Publications by authors named "Jacques Balthazart"

175 Publications

Repeated assessment of changes in testes size in canaries by X-ray computer tomography.

Gen Comp Endocrinol 2021 May 6;310:113808. Epub 2021 May 6.

GIGA Neurosciences, University of Liège, Belgium. Electronic address:

Numerous studies have evaluated changes in time of testicular development in birds by exploratory laparotomy or post-mortem autopsy. The invasive nature of these approaches has obviously limited the frequency at which these measures can be collected. We demonstrate here that accurate assessment of gonadal size can be reliably and repeatedly obtained by computer-assisted X-ray tomography (CT scans). This approach provides images of the testes in the three orthogonal planes that allow measuring either the largest diameter or even the volume of the testes, providing results that match those obtained by surgical approaches.
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http://dx.doi.org/10.1016/j.ygcen.2021.113808DOI Listing
May 2021

Effect of chronic intracerebroventricular administration of an aromatase inhibitor on the expression of socio-sexual behaviors in male Japanese quail.

Behav Brain Res 2021 Jul 24;410:113315. Epub 2021 Apr 24.

GIGA Neurosciences, University of Liège, B-4000, Liège, Belgium. Electronic address:

Aromatase converts androgens into estrogens in the brain of vertebrates including humans. This enzyme is also expressed in other tissues where its action may result in negative effects on human health (e.g., promotion of tumor growth). To prevent these effects, aromatase inhibitors were developed and are currently used to block human estrogen-dependent tumors. In vertebrates including quail, aromatase is expressed in a highly conserved set of interconnected brain nuclei known as the social behavior network. This network is directly implicated in the expression of a large range of social behaviors. The primary goal of this study was to characterize in Japanese quail the potential impact of brain aromatase on sexual behavior, aggressiveness and social motivation (i.e., tendency to approach and stay close to conspecifics). An additional goal was to test the feasibility and effectiveness of long-term delivery of an aromatase inhibitor directly into the third ventricle via Alzet™ osmotic minipumps using male sexual behavior as the aromatase dependent measure. We demonstrate that this mode of administration results in the strongest inhibition of both copulatory behavior and sexual motivation ever observed in this species, while other social behaviors were variably affected. Sexual motivation and the tendency to approach a group of conspecifics including females clearly seem to depend on brain aromatase, but the effects of central estrogen production on aggressive behavior and on the motivation to approach males remain less clear.
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http://dx.doi.org/10.1016/j.bbr.2021.113315DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8178220PMC
July 2021

DNA Methylation Regulates Transcription Factor-Specific Neurodevelopmental but Not Sexually Dimorphic Gene Expression Dynamics in Zebra Finch Telencephalon.

Front Cell Dev Biol 2021 19;9:583555. Epub 2021 Mar 19.

Laboratory of Protein Chemistry, Proteomics and Epigenetic Signaling (PPES), Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.

Song learning in zebra finches () is a prototypical example of a complex learned behavior, yet knowledge of the underlying molecular processes is limited. Therefore, we characterized transcriptomic (RNA-sequencing) and epigenomic (RRBS, reduced representation bisulfite sequencing; immunofluorescence) dynamics in matched zebra finch telencephalon samples of both sexes from 1 day post hatching (1 dph) to adulthood, spanning the critical period for song learning (20 and 65 dph). We identified extensive transcriptional neurodevelopmental changes during postnatal telencephalon development. DNA methylation was very low, yet increased over time, particularly in song control nuclei. Only a small fraction of the massive differential expression in the developing zebra finch telencephalon could be explained by differential CpG and CpH DNA methylation. However, a strong association between DNA methylation and age-dependent gene expression was found for various transcription factors (i.e., , , and ) involved in neurodevelopment. Incomplete dosage compensation, independent of DNA methylation, was found to be largely responsible for sexually dimorphic gene expression, with dosage compensation increasing throughout life. In conclusion, our results indicate that DNA methylation regulates neurodevelopmental gene expression dynamics through steering transcription factor activity, but does not explain sexually dimorphic gene expression patterns in zebra finch telencephalon.
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http://dx.doi.org/10.3389/fcell.2021.583555DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8017237PMC
March 2021

Statistical rules versus biological reasoning: Some apparent conflicts and how to solve them.

