traits, which sheds light on the mechanisms shaping heritable endocrine phenotypes. [less ▲]

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See detailTestosterone or estradiol when implanted in the medial preoptic nucleus trigger short low-amplitude songs in female canaries
Vandries, Laura ULiege; Ghorbanpoor, Samar; Cornez, Gilles ULiege et al

in eNeuro (2019), 6(2), 0502-182019

In male songbirds, the motivation to sing is largely regulated by testosterone action in the medial preoptic area, whereas testosterone acts on song control nuclei to modulate aspects of song quality ... [more ▼]

In male songbirds, the motivation to sing is largely regulated by testosterone action in the medial preoptic area, whereas testosterone acts on song control nuclei to modulate aspects of song quality. Stereotaxic implantation of testosterone in the medial preoptic nucleus (POM) of castrated male canaries activates a high rate of singing activity, albeit with a longer latency than after systemic testosterone treatment. Systemic testosterone also increases the occurrence of male-like song in female canaries. We hypothesized that this effect is also mediated by testosterone action in the POM. Females were stereotaxically implanted with either testosterone or with estradiol targeted at the POM and their singing activity was recorded daily during 2 hours for 28 days until brains were collected for histological analyses. Following identification of implant localizations, 3 groups of subjects were constituted that had either testosterone or estradiol implanted in the POM or had an implant that had missed the POM (Out). Testosterone and estradiol in POM significantly increased the number of songs produced and the percentage of time spent singing as compared with the Out group. The songs produced were in general of a short duration and of poor quality. This effect was not associated with an increase in HVC volume as observed in males, but testosterone in POM enhanced neurogenesis in HVC, as reflected by an increased density of doublecortin-immunoreactive multipolar neurons. These data indicate that, in female canaries, testosterone acting in the POM plays a significant role in hormone-induced increases in the motivation to sing. [less ▲]

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See detailRapid testosterone-induced growth of the medial preoptic nucleus in male canaries.
Shevchouk, Olesya T.; Ball, Gregory F.; Cornil, Charlotte ULiege et al

in Physiology and Behavior (2019), 204

Testosterone activates singing within days in castrated male songbirds but full song quality only develops after a few weeks. Lesions of the medial preoptic nucleus (POM) inhibit while stereotaxic ... [more ▼]

Testosterone activates singing within days in castrated male songbirds but full song quality only develops after a few weeks. Lesions of the medial preoptic nucleus (POM) inhibit while stereotaxic testosterone implants into this nucleus increase singing rate suggesting that this site plays a key role in the regulation of singing motivation. Testosterone action in the song control system works in parallel to control song quality. Accordingly, systemic testosterone increases POM volume within 1-2days in female canaries, while the increase in volume of song control nuclei takes at least 2weeks. The current study tested whether testosterone action is associated with similar differences in latencies in males. Photosensitive castrated male canaries were implanted with testosterone-filled Silastic implants and control castrates received empty implants, while simultaneously the photoperiod was switched from short- to long-days. Brains were collected from all subjects two days later. Plasma testosterone was elevated in testosterone-treated but not in controls. HVC volumes were not affected, but testosterone significantly increased the POM volume as identified by the dense group of aromatase-immunoreactive neurons, the number and somal area of these neurons and the fractional area they cover in POM. Testosterone-treated females from a previous experiment had a smaller POM volume in similar conditions suggesting the existence of a stable sex difference potentially affecting singing behavior. Thus testosterone induces male POM growth and aromatase expression in this nucleus within two days without affecting HVC size, further supporting the notion that testosterone increases singing motivation via its action in POM. [less ▲]

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See detailSteroid profiles in quail brain and serum: sex and regional differences and effects of castration with steroid replacement
Liere, Philippe; Cornil, Charlotte ULiege; de Bournonville, Marie-Pierre ULiege et al

in Journal of Neuroendocrinology (2019), 31(2), 12681

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See detailEffects of a novel partner and sexual satiety on the expression of male sexual behavior and brain aromatase activity in quail.
de Bournonville, Catherine; Schmit, Mélanie; Telle, Maxime et al

in Behavioural Brain Research (2019), 359

This study was designed to determine whether changes in sexual motivation acutely regulate brain estrogen synthesis by aromatase. Five experiments (Exp.1–5) were first conducted to determine the effect of ... [more ▼]

