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See detailReversing song behavior phenotype: Testosterone driven induction of singing and measures of song quality in adult male and female canaries (Serinus canaria)
Madison, Farrah N.; Rouse, Melvin L. Jr; Balthazart, Jacques ULg et al

in General and comparative endocrinology (2015), 215

In songbirds, such as canaries (Serinus canaria), the song control circuit has been shown to undergo a remarkable change in morphology in response to exogenous testosterone (T). It is also well ... [more ▼]

In songbirds, such as canaries (Serinus canaria), the song control circuit has been shown to undergo a remarkable change in morphology in response to exogenous testosterone (T). It is also well established that HVC, a telencephalic nucleus involved in song production, is significantly larger in males than in females. T regulates seasonal changes in HVC volume in males, and exposure to exogenous T in adult females increases HVC volume and singing activity such that their song becomes more male-like in frequency and structure. However, whether there are sex differences in the ability of T to modulate changes in the song system and song behavior has not been investigated in canaries. In this study, we compared the effects of increasing doses of T on singing and song control nuclei volumes in adult male and female American Singer canaries exposed to identical environmental conditions. Males were castrated and all birds were placed on short days (8L:16D) for 8weeks. Males and females were implanted either with a 2, 6 or 12mm long Silastic implant filled with crystalline T or an empty 12mm implant as control. Birds were then housed individually in sound-attenuated chambers. Brains were collected from six birds from each group after 1week or 3weeks of treatment. Testosterone was not equally effective in increasing singing activity in both males and females. Changes in song quality and occurrence rate took place after a shorter latency in males than in females; however, females did undergo marked changes in a number of measures of song behavior if given sufficient time. Males responded with an increase in HVC volume at all three doses. In females, T-induced changes in HVC volume only had limited amplitude and these volumes never reached male-typical levels, suggesting that there are sex differences in the neural substrate that responds to T. [less ▲]

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See detailSeasonal changes in the neuroendocrine system: Introduction to the special issue.
Ball, Gregory F.; Balthazart, Jacques ULg

in Frontiers in neuroendocrinology (2015), 37

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See detailGlutamate controls brain estrogen synthesis during sexual interactions
de Bournonville, Catherine ULg; Aourz, Najat; Van Eeckhaut, Ann et al

Poster (2014, November 17)

Besides their long-lasting effects mediated by a modulation of gene transcription, brain-derived estrogens can rapidly regulate (within minutes) reproductive behaviors. In vitro, the activity of aromatase ... [more ▼]

Besides their long-lasting effects mediated by a modulation of gene transcription, brain-derived estrogens can rapidly regulate (within minutes) reproductive behaviors. In vitro, the activity of aromatase (AA), the enzyme responsible for the conversion of androgens into estrogens, is also regulated on a similar short time-scale, via phosphorylation of the enzyme resulting from changes in neuronal activity or glutamate release. Acute changes in AA have been documented ex vivo in specific brain regions following exposure to social or stressful stimuli but the mechanism underlying these regulations is not known. To investigate whether glutamate is implicated in these rapid changes in AA, male quail received a unilateral injection of kainate in the medial preoptic nucleus (POM). The left and right preoptic areas were collected 20 min later and assayed separately by the tritiated water technique for AA. As shown previously in preoptic explants maintained in vitro, AA was downregulated in the kainate-injected hemisphere as compared to the non-injected side. To determine whether the decline in AA detected in the POM after a sexual interaction could be mediated by an increased release of glutamate in this region, extracellular glutamate concentration was measured by in vivo microdialysis with a probe implanted in the POM of sexually mature males. Dialysate was collected every 3 minutes over three periods of 15 min when the male was (1) alone, (2) allowed to freely copulate with a female and (3) alone again. A transient rise in extracellular glutamate concentration was observed specifically and immediately after the expression of cloacal contact movements, when semen is transferred to the female. Glutamate returned to a basal level after the female was removed. Together, these results indicate that the mechanism of acute regulation of aromatase activity by glutamate identified in vitro is potentially responsible for the acute regulation of the enzyme observed in vivo following copulation. As rapid changes in brain estrogen synthesis and its actions are apparently related to the control of sexual motivation rather than sexual performance, follow up experiments should now determine whether the release of glutamate in the POM occurs in parallel with an increase in motivation or follows the termination of the copulatory sequence. [less ▲]