Horm Behav 2021 Feb 16:104938. Epub 2021 Feb 16.

Psychology Department, Brock University, Canada.

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http://dx.doi.org/10.1016/j.yhbeh.2021.104938DOI Listing
February 2021

Hypothalamic plasticity in response to changes in photoperiod and food quality: An adaptation to support pre-migratory fattening in songbirds?

Eur J Neurosci 2021 Jan 22;53(2):430-448. Epub 2020 Oct 22.

Department of Zoology, University of Delhi, Delhi, India.

In latitudinal avian migrants, increasing photoperiods induce fat deposition and body mass increase, and subsequent night-time migratory restlessness in captive birds, but the underlying mechanisms remain poorly understood. We hypothesized that an enhanced hypothalamic neuronal plasticity was associated with the photostimulated spring migration phenotype. We tested this idea in adult migratory red-headed buntings (Emberiza bruniceps), as compared with resident Indian weaverbirds (Ploceus philippinus). Birds were exposed to a stimulatory long photoperiod (14L:10D, LP), while controls were kept on a short photoperiod (10L:14D, SP). Under both photoperiods, one half of birds also received a high calorie, protein- and fat-rich diet (SP-R, LP-R) while the other half stayed on the normal diet (SP-N, LP-N). Thirty days later, as expected, the LP had induced multiple changes in the behaviour and physiology in migratory buntings. Photostimulated buntings also developed a preference for the rich food diet. Most interestingly, the LP and the rich diet, both separately and in association, increased neurogenesis in the mediobasal hypothalamus (MBH), as measured by an increased number of cells immunoreactive for doublecortin (DCX), a marker of recently born neurons, in buntings, but not weaverbirds. This neurogenesis was associated with an increased density of fibres immunoreactive for the orexigenic neuropeptide Y (NPY). This hypothalamic plasticity observed in a migratory, but not in a non-migratory, species in response to photoperiod and food quality might represent an adaptation to the pre-migratory fattening, as required to support the extensive energy expenses that incur during the migratory flight.
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http://dx.doi.org/10.1111/ejn.14994DOI Listing
January 2021

Effects of Inactivation of the Periaqueductal Gray on Song Production in Testosterone-Treated Male Canaries ().

eNeuro 2020 Jul/Aug;7(4). Epub 2020 Aug 17.

Program in Neuroscience and Cognitive Science, Department of Psychology, University of Maryland, College Park, MD 20742.

Male canaries () display seasonal changes in the motivation to sing which have been found to be dependent on the action of testosterone (T). During the breeding season when T is high, males sing at a higher rate compared with males with low T. The effect of T on song rate is known to be mediated by the medial preoptic nucleus (POM); however, it is unclear how T signaling in POM impacts song production. One potential mechanism is via modulation of dopaminergic input into song control nuclei by the periaqueductal gray (PAG). In order to test the role of PAG in T-mediated song production, we treated male canaries with peripheral T implants and implanted a guide cannula targeting the PAG. Through this guide cannula, we transiently inactivated PAG with injections of the GABA agonist, muscimol. Each bird received multiple infusions of both muscimol and saline with a 48-h washout period between treatments. The order of injection type was randomized and counterbalanced between individuals. Muscimol infusion into the PAG, but not nearby regions, increased the latency to sing post-injection. These results support the hypothesis that PAG is involved in the production of song, potentially mediating the motivation to sing or alternatively interfering with the pre-motor activity of nucleus RA. Other song features were however not affected.
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http://dx.doi.org/10.1523/ENEURO.0048-20.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7438058PMC
August 2020

Sex differences and similarities in the neural circuit regulating song and other reproductive behaviors in songbirds.