This study was designed to determine whether changes in sexual motivation acutely regulate brain estrogen synthesis by aromatase. Five experiments (Exp.1–5) were first conducted to determine the effect of recent mating and of the presentation of a new female (Coolidge effect) on sexual motivation. Exp.1–2 showed that 10 min or overnight access to copulation decreases measures of male sexual motivation when male subjects were visually exposed to the female they had copulated with and this effect is not counteracted by the view of a new female. Exp.3 showed that sexual motivation is revived by the view of a new female in previously unmated males only allowed to see another female for 10 min. After mating for 10 min (Exp.4) or overnight (Exp.5) with a female, males showed a decrease in copulatory behavior that was not reversed by access to a new female. Exp.6 and 7 confirmed that overnight copulation (Exp.6) and view of a novel female (Exp.7) respectively decreases and increases sexual behavior and motivation. Yet, these manipulations did not affect brain aromatase activity except in the tuberal hypothalamus. Together these data confirm that copulation or prolonged view of a female de- crease sexual motivation but a reactivation of sexual motivation by a new female can only be obtained if males had only seen another female but not copulated with her, which is different in some degree from the Coolidge effect described in rodents. Moreover changes in brain aromatase do not simply reflect changes in motivation and more complex mechanisms must be considered. [less ▲]

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See detailThe organization and activation of sexual behavior in quail
Cornil, Charlotte ULiege

in Ludwig, Mike; Levkowitz, Gil (Eds.) Model animals in neuroendocrinology: From worm to mouse to man (2019)

Japanese quail are small galliformes, easily raised and maintained in laboratory settings. As their behavior is tightly regulated by sex steroid hormones, they constitute the most studied avian species ... [more ▼]

Japanese quail are small galliformes, easily raised and maintained in laboratory settings. As their behavior is tightly regulated by sex steroid hormones, they constitute the most studied avian species for the hormonal regulation of sexual behavior. They were used to establish the hormonal specificity of this regulation, to map the brain regions involved in behavior control and to demonstrate the key role of brain aromatization of testosterone in the regulation of male sexual behavior. As the quail brain expresses large amounts of aromatase, the key enzyme for the conversion androgens into estrogens, Japanese quail constitutes an exquisite model to study the role and control mechanisms of this enzyme both in vitro and in vivo. Work conducted in quail contributed to show that along with the long-term regulation of the expression of aromatase by sex steroids, its activity is also rapidly regulated by neuronal activity. More recently, work in quail unraveled a role for brain aromatase in the regulation of female sexual behavior. Finally, Japanese quail have been used to study how sex steroid hormones contribute to the emergence and maintenance of sex differences in brain and behavior. In particular, as the embryo develops outside the mother’s womb, they constitute a suitable model to distinguish between the direct effects of hormonal treatments and their influence through modulation of the maternal environment. Most techniques classically employed in neuroscience and neuroendocrinology have been adapted to this species and more modern techniques such as transgenesis and viral transfection,are now becoming available as well thus expanding the possibilities offered by this model. [less ▲]

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See detailCorrelation between song learning and perineuronal nets development in song control system nuclei of juvenile canaries
Cornez, Gilles ULiege; Collignon, Clémentine ULiege; Müller, Wendt et al

Poster (2018, November 05)

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

Perineuronal nets (PNN) are aggregations of extracellular matrix components surrounding the soma of specific neurons, mainly GABAergic interneurons expressing the calcium binding protein parvalbumin (PV+). In mammals, the development of PNN limits synaptogenesis around PV+ neurons and PNNs have been identified as a marker of the end of sensitive periods for brain plasticity in several neuronal systems. In songbirds, vocal learning requires exposure to conspecific vocalizations by male tutors during a sensitive period. This is followed by a sensorimotor period when birds progressively match their vocalizations with the memorized tutor’s song until the fully mature song is crystallized. In a closed-ended learner, the zebra finch, PNN expression in select song nuclei is higher in males than in females and higher in adults than in juvenile males. The timing of PNN appearance in the developing zebra finch brain correlates with the timing of sensitive periods for song learning. We also showed that PNN are more densely expressed in the song control system of zebra finches than in two open-ended learners, the European starling and the canary and that testosterone (T) induces song crystallization in early spring and increases the number of PNN in castrated canaries. Together these data suggest that PNN might regulate the end of the sensitive period(s) for vocal learning during ontogeny. To elucidate this question further, we quantified PNN expression at critical time points during the first year of life in canaries and correlated these data with their song development. Brains were collected from groups of males (n=6-8/group) at time points corresponding to specific vocal developmental stages: first spring (subsong), summer (early plastic song), fall (plastic song), winter (ongoing song crystallization), and second spring (fully crystallized song/adults). In winter, one additional group received T implants to test whether this accelerates PNN development and song crystallization. The number of PNN reached their maximum in the fall in HVC but only in the winter in RA and Area X. In the group treated with T there was no further enhancement of PNN expression over what was observed in untreated birds at the same age. Total song duration and song developmental score only reached their maximum in the spring and were enhanced by T in the winter. Other song characteristics such as the energy or bandwidth were already at the adult levels during the winter. Most of these song measurements correlated with the number of PNN in the song nuclei suggesting that PNN contribute to song crystallization that starts in the winter and is completed at the onset of spring. [less ▲]

