Ontogeny of sex differences in steroid-sensitive regions in the quail brain (Coturnix Japonica)
Mouriec, Karen ; ; Balthazart, Jacques
Poster (2010, May)
Sex differences affecting the expression of sexual behavior are observed in many species. In quail, expression of the male-typical copulatory pattern is androgen-dependent. This behavior disappears within ... [more ▼]
Sex differences affecting the expression of sexual behavior are observed in many species. In quail, expression of the male-typical copulatory pattern is androgen-dependent. This behavior disappears within a week after castration and is restored after a few days of treatment with exogenous testosterone. In contrast, ovariectomized females treated with testosterone never show the sequence of male-typical copulatory behavior. This sex difference in responsiveness to testosterone results from organizational effects of embryonic estrogens secreted by the female ovary. The behavioral phenotype can be completely reversed by treatment, before embryonic day 12, of male embryos with estrogens or of female embryos with an aromatase inhibitor. In the quail brain, the medial preoptic nucleus (POM) is a necessary and sufficient site for the activation by testosterone of sexual behavior. Aromatase, the enzyme converting testosterone into estradiol, is densely expressed in POM and its activity is sexually differentiated (males>females) even when birds are treated with a same dose of testosterone. Aromatase and other neuroendocrine systems are thus, like sexual behavior, differentially activated by testosterone in adult quail but the cellular basis of these sexually differentiated features presumably organized in early life by steroid action have not been identified. To analyze the ontogeny of steroid sensitive regions that control behavioral sex differences in the quail brain, we injected 5-bromo-2-deoxyuridine (BrdU) in eggs at different stages of the embryonic (E) development (E8, E10, E12, E14 and E16) and sacrificed the animals at postnatal (PN) day 56. Large numbers of BrdU-positive cells were observed throughout the POM of males and females injected on E8-E10 but most cells were post-mitotic in both sexes on E14-E16. E12 injections resulted in a larger number of BrdU cells in females than in males. This differential number of BrdU-positive cells seen at PN56 in birds injected on E12 could result from a) a difference in the age at which cells become post-mitotic (males before females or alternatively females before males, so that male cells labeled by BrdU on E12 dilute their label in subsequent divisions) or b) a differential apoptosis between E13 and PN56. However, no sex differences in the number of BrdU positive cells was observed in embryos injected with BrdU on E12 and killed on E13. Furthermore, BrdU injections on E14 labeled very few cells at PN 56 suggesting that the POM is essentially post-mitotic at that age. The sex difference observed in birds injected at E12 should result from a differential apoptosis after E13. Double-label immunohistochemistry for BrdU and the neuronal marker Hu (C/D) indicated that all BrdU-positive cells born between E8 and E16 are not neurons (no double label) suggesting that these are glial cells. This sex difference in (glial?) proliferation around the end of the critical period of sexual differentiation may play a key role in the differentiation of brain and behavior. The specific phenotype of these cells and the mechanisms mediating their differential development are currently under investigation. [less ▲]Detailed reference viewed: 35 (1 ULg)
Testosterone increases cell turnover in song nucleus HVC and increases cell recruitment into Area X of adult female canaries.
Barker, Jennifer ; ; Balthazart, Jacques et al
Poster (2010, May)
In songbirds, song control nuclei such as HVC and Area X, show seasonal changes in volume that are regulated, at least in part, by the action of gonadal testosterone (T) and its metabolites. These changes ... [more ▼]
In songbirds, song control nuclei such as HVC and Area X, show seasonal changes in volume that are regulated, at least in part, by the action of gonadal testosterone (T) and its metabolites. These changes in volume are a result of changes in cell size, dendritic branching and, in HVC, the incorporation of newborn neurons. Doublecortin (DCX) is a microtubule-associated protein expressed during development and in adulthood in post-mitotic migrating and differentiating neurons in mammals. Our previous studies in male canaries demonstrated that DCX is expressed in BrdU-positive neurons consistent with DCX being a marker of neurogenesis in adult canaries. Testosterone induces marked increases in song nuclei volume in adult female canaries making these nuclei more male-like. Within the songbird brain, T can be metabolized to 5 alpha-dihydrotestosterone (DHT) and 17 beta-estradiol (E2). We found previously that both these metabolites are required to increase the volume of song nuclei in adult female canaries, but the cellular basis of this adult neuroplasticity is not well understood. Within HVC, the number of DCX-immunoreactive (ir) cells can be increased by photostimulation or treatment with T, but the effects of T and its metabolites on cell death in the songbird brain had not yet been elucidated. We therefore examined the effect of DHT and E2 on DCX expression and cell death in the song nuclei of adult female canaries. Intact female canaries were implanted with Silastic tubing containing crystalline T, DHT, E2, or a combination of DHT+E2. Control animals received empty implants. All birds were kept under early spring-like photoperiodic conditions (11L:13D) for 3 weeks. In HVC, the total number of DCX-ir cells was increased by treatment with T or DHT+E2 as compared to control birds, but was not affected by treatment with DHT or E2 alone. The number of pyknotic cells observed in the HVC was also increased by T but not by its metabolites. In Area X, the total number of DCX-ir cells was increased by treatment with T or DHT+E2, but the number of pyknotic cells was unaffected by hormone treatment. These results suggest that T enhances cellular turnover in the HVC (migration into, and cell death within, HVC), but affects only recruitment of new neurons into Area X. [less ▲]Detailed reference viewed: 78 (3 ULg)
Japanese quail as a model system for studying the neuroendocrine control of reproductive and social behaviors.