Neurosci Biobehav Rev 2020 11 28;118:258-269. Epub 2020 Jul 28.

GIGA Neuroscience, University of Liege, 15 Avenue Hippocrate, 4000, Liege, Belgium.

In the 1970s, Nottebohm and Arnold reported marked male-biased sex differences in the volume of three song control nuclei in songbirds. Subsequently a series of studies on several songbird species suggested that there is a positive correlation between the degree to which there is a sex difference in the volume of these song control nuclei and in song behavior. This correlation has been questioned in recent years. Furthermore, it has become clear that the song circuit is fully integrated into a more comprehensive neural circuit that regulates multiple courtship and reproductive behaviors including song. Sex differences in songbirds should be evaluated in the context of the full complement of behaviors produced by both sexes in relation to reproduction and based on the entire circuit in order to understand the functional significance of variation between males and females in brain and behavior. Variation in brain and behavior exhibited among living songbird species provides an excellent opportunity to understand the functional significance of sex differences related to social behaviors.
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http://dx.doi.org/10.1016/j.neubiorev.2020.07.026DOI Listing
November 2020

Key role of estrogen receptor β in the organization of brain and behavior of the Japanese quail.

Horm Behav 2020 09 14;125:104827. Epub 2020 Aug 14.

Neuroendocrinology laboratory, GIGA Neurosciences, University of Liège, B-4000 Liège, Belgium. Electronic address:

Estrogens play a key role in the sexual differentiation of the brain and behavior. While early estrogen actions exert masculinizing effects on the brain of male rodents, a diametrically opposite effect is observed in birds where estrogens demasculinize the brain of females. Yet, the two vertebrate classes express similar sex differences in the brain and behavior. Although ERα is thought to play a major role in these processes in rodents, the role of ERβ is still controversial. In birds, the identity of the estrogen receptor(s) underlying the demasculinization of the female brain remains unclear. The aim of the present study was thus to determine in Japanese quail the effects of specific agonists of ERα (propylpyrazole triol, PPT) and ERβ (diarylpropionitrile, DPN) administered at the beginning of the sensitive period (embryonic day 7, E7) on the sexual differentiation of male sexual behavior and on the density of vasotocin-immunoreactive (VT-ir) fibers, a known marker of the organizational action of estrogens on the quail brain. We demonstrate that estradiol benzoate and the ERβ agonist (DPN) demasculinize male sexual behavior and decrease the density of VT-ir fibers in the medial preoptic nucleus and the bed nucleus of the stria terminalis, while PPT has no effect on these measures. These results clearly indicate that ERβ, but not ERα, is involved in the estrogen-induced sexual differentiation of brain and sexual behavior in quail.
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http://dx.doi.org/10.1016/j.yhbeh.2020.104827DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7541764PMC
September 2020

Sexual partner preference in animals and humans.

Neurosci Biobehav Rev 2020 08 22;115:34-47. Epub 2020 May 22.

GIGA Neurosciences, University of Liège, Belgium. Electronic address:

Sex differences in brain and behavior of animals including humans result from an interaction between biological and environmental influences. This is also true for the differences between men and women concerning sexual orientation. Sexual differentiation is mediated by three groups of biological mechanisms: early actions of sex steroids, more direct actions of sex-specific genes not mediated by gonadal sex steroids and epigenetic mechanisms. Differential interactions with parents and conspecifics have additionally long-term influences on behavior. This presentation reviews available evidence indicating that these different mechanisms play a significant role in the control of sexual partner preference in animals and humans, in other words the homosexual versus heterosexual orientation. Clinical and epidemiological studies of phenotypically selected populations indicate that early actions of hormones and genetic factors clearly contribute to the determination of sexual orientation. The maternal embryonic environment also modifies the incidence of male homosexuality via immunological mechanisms. The relative contribution of each of these mechanisms remains however to be determined.
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http://dx.doi.org/10.1016/j.neubiorev.2020.03.024DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7484171PMC
August 2020

Sexually differentiated and neuroanatomically specific co-expression of aromatase neurons and GAD67 in the male and female quail brain.