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See detailDoes membrane estrogen signaling play a role in brain sexual differentiation ?
Cornil, Charlotte ULiege

Conference (2018, July 17)

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See detailLa souris, le patient, et le faux expert. Décryptage d'une mystification.
Bakker, Julie ULiege; Balthazart, Jacques ULiege; Baron, Frédéric ULiege et al

Article for general public (2018)

La recherche sur animaux est actuellement encadrée de façon stricte en Wallonie comme dans toute l'Union Européenne (voir l'article de Marc Vandenheede publié dans le Vif). Cette législation et les ... [more ▼]

La recherche sur animaux est actuellement encadrée de façon stricte en Wallonie comme dans toute l'Union Européenne (voir l'article de Marc Vandenheede publié dans le Vif). Cette législation et les contrôles qui y sont associés induisent de nombreuses contraintes pratiques, des charges administratives et des coûts financiers importants que les chercheurs seraient certainement heureux d'éviter s'il existait une alternative à l'expérimentation animale. [less ▲]

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See detailNeuroestrogens play a key role in the control of male and female behavior
Cornil, Charlotte ULiege

Scientific conference (2018, February 26)

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See detailDifferential control of appetitive and consummatory sexual behavior by neuroestrogens in male quail
Cornil, Charlotte ULiege; Ball, Gregory; Balthazart, Jacques ULiege

in Hormones and Behavior (2018), 104

Estrogens exert pleiotropic effects on multiple physiological and behavioral traits including sexual behavior. These effects are classically mediated via binding to nuclear receptors and subsequent ... [more ▼]

Estrogens exert pleiotropic effects on multiple physiological and behavioral traits including sexual behavior. These effects are classically mediated via binding to nuclear receptors and subsequent regulation of target gene transcription. Estrogens also affect neuronal activity and cell-signaling pathways via faster, membrane-initiated events. Although the distinction between appetitive and consummatory aspects of sexual behavior has been criticized, this distinction remains valuable in that it facilitates the causal analysis of certain behavioral systems. Effects of neuroestrogens produced by neuronal aromatization of testosterone on copulatory performance (consummatory aspect) and on sexual motivation (appetitive aspect) are described in male quail. The central administration of estradiol rapidly increases expression of sexual motivation, as assessed by two 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 in- tracerebroventricular injection of estrogen receptor antagonists or aromatase inhibitors, respectively, decreases sexual motivation within minutes without affecting performance. The same steroid has thus evolved com- plementary 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. Changes in preoptic aromatase activity and estradiol as well as glutamate concentrations are observed during or immediately after copulation. The interaction between these neuroendocrine/neurochemical changes and their functional significance is discussed. [less ▲]

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See detailThe regulation of birdsong by testosterone: Multiple time-scales and multiple sites of action
Alward, Beau; Cornil, Charlotte ULiege; Balthazart, Jacques ULiege et al

in Hormones and Behavior (2018), 104

Sex steroid hormones act during early development to shape the circuitry upon which these same hormones act in adulthood to control behavioral responses to various stimuli. The “organizational” vs ... [more ▼]