; Balthazart, Jacques
in ILAR Journal (2010), 51(4), 310-25
Japanese quail (Coturnix japonica; referred to simply as quail in this article) readily exhibit sexual behavior and related social behaviors in captive conditions and have therefore proven valuable for ... [more ▼]
Japanese quail (Coturnix japonica; referred to simply as quail in this article) readily exhibit sexual behavior and related social behaviors in captive conditions and have therefore proven valuable for studies of how early social experience can shape adult mate preference and sexual behavior. Quail have also been used in sexual conditioning studies illustrating that natural stimuli predict successful reproduction via Pavlovian processes. In addition, they have proven to be a good model to study how variation in photoperiod regulates reproduction and how variation in gonadal steroid hormones controls sexual behavior. For example, studies have shown that testosterone activates male-typical behaviors after being metabolized into estrogenic and androgenic metabolites. A critical site of action for these metabolites is the medial preoptic nucleus (POM), which is larger in males than in females. The enzyme aromatase converts testosterone to estradiol and is enriched in the POM in a male-biased fashion. Quail studies were the first to show that this enzyme is regulated both relatively slowly via genomic actions of steroids and more quickly via phosphorylation. With this base of knowledge and the recent cloning of the entire genome of the closely related chicken, quail will be valuable for future studies connecting gene expression to sexual and social behaviors. [less ▲]Detailed reference viewed: 26 (2 ULg)
Diversity of mechanisms involved in aromatase regulation and estrogen action in the brain
Charlier, Thierry ; Cornil, Charlotte ; 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 ▲]Detailed reference viewed: 55 (5 ULg)
Pheromones in birds: myth or reality?
; Balthazart, Jacques
in Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural and Behavioral Physiology (2010), 196(10), 751-66
Birds are anosmic or at best microsmatic... This misbelief persisted until very recently and has strongly influenced the outcome of communication studies in birds, with olfaction remaining neglected as ... [more ▼]
Birds are anosmic or at best microsmatic... This misbelief persisted until very recently and has strongly influenced the outcome of communication studies in birds, with olfaction remaining neglected as compared to acoustic and visual channels. However, there is now clear empirical evidence showing that olfaction is perfectly functional in birds and birds use olfactory information in a variety of ethological contexts. Although the existence of pheromones has never been formally demonstrated in this vertebrate class, different groups of birds, such as petrels, auklets and ducks have been shown to produce specific scents that could play a significant role in within-species social interactions. Behavioral experiments have indeed demonstrated that these odors influence the behavior of conspecifics. Additionally, in quail, deprivation of olfactory inputs decreases neuronal activation induced by sexual interactions with a female. It seems therefore well established that birds enjoy a functional sense of smell and a fast growing body of experimental evidence suggests that they use this channel of olfactory communication to control their social life. The unequivocal identification of an avian pheromone is, however, still ahead of us but there are now many exciting opportunities to unravel the behavioral and physiological particularities of chemical communication in birds. [less ▲]Detailed reference viewed: 82 (1 ULg)
Effects of estrogen receptors alpha and beta agonists on the sexual behavior and the neuroplasticity in male Japanese quail.