Eur J Neurosci 2020 08 10;52(3):2963-2981. Epub 2020 Jun 10.

GIGA Neurosciences, University of Liège, Liège, Belgium.

Testosterone aromatization into estrogens in the preoptic area (POA) is critical for the activation of male sexual behavior in many vertebrates. Yet, the cellular mechanisms mediating actions of neuroestrogens on sexual behavior remain largely unknown. We investigated in male and female Japanese quail by dual-label fluorescent in situ hybridization (FISH) whether aromatase-positive (ARO) neurons express glutamic acid decarboxylase 67 (GAD67), the rate-limiting enzyme in GABA biosynthesis. ARO cells and ARO cells double labeled with GAD67 (ARO-GAD67) were counted at standardized locations in the medial preoptic nucleus (POM) and the medial bed nucleus of the stria terminalis (BST) to produce three-dimensional distribution maps. Overall, males had more ARO cells than females in POM and BST. The number of double-labeled ARO-GAD67 cells was also higher in males than in females and greatly varied as a function of the specific position in these nuclei. Significant sex differences were however present only in the most caudal part of POM. Although both ARO and GAD67 were expressed in the VMN, no colocalization between these markers was detected. Together, these data show that a high proportion of estrogen-synthesizing neurons in POM and BST are inhibitory and the colocalization of GAD67 with ARO exhibits a high degree of anatomical specificity as well as localized sex differences. The fact that many preoptic ARO neurons project to the periaqueductal gray in male quail suggests possible mechanisms through which locally produced estrogens could activate male sexual behavior.
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http://dx.doi.org/10.1111/ejn.14765DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7481516PMC
August 2020

Development of Perineuronal Nets during Ontogeny Correlates with Sensorimotor Vocal Learning in Canaries.

eNeuro 2020 Mar/Apr;7(2). Epub 2020 Apr 15.

Behavioral Neuroendocrinology Lab, GIGA Neurosciences, University of Liege, Liege 4000, Belgium

Songbirds are a powerful model to study vocal learning given that aspects of the underlying behavioral and neurobiological mechanisms are analogous in many ways to mechanisms involved in speech learning. Perineuronal nets (PNNs) represent one of the mechanisms controlling the closing of sensitive periods for vocal learning in the songbird brain. In zebra finches, PNN develop around parvalbumin (PV)-expressing interneurons in selected song control nuclei during ontogeny and their development is delayed if juveniles are deprived of a tutor. However, song learning in zebra finches takes place during a relatively short period of development, and it is difficult to determine whether PNN development correlates with the end of the sensory or the sensorimotor learning period. Canaries have a longer period of sensorimotor vocal learning, spanning over their first year of life so that it should be easier to test whether PNN development correlates with the end of sensory or sensorimotor vocal learning. Here, we quantified PNN around PV-interneurons in the brain of male canaries from hatching until the first breeding season and analyzed in parallel the development of their song. PNN development around PV-interneurons specifically took place and their number reached its maximum around the end of the sensorimotor learning stage, well after the end of sensory vocal learning, and correlated with song development. This suggests that PNN are specifically involved in the termination of the sensitive period for sensorimotor vocal learning.
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http://dx.doi.org/10.1523/ENEURO.0361-19.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7160306PMC
April 2020

Molecular correlates of hypothalamic development in songbird ontogeny in comparison with the telencephalon.

FASEB J 2020 04 13;34(4):4997-5015. Epub 2020 Feb 13.

Laboratory of Behavioral Neuroendocrinology, GIGA Neuroscience, University of Liege, Liege, Belgium.