Sex steroid hormones act during early development to shape the circuitry upon which these same hormones act in adulthood to control behavioral responses to various stimuli. The “organizational” vs. “activational” dis- tinction was proposed to explain this temporal difference in hormone action. In both of these cases steroids were thought to act genomically over a time-scale of days to weeks. However, sex steroids can affect behavior over short (e.g., seconds or minutes) time-scales. Here, we discuss how testosterone controls birdsong via actions at different sites and over different time-scales, with an emphasis on this process in canaries (Serinus canaria). Our work shows that testosterone in the medial preoptic nucleus regulates the motivation to sing, but not aspects of song performance. Instead, different aspects of song performance are regulated by long-term actions of testos- terone in steroid-sensitive cortical-like brain regions and the syrinx, the avian vocal production organ. On the other hand, acute aromatase inhibition rapidly reduces the availability of estrogens and this reduction is cor- related with reductions in the motivation to sing and song performance. Thus, testosterone and its estrogenic metabolites regulate distinct features of birdsong depending on the site and temporal window of action. The number of brain areas expressing androgen receptors is higher in species producing learned vocalization as compared to species that produce unlearned calls. An appealing scenario is that rapid effects of steroids in specific brain regions is a derived trait secondary to the widespread genomic effects of steroids in systems where steroids coordinate morphological, physiological, and behavioral traits. [less ▲]

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See detailTiming of perineuronal nets development in the zebra finch song control system correlates with developmental song learning
Cornez, Gilles ULiege; Jonckers, Elisabeth; ter Haar, Sita et al

in Proceedings of the Royal Society. Biological Sciences (2018)

The appearance of perineuronal nets (PNN) represents one of the mechanisms that contribute to the closing of sensitive periods for neural plasticity. This relationship has mostly been studied in the ... [more ▼]

The appearance of perineuronal nets (PNN) represents one of the mechanisms that contribute to the closing of sensitive periods for neural plasticity. This relationship has mostly been studied in the ocular dominance model in rodents. Previous studies also indicated that PNN might control neural plasticity in the song control system (SCS) of songbirds. To further elucidate this relationship, we quantified PNN expression and their localization around parvalbumin interneurons at key time-points during ontogeny in both male and female zebra finches and correlated these data with the well-described development of song in this species. We also extended these analyses to the auditory system. The development of PNN during ontogeny correlated with song crystallization although the timing of PNN appearance in the four main telencephalic song control nuclei slightly varied between nuclei in agreement with the established role these nuclei play during song learning. Our data also indicate that very few PNN develop in the secondary auditory forebrain areas even in adult birds, which may allow constant adaptation to a changing acoustic environment by allowing synaptic reorganization during adulthood. [less ▲]

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See detailBehavioral evidence for sex steroids hypersensitivity in castrated male canaries
Shevchouk, Olesya ULiege; Ghorbanpoor, Samar; Smith, Ed et al

in Hormones and Behavior (2018)

In seasonally breeding songbirds such as canaries, singing behavior is predominantly under the control of tes- tosterone and its metabolites. Short daylengths in the fall that break photorefractoriness ... [more ▼]

In seasonally breeding songbirds such as canaries, singing behavior is predominantly under the control of tes- tosterone and its metabolites. Short daylengths in the fall that break photorefractoriness are followed by in- creasing daylengths in spring that activate singing via both photoperiodic and hormonal mechanisms. However, we observed in a group of castrated male Fife fancy canaries maintained for a long duration under a short day photoperiod a large proportion of subjects that sang at high rates. This singing rate was not correlated with variation in the low circulating concentrations of testosterone. Treatment of these actively singing castrated male canaries with a combination of an aromatase inhibitor (ATD) and an androgen receptor blocker (flutamide) only marginally decreased this singing activity as compared to control untreated birds and did not affect various measures of song quality. The volumes of HVC and of the medial preoptic nucleus (POM) were also unaffected by these treatments but were relatively large and similar to volumes in testosterone-treated males. In contrast, peripheral androgen-sensitive structures such as the cloacal protuberance and syrinx mass were small, similar to what is observed in castrates. Together these data suggest that after a long-term steroid deprivation singing behavior can be activated by very low concentrations of testosterone. Singing normally depends on the acti- vation by testosterone and its metabolites of multiple downstream neurochemical systems such as catechola- mines, nonapeptides or opioids. These transmitter systems might become hypersensitive to steroid action after long term castration as they probably are at the end of winter during the annual cycle in seasonally breeding temperate zone species. [less ▲]

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