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See detailIs it useful to view the brain as a secondary sexual characteristic?
Ball, Gregory F.; Balthazart, Jacques ULg; McCarthy, Margaret M.

in Neuroscience and biobehavioral reviews (2014), 46 Pt 4

Many sex differences in brain and behavior related to reproduction are thought to have evolved based on sexual selection involving direct competition for mates during male-male competition and female ... [more ▼]

Many sex differences in brain and behavior related to reproduction are thought to have evolved based on sexual selection involving direct competition for mates during male-male competition and female choice. Therefore, certain aspects of brain circuitry can be viewed as secondary sexual characteristics. The study of proximate causes reveals that sex differences in the brain of mammals and birds reflect organizational and activational effects of sex steroids as articulated by Young and collaborators. However, sex differences in brain and behavior have been identified in the cognitive domain with no obvious link to reproduction. Recent views of sexual selection advocate for a broader view of how intra-sexual selection might occur including such examples as competition within female populations for resources that facilitate access to mates rather than mating competition per se. Sex differences can also come about for other reasons than sexual selection and recent work on neuroendocrine mechanisms has identified a plethora of ways that the brain can develop in a sex specific manner. Identifying the brain as sexually selected requires careful hypothesis testing so that one can link a sex-biased aspect of a neural trait to a behavior that provides an advantage in a competitive mating situation. [less ▲]

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See detailEndogenous versus exogenous markers of adult neurogenesis in canaries and other birds: advantages and disadvantages.
Balthazart, Jacques ULg; Ball, Gregory F.

in The Journal of comparative neurology (2014), 522(18), 4100-20

Although the existence of newborn neurons had originally been suggested, but not broadly accepted, based on studies in adult rodent brains, the presence of an active neurogenesis process in adult ... [more ▼]

Although the existence of newborn neurons had originally been suggested, but not broadly accepted, based on studies in adult rodent brains, the presence of an active neurogenesis process in adult homoeothermic vertebrates was first firmly established in songbirds. Adult neurogenesis was initially studied with the tritiated thymidine technique, later replaced by the injection and detection of the marker of DNA replication 5-bromo-2'-deoxyuridine (BrdU). More recently, various endogenous markers were used to identify young neurons or cycling neuronal progenitors. We review here the respective advantages and pitfalls of these different approaches in birds, with specific reference to the microtubule-associated protein, doublecortin (DCX), that has been extensively used to identify young newly born neurons in adult brains. All these techniques of course have limitations. Exogenous markers label cells replicating their DNA only during a brief period and it is difficult to select injection doses that would exhaustively label all these cells without inducing DNA damage that will also result in some form of labeling during repair. On the other hand, specificity of endogenous markers is difficult to establish due to problems related to the specificity of antibodies (these problems can be, but are not always, addressed) and more importantly because it is difficult, if not impossible, to prove that a given marker exhaustively and specifically labels a given cell population. Despite these potential limitations, these endogenous markers and DCX staining in particular clearly represent a useful approach to the detailed study of neurogenesis especially when combined with other techniques such as BrdU. [less ▲]

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See detailDissociable effects of social context on song and doublecortin immunoreactivity in male canaries.
Alward, Beau A.; Mayes, Wade D.; Peng, Katherine et al

in The European journal of neuroscience (2014), 40(6), 2941-7

Variation in environmental factors such as day length and social context greatly affects reproductive behavior and the brain areas that regulate these behaviors. One such behavior is song in songbirds ... [more ▼]