Development of the songbird brain provides an excellent experimental model for understanding the regulation of sex differences in ontogeny. Considering the regulatory role of the hypothalamus in endocrine, in particular reproductive, physiology, we measured the structural (volume) and molecular correlates of hypothalamic development during ontogeny of male and female zebra finches. We quantified by relative quantitative polymerase chain reaction (rqPCR) the expression of 14 genes related to thyroid and steroid hormones actions as well as 12 genes related to brain plasticity at four specific time points during ontogeny and compared these expression patterns with the expression of the same genes as detected by transcriptomics in the telencephalon. These two different methodological approaches detected specific changes with age and demonstrated that in a substantial number of cases changes observed in both brain regions are nearly identical. Other genes however had a tissue-specific developmental pattern. Sex differences or interactions of sex by age were detected in the expression of a subset of genes, more in hypothalamus than telencephalon. These results correlate with multiple known aspects of the developmental and reproductive physiology but also raise a number of new functional questions.
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http://dx.doi.org/10.1096/fj.201902477RDOI Listing
April 2020

How technical progress reshaped behavioral neuroendocrinology during the last 50 years… and some methodological remarks.

Horm Behav 2020 02 13;118:104682. Epub 2020 Jan 13.

GIGA Neurosciences, University of Liege, Belgium. Electronic address:

The first issue of Hormones and Behavior was published 50 years ago in 1969, a time when most of the techniques we currently use in Behavioral Endocrinology were not available. Researchers have during the last 5 decades developed techniques that allow measuring hormones in small volumes of biological samples, identify the sites where steroids act in the brain to activate sexual behavior, characterize and quantify gene expression correlated with behavior expression, modify this expression in a specific manner, and manipulate the activity of selected neuronal populations by chemogenetic and optogenetic techniques. This technical progress has considerably transformed the field and has been very beneficial for our understanding of the endocrine controls of behavior in general, but it did also come with some caveats. The facilitation of scientific investigations came with some relaxation of methodological exigency. Some critical controls are no longer performed on a regular basis and complex techniques supplied as ready to use kits are implemented without precise knowledge of their limitations. We present here a selective review of the most important of these new techniques, their potential problems and how they changed our view of the hormonal control of behavior. Fortunately, the scientific endeavor is a self-correcting process. The problems have been identified and corrections have been proposed. The next decades will obviously be filled with exciting discoveries in behavioral neuroendocrinology.
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http://dx.doi.org/10.1016/j.yhbeh.2020.104682DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7019036PMC
February 2020

Seasonal changes of perineuronal nets and song learning in adult canaries (Serinus canaria).

Behav Brain Res 2020 02 16;380:112437. Epub 2019 Dec 16.

Laboratory of Behavioral Neuroendocrinology, GIGA Neurosciences, University of Liege, Belgium. Electronic address:

Songbirds learn their song during a sensitive period of development associated with enhanced neural plasticity. In addition, in open-ended learners such as canaries, a sensitive period for sensorimotor vocal learning reopens each year in the fall and leads to song modifications between successive breeding seasons. The variability observed in song production across seasons in adult canaries correlates with seasonal fluctuations of testosterone concentrations and with morphological changes in nuclei of the song control system (SCS). The sensitive periods for song learning during ontogeny and then again in adulthood could be controlled by the development of perineuronal nets (PNN) around parvalbumin-expressing interneurones (PV) which limits learning-induced neuroplasticity. However, this relationship has never been investigated in the context of adult vocal learning in adult songbirds. Here we explored PNN and PV expression in the SCS of adult male Fife Fancy canaries in relation to the seasonal variations of their singing behaviour. We found a clear pattern of seasonal variation in testosterone concentrations and song production. Furthermore, PNN expression was significantly higher in two specific song control nuclei, the robust nucleus of the arcopallium (RA) and the Area X of the basal ganglia, during the breeding season and during the later stages of sensorimotor song development compared to birds in an earlier stage of sensorimotor development during the fall. These data provide the first evidence that changes in PNN expression could represent a mechanism regulating the closing-reopening of sensitive periods for vocal learning across seasons in adult songbirds.
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http://dx.doi.org/10.1016/j.bbr.2019.112437DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6945773PMC
February 2020

Testosterone stimulates perineuronal nets development around parvalbumin cells in the adult canary brain in parallel with song crystallization.