Seredynski, Aurore ; Charlier, Thierry ; Balthazart, Jacques
Poster (2010)Detailed reference viewed: 10 (1 ULg)
Neuroplasticity and steroid-dependent male sexual behavior modulated by steroid receptor coactivator 2 (SRC2) in Japanese quail (Coturnix japonica).
Niessen, Neville-Andrew ; Balthazart, Jacques ; et al
Poster (2010)Detailed reference viewed: 13 (3 ULg)
Own song selectivity in the songbird auditory pathway: suppression by norepinephrine
; ; et al
Poster (2010)Detailed reference viewed: 5 (0 ULg)
Expression of the steroid receptor coactivators SRC-1 and CARM1 is modulated during different phases of neurogenesis in the dentate gyrus of adult female rats
Charlier, Thierry ; ; Balthazart, Jacques et al
Poster (2010)Detailed reference viewed: 10 (1 ULg)
Steroid receptor coactivator 2 (SRC-2) mediates steroid-dependent male sexual behavior and neuroplasticity in Japanese quail (Coturnix japonica).
Niessen, Neville-Andrew ; Balthazart, Jacques ; et al
Poster (2010)Detailed reference viewed: 11 (3 ULg)
Sex steroid-induced neuroplasticity and behavioral activation in birds
Balthazart, Jacques ; Charlier, Thierry ; Barker, Jennifer et al
in European Journal of Neuroscience (2010), 32Detailed reference viewed: 24 (6 ULg)
Rapid regulation of aromatase activity and the role of stress
; Charlier, Thierry ; Cornil, Charlotte et al
Poster (2010)Detailed reference viewed: 19 (2 ULg)
Sex difference and steroid control of corticosteroid-binding globulin concentration in Japanese quail
Charlier, Thierry ; Seredynski, Aurore ; Balthazart, Jacques
Poster (2010)Detailed reference viewed: 16 (1 ULg)
Behavioral implications of rapid changes in steroid production action in the brain [Commentary on Pradhan D.S., Newman A.E.M., Wacker D.W., Wingfield J.C., Schlinger B.A. and Soma K.K.: Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season. Hormones and Behavior, this issue].
in Hormones & Behavior (2010), 57Detailed reference viewed: 26 (6 ULg)
Seasonal and hormonal modulation of neurotransmitter systems in the song control circuit.
; Balthazart, Jacques
in Journal of Chemical Neuroanatomy (2010), 39(2), 82-95
In the years following the discovery of the song system, it was realized that this specialized circuit controlling learned vocalizations in songbirds (a) constitutes a specific target for sex steroid ... [more ▼]
In the years following the discovery of the song system, it was realized that this specialized circuit controlling learned vocalizations in songbirds (a) constitutes a specific target for sex steroid hormone action and expresses androgen and (for some nuclei) estrogen receptors, (b) exhibits a chemical neuroanatomical pattern consisting in a differential expression of various neuropeptides and neurotransmitters receptors as compared to surrounding structures and (c) shows pronounced seasonal variations in volume and physiology based, at least in the case of HVC, on a seasonal change in neuron recruitment and survival. During the past 30 years numerous studies have investigated how seasonal changes, transduced largely but not exclusively through changes in sex steroid concentrations, affect singing frequency and quality by modulating the structure and activity of the song control circuit. These studies showed that testosterone or its metabolite estradiol, control seasonal variation in singing quality by a direct action on song control nuclei. These studies also gave rise to the hypothesis that the probability of song production in response to a given stimulus (i.e. its motivation) is controlled through effects on the medial preoptic area and on catecholaminergic cell groups that project to song control nuclei. Selective pharmacological manipulations confirmed that the noradrenergic system indeed plays a role in the control of singing behavior. More experimental work is, however, needed to identify specific genes related to neurotransmission that are regulated by steroids in functionally defined brain areas to enhance different aspects of song behavior. [less ▲]Detailed reference viewed: 27 (2 ULg)
Introduction to the chemical neuroanatomy of birdsong.
; Balthazart, Jacques
in Journal of Chemical Neuroanatomy (2010), 39(2), 67-71Detailed reference viewed: 47 (0 ULg)
Testosterone recruits new aromatase-imunoreactive cells in neonatal quail brain.
; Cornil, Charlotte ; Balthazart, Jacques
in Neuroreport (2010), 21(5), 376-80
It was shown earlier that, in Japanese quail the mechanism controlling the induction by testosterone of aromatase activity develops between embryonic days 10 and 14. The cellular processes underlying this ... [more ▼]
It was shown earlier that, in Japanese quail the mechanism controlling the induction by testosterone of aromatase activity develops between embryonic days 10 and 14. The cellular processes underlying this activation have, however, not been investigated in detail. Here, we demonstrate that the increase in aromatase activity observed in neonates treated with testosterone propionate between postnatal days 1 and 3 results from the recruitment of additional populations of aromatase-immunoreactive cells that were not expressing the enzyme at detectable levels before. This recruitment concerns all brain nuclei normally expressing the enzyme even if it is more prominent in the ventromedial hypothalamus than in other nuclei. [less ▲]Detailed reference viewed: 23 (1 ULg)
Behavioral effects of brain-derived estrogens in birds.
Balthazart, Jacques ; Taziaux, Mélanie ; et al
in Annals of the New York Academy of Sciences (2009), 1163
In birds as in other vertebrates, estrogens produced in the brain by aromatization of testosterone have widespread effects on behavior. Research conducted with male Japanese quail demonstrates that ... [more ▼]
In birds as in other vertebrates, estrogens produced in the brain by aromatization of testosterone have widespread effects on behavior. Research conducted with male Japanese quail demonstrates that effects of brain estrogens on all aspects of sexual behavior, including appetitive and consummatory components as well as learned aspects, can be divided into two main classes based on their time course. First, estrogens via binding to estrogen receptors regulate the transcription of a variety of genes involved primarily in neurotransmission. These neurochemical effects ultimately result in the activation of male copulatory behavior after a latency of a few days. Correlatively, testosterone and its aromatized metabolites increase the transcription of the aromatase mRNA, resulting in an increased concentration and activity of the enzyme that actually precedes behavioral activation. Second, recent studies with quail demonstrate that brain aromatase activity can also be modulated within minutes by phosphorylation processes regulated by changes in intracellular calcium concentration, such as those associated with glutamatergic neurotransmission. The rapid upregulations or downregulations of brain estrogen concentration (presumably resulting from these changes in aromatase activity) affect, by nongenomic mechanisms with relatively short latencies (frequency increases or decreases respectively within 10-15 min), the expression of male sexual behavior in quail and also in rodents. Brain estrogens thus affect behavior on different time scales by genomic and nongenomic mechanisms similar to those of a hormone or a neurotransmitter. [less ▲]Detailed reference viewed: 29 (3 ULg)
Estradiol, a key endocrine signal in the sexual differentiation and activation of reproductive behavior in quail.
Balthazart, Jacques ; Cornil, Charlotte ; Charlier, Thierry et al
in Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology (2009), 311(5), 323-45
In Japanese quail, estrogen's effects on sexual behavior can be divided into three classes based on the underlying mechanisms and time-course of action and release. During embryonic life, the embryonic ... [more ▼]
In Japanese quail, estrogen's effects on sexual behavior can be divided into three classes based on the underlying mechanisms and time-course of action and release. During embryonic life, the embryonic ovary secretes large amounts of estrogens. In contrast to what is observed in mammals where sexual differentiation essentially proceeds via masculinization of the males, in quail, females are demasculinized by their endogenous ovarian estrogens, an effect that can be blocked by injection of an aromatase inhibitor and mimicked in male embryos by an injection of estradiol. In adulthood, testosterone secreted by the testes is converted into estrogens by the preoptic aromatase. Locally produced estrogens activate male sexual behavior largely through the activation of estrogen receptors resulting in the transcription of a variety of genes, including brain aromatase (genomic effect). Both changes in estrogen production and action are observed within latencies ranging from a few hours to a few days, and are completely reversible. Additionally, brain aromatase activity can be modulated within minutes by calcium-dependent phosphorylations, triggered by variations in glutamatergic neurotransmission. These rapid changes in aromatase activity affect with relatively short latencies (10-15 min) the expression of male sexual behavior in quail and also in mice. Overall, the effects of estrogens on sexual behavior can thus be categorized into three classes: organizational (irreversible genomic action during ontogeny), activational (reversible genomic action during adulthood) and rapid nongenomic effects. Rapid and slower changes in brain aromatase activity match well with the two modes of estrogen action on behavior and provide temporal variations in the estrogens' bioavailability that should be able to support the entire range of established effects for this steroid. [less ▲]Detailed reference viewed: 29 (11 ULg)