Variation in environmental factors such as day length and social context greatly affects reproductive behavior and the brain areas that regulate these behaviors. One such behavior is song in songbirds, which males use to attract a mate during the breeding season. In these species the absence of a potential mate leads to an increase in the number of songs produced, while the presence of a mate greatly diminishes singing. Interestingly, although long days promote song behavior, producing song itself can promote the incorporation of new neurons in brain regions controlling song output. Social context can also affect such neuroplasticity in these song control nuclei. The goal of the present study was to investigate in canaries (Serinus canaria), a songbird species, how photoperiod and social context affect song and the incorporation of new neurons, as measured by the microtubule-associated protein doublecortin (DCX) in HVC, a key vocal production brain region of the song control system. We show that long days increased HVC size and singing activity. In addition, male canaries paired with a female for 2 weeks showed enhanced DCX-immunoreactivity in HVC relative to birds housed alone. Strikingly, however, paired males sang fewer songs that exhibited a reduction in acoustic features such as song complexity and energy, compared with birds housed alone, which sang prolifically. These results show that social presence plays a significant role in the regulation of neural and behavioral plasticity in songbirds and can exert these effects in opposition to what might be expected based on activity-induced neurogenesis. [less ▲]

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See detailFos expression in monoaminergic cell groups in response to sociosexual interactions in male and female Japanese quail.
Iyilikci, Onur; Baxter, Samantha; Balthazart, Jacques ULg et al

in Behavioral neuroscience (2014), 128(1), 48-60

Monoaminergic neurotransmitters regulate different components of sexual behaviors, but how the different monoaminergic cell groups selectively regulate these behaviors is not well understood. We examined ... [more ▼]

Monoaminergic neurotransmitters regulate different components of sexual behaviors, but how the different monoaminergic cell groups selectively regulate these behaviors is not well understood. We examined the potential contribution of these different cell groups in the control of different aspects of sexual behaviors in male and female quail. We used double-label immunohistochemistry, labeling the protein product of the immediate early gene, Fos, along with tyrosine hydroxylase (TH) or tryptophan hydroxylase (TPH), markers for catecholaminergic or indolaminergic cells, respectively. Rhythmic Cloacal Sphincter Movements (RCSM) were recorded as a measure of male appetitive sexual behavior. Consummatory sexual behaviors were evaluated based on the species-typical copulation sequence. Enhanced Fos expression in the medial preoptic nucleus and bed nucleus of the stria terminalis was observed in association with both physical and visual contact to the opposite sex for males, but not for females. Fos induction associated with physical contact was observed in the ventral tegmental area and anterior periaqueductal gray in both sexes. In males only, the number of Fos-immunoreactive (ir) cells increased in the visual contact condition in these 2 dopaminergic cell groups, however no significant effect was observed for double-labeled TH-Fos-ir cells. In addition, consummatory but not appetitive sexual behavior increased Fos expression in TPH-ir cells in the raphe pallidus of males. This increase following physical but not visual contact agrees with the notion that activation of the serotoninergic system is implicated in the development of sexual satiation but not activated by simply viewing a female, in contrast to the dopaminergic system. [less ▲]

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See detailEstrogens control female sexual motivation and receptivity in quail.
de Bournonville, Catherine ULg; Ball, Gregory, F.; Balthazart, Jacques ULg et al

Poster (2013, November 10)

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See detailFemale sexual and social behaviors are controlled by estrogens
de Bournonville, Catherine ULg; Ball, Gregory F; Balthazart, Jacques ULg et al

Poster (2013)

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See detailFemale sexual motivation is controlled by estrogens in quail
de Bournonville, Catherine ULg; Ball, Gregory F; Balthazart, Jacques ULg et al

Poster (2013)

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See detailLocal estradiol synthesis in the brain and its implication in male and female sexual motivation of Japanese quail
de Bournonville, Catherine ULg; Schmit, Mélanie; Ball, Gregory F et al

in Trabajos del Instituto Cajal (2013)

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See detailAre neuroestrogens implicated in sexual motivation? Development of experimental protocols.
de Bournonville, Catherine ULg; Schmit, Mélanie; Ball, Gregory F et al

Poster (2013)

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See detailRapid control of reproductive behaviour by locally synthesised oestrogens: focus on aromatase.
Cornil, Charlotte ULg; Seredynski, Aurore ULg; de Bournonville, Catherine ULg et al

in Journal of Neuroendocrinology (2013), 25(11), 1070-8

Oestrogens activate nucleus- and membrane-initiated signalling. Nucleus-initiated events control a wide array of physiological and behavioural responses. These effects generally take place within ... [more ▼]