Horm Behav 2020 03 6;119:104643. Epub 2019 Dec 6.

GIGA Neuroscience, University of Liege, Liege 4000, Belgium. Electronic address:

Perineuronal nets (PNN) of the extracellular matrix are dense aggregations of chondroitin-sulfate proteoglycans that usually surround fast-spiking parvalbumin-expressing inhibitory interneurons (PV). The development of PNN around PV appears specifically at the end of sensitive periods of visual learning and limits the synaptic plasticity in the visual cortex of mammals. Seasonal songbirds display a high level of adult neuroplasticity associated with vocal learning, which is regulated by fluctuations of circulating testosterone concentrations. Seasonal changes in testosterone concentrations and in neuroplasticity are associated with vocal changes between the non-breeding and breeding seasons. Increases in blood testosterone concentrations in the spring lead to the annual crystallization of song so that song becomes more stereotyped. Here we explore whether testosterone also regulates PNN expression in the song control system of male and female canaries. We show that, in both males and females, testosterone increases the number of PNN and of PV neurons in the three main telencephalic song control nuclei HVC, RA (nucleus robustus arcopallialis) and Area X and increases the PNN localization around PV interneurons. Singing activity was recorded in males and quantitative analyses demonstrated that testosterone also increased male singing rate, song duration and song energy while decreasing song entropy. Together, these data suggest that the development of PNN could provide the synaptic stability required to maintain the stability of the testosterone-induced crystallized song. This provides the new evidence for a role of PNN in the regulation of adult seasonal plasticity in seasonal songbirds.
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http://dx.doi.org/10.1016/j.yhbeh.2019.104643DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7065963PMC
March 2020

Comparing perineuronal nets and parvalbumin development between blackbird species with differences in early developmental song exposure.

J Exp Biol 2020 01 6;223(Pt 1). Epub 2020 Jan 6.

Department of Biology, Hofstra University, Hempstead, NY 11549, USA

Brood parasitic songbirds are a natural system in which developing birds are isolated from species-typical song and therefore present a unique opportunity to compare neural plasticity in song learners raised with and without conspecific tutors. We compared perineuronal nets (PNN) and parvalbumin (PV) in song control nuclei in juveniles and adults of two closely related icterid species (i.e. blackbirds): brown-headed cowbirds (; brood parasite) and red-winged blackbirds (; non-parasite). The number of PV cells per nucleus was significantly higher in adults compared with juveniles in the nucleus HVC and the robust nucleus of the arcopallium (RA), whereas no significant species difference appeared in any region of interest. The number of PNN per nuclei was significantly higher in adults compared with juveniles in HVC, RA and Area X, but only RA exhibited a significant difference between species. PV cells surrounded by PNN (PV+PNN) also exhibited age-related differences in HVC, RA and Area X, but RA was the only region in which PV+PNN exhibited significant species differences. Furthermore, a significant interaction existed in RA between age and species with respect to PNN and PV+PNN, revealing RA as a region displaying differing plasticity patterns across age and species. Additional comparisons of PNN and PV between adult male and female cowbirds revealed that males have greater numbers of all three measures in RA compared with females. Species-, sex- and age-related differences in RA suggest that species differences in neural plasticity are related to differences in song production rather than sensitivity to song learning, despite a stark contrast in early exposure to conspecific male tutors.
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http://dx.doi.org/10.1242/jeb.212910DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6983712PMC
January 2020

In vivo online monitoring of testosterone-induced neuroplasticity in a female songbird.

Horm Behav 2020 02 30;118:104639. Epub 2019 Nov 30.

Bio-Imaging Lab, University of Antwerp, Belgium. Electronic address:

Adult neuroplasticity in the song control system of seasonal songbirds is largely driven by photoperiod-induced increases in testosterone. Prior studies of the relationships between testosterone, song performance and neuroplasticity used invasive techniques, which prevent analyzing the dynamic changes over time and often focus on pre-defined regions-of-interest instead of examining the entire brain. Here, we combined (i) in vivo diffusion tensor imaging (DTI) to assess structural neuroplasticity with (ii) repeated monitoring of song and (iii) measures of plasma testosterone concentrations in thirteen female photosensitive starlings (Sturnus vulgaris) who received a testosterone implant for 3 weeks. We observed fast (days) and slower (weeks) effects of testosterone on song behavior and structural neuroplasticity and determined how these effects correlate on a within-subject level, which suggested separate contributions of the song motor and anterior forebrain pathways in the development of song performance. Specifically, the increase in testosterone correlated with a rapid increase of song rate and RA volume, and with changes in Area X microstructure. After implant removal, these variables rapidly reverted to baseline levels. In contrast, the more gradual improvement of song quality was positively correlated with the fractional anisotropy values (DTI metric sensitive to white matter changes) of the HVC-RA tract and of the lamina mesopallialis, which contains fibers connecting the song control nuclei. Thus, we confirmed many of the previously reported testosterone-induced effects, like the increase in song control nuclei volume, but identified for the first time a more global picture of the spatio-temporal changes in brain plasticity.
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http://dx.doi.org/10.1016/j.yhbeh.2019.104639DOI Listing
February 2020

How does testosterone act to regulate a multifaceted adaptive response? Lessons from studies of the avian song system.

J Neuroendocrinol 2020 01 2;32(1):e12793. Epub 2019 Oct 2.

Department of Psychology, University of Maryland, College Park, MD, USA.

In male songbirds, song functions to attract a mate or to defend a territory; it is therefore often produced in the context of reproduction. Testosterone of gonadal origin increases during the reproductive phase of the annual cycle and significantly enhances song production, as well as song development, via effects on song crystallisation. The neural control of birdsong production and learning is highly modular. We implanted testosterone or androgen antagonists into specific brain regions or in the periphery of castrated male canaries and, in this way, identified how androgen signalling in specific locations regulates a variety of birdsong features. For example, castrated male canaries treated with testosterone in the preoptic area only and exposed to long days sing at high rates compared to castrated male canaries not treated with testosterone. However, these birds with testosterone in the preoptic area still produce songs with substantially lower song stereotypy and amplitude; these features are controlled by testosterone acting in the song control nuclei HVC and robust nucleus of the arcopallium. Specific aspects of the learned singing behaviour are thus regulated by androgens acting at multiple levels in the brain in a non-redundant fashion. The action of testosterone in the preoptic area is related to the hormonal regulation of the motivation to sing but not to various aspects of song performance. Multiple aspects of song quality are instead precisely regulated by steroids acting in distinct song control nuclei. Females exert a strong choice for specific features of male song in canaries and this choice is influenced by the endocrine state of the female. The female song system is also involved in song production, as well as song perception, although the specificity of this hormone action has not yet been investigated.
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http://dx.doi.org/10.1111/jne.12793DOI Listing
January 2020

The neuroendocrine integration of environmental information, the regulation and action of testosterone and the challenge hypothesis.

Horm Behav 2020 07 5;123:104574. Epub 2019 Sep 5.

Neuroendocrinology Unit, GIGA Neurosciences, University of Liège, 15 avenue Hippocrate (B36), 4000 Liège, Belgium.

The authors of the original challenge hypothesis proposed influential hypotheses concerning the relationship between testosterone concentrations in the blood and aggressive social behaviors. Many of the key observations were made in avian species studied in the wild and in captivity. In this review we evaluate some remaining questions about the ideas discussed in the