Oestrogens activate nucleus- and membrane-initiated signalling. Nucleus-initiated events control a wide array of physiological and behavioural responses. These effects generally take place within relatively long periods of time (several hours to days). By contrast, membrane-initiated signalling affects a multitude of cellular functions in a much shorter timeframe (seconds to minutes). However, much less is known about their functional significance. Furthermore, the origin of the oestrogens able to trigger these acute effects is rarely examined. Finally, these two distinct types of oestrogenic actions have often been studied independently such that we do not exactly know how they cooperate to control the same response. The present review presents a synthesis of recent work carried out in our laboratory that aimed to address these issues in the context of the study of male sexual behaviour in Japanese quail, which is a considered as a suitable species for tackling these issues. The first section presents data indicating that 17b-oestradiol, or its membrane impermeable analogues, acutely enhances measures of male sexual motivation but does not affect copulatory behaviour. These effects depend on the activation of membrane-initiated events and local oestrogen production. The second part of this review discusses the regulation of brain oestrogen synthesis through post-translational modifications of the enzyme aromatase. Initially discovered in vitro, these rapid and reversible enzymatic modulations occur in vivo following variations in the social and environment context and therefore provide a mechanism of acute regulation of local oestrogen provision with a spatial and time resolution compatible with the rapid effects observed on male sexual behaviour. Finally, we discuss how these distinct modes of oestrogenic action (membrane- versus nucleus-initiated) acting in different time frames (short- versus long-term) interact to control different components (motivation versus performance) of the same behavioural response and improve reproductive fitness. [less ▲]

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See detailA new method for in vitro detection of bromodeoxyuridine in serum: a proof of concept in a songbird species, the canary.
Barker, Jennifer M.; Charlier, Thierry D.; Ball, Gregory F. et al

in PloS one (2013), 8(5), 63692

Systemic injection of a thymidine analogue such as bromodeoxyuridine (BrdU) in vertebrates is commonly used to detect and study cell production during development, adulthood, and pathology, particularly ... [more ▼]

Systemic injection of a thymidine analogue such as bromodeoxyuridine (BrdU) in vertebrates is commonly used to detect and study cell production during development, adulthood, and pathology, particularly in studies of adult neurogenesis. Although researchers are applying this technique to multiple species in various physiological conditions, the rate of BrdU clearance from the serum remains unknown in most cases. Changes in this clearance rate as a function of the species, sex or endocrine condition could however profoundly affect the interpretation of the results. We describe a rapid, sensitive, but simple bioassay for post-injection detection and quantification of BrdU in serum. This procedure was shown to be suitable for determining the length of time a thymidine analogue remains in the bloodstream of one avian species and seems applicable to any vertebrate provided sufficiently large blood samples can be collected. This technique was used to demonstrate that, in canaries, BrdU injected at a dose of 100 mg/kg is no longer available for incorporation into DNA between 30 and 60 min post-injection, a delay shorter than anticipated based on the available literature. Preliminary data suggest a similar fast clearance in Japanese quail and mice. [less ▲]

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See detailAnatomically discrete sex differences and enhancement by testosterone of cell proliferation in the telencephalic ventricle zone of the adult canary brain.
Barker, Jennifer M.; Ball, Gregory F.; Balthazart, Jacques ULg

in Journal of chemical neuroanatomy (2013)

Previous work in songbirds has suggested that testosterone increases neuronal recruitment and survival in HVC but does not affect neuronal proliferation in the ventricular zone and that males and females ... [more ▼]

Previous work in songbirds has suggested that testosterone increases neuronal recruitment and survival in HVC but does not affect neuronal proliferation in the ventricular zone and that males and females have similar rates of proliferation except at discrete locations. Many of these conclusions are however based on limited data or were inferred indirectly. Here we specifically tested the effects of testosterone on cellular proliferation in the ventricular zone of both male and female adult canaries. We implanted adult birds of both sexes with testosterone or empty implants for 1 week and injected them with BrdU. One day later, we collected their brains and quantified BrdU-positive cells in the ventricular zone (VZ) at different rostro-caudal levels of the brain, ranging from the level where the song nucleus Area X occurs through the caudal extent of HVC. Proliferation in the dorsal part of the VZ was low and unaffected by sex or testosterone treatment. In the ventral part of the VZ, females had more proliferating cells than males, but only at rostral levels, near Area X. Also in the ventral part of the VZ, testosterone increased proliferation in birds of both sexes, but only in the mid- to caudal-VZ, caudal to the level of Area X, around the septum and HVC. We thus demonstrate here that there is both an effect of testosterone and possibly a more subtle effect of sex on cellular proliferation in the adult songbird brain, and that these effects are specific to different levels of the brain. [less ▲]

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See detailDifferential effects of global versus local testosterone on singing behavior and its underlying neural substrate.
Alward, Beau A.; Balthazart, Jacques ULg; Ball, Gregory F.

in Proceedings of the National Academy of Sciences of the United States of America (2013), 110(48), 19573-8

Steroid hormones regulate multiple but distinct aspects of social behaviors. Testosterone (T) has multiple effects on learned courtship song in that it regulates both the motivation to sing in a ... [more ▼]

Steroid hormones regulate multiple but distinct aspects of social behaviors. Testosterone (T) has multiple effects on learned courtship song in that it regulates both the motivation to sing in a particular social context as well as the quality of song produced. The neural substrate(s) where T acts to regulate the motivation to sing as opposed to other aspects of song has not been definitively characterized. We show here that T implants in the medial preoptic nucleus (POM) of castrated male canaries (Serinus canaria) increase song rate but do not enhance acoustic features such as song stereotypy compared with birds receiving peripheral T that can act globally throughout the brain. Strikingly, T action in the POM increased song control nuclei volume, consistent with the hypothesis that singing activity induces neuroplasticity in the song control system independent of T acting in these nuclei. When presented with a female canary, POM-T birds copulated at a rate comparable to birds receiving systemic T but produced fewer calls and songs in her presence. Thus, POM is a key site where T acts to activate copulation and increase song rate, an appetitive sexual behavior in songbirds, but T action in other areas of the brain or periphery (e.g., HVC, dopaminergic cell groups, or the syrinx) is required to enhance the quality of song (i.e., stereotypy) as well as regulate context-specific vocalizations. These results have broad implications for research concerning how steroids act at multiple brain loci to regulate distinct sociosexual behaviors and the associated neuroplasticity. [less ▲]

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See detailDynamic changes in brain aromatase activity following sexual interactions in males: Where, when and why?
de Bournonville, Catherine ULg; Dickens, Molly J.; Ball, Gregory F. et al

in Psychoneuroendocrinology (2013), 38(6), 789-99

It is increasingly recognized that estrogens produce rapid and transient effects at many neural sites ultimately impacting physiological and behavioral endpoints. The ability of estrogens to acutely ... [more ▼]

It is increasingly recognized that estrogens produce rapid and transient effects at many neural sites ultimately impacting physiological and behavioral endpoints. The ability of estrogens to acutely regulate cellular processes implies that their concentration should also be rapidly fine-tuned. Accordingly, rapid changes in the catalytic activity of aromatase, the limiting enzyme for estrogen synthesis, have been identified that could serve as a regulatory mechanism of local estrogen concentrations. However, the precise anatomical localization, time-course, triggering stimuli and functional significance of these enzymatic changes in vivo are not well understood. To address these issues as to where, when and why aromatase activity (AA) rapidly changes after sexual interactions, AA was assayed in six populations of aromatase-expressing cells microdissected from the brain of male quail that experienced varying durations of visual exposure to or copulation with a female. Sexual interactions resulted in a rapid AA inhibition. This inhibition occurred in specific brain regions (including the medial preoptic nucleus), in a context-dependent fashion and time-scale suggestive of post-translational modifications of the enzyme. Interestingly, the enzymatic fluctuations occurring in the preoptic area followed rather than preceded copulation and were tied specifically to the female's presence. This pattern of enzymatic changes suggests that rapid estrogen effects are important during the motivational phase of the behavior to trigger physiological events essential to activate mate search and copulation. [less ▲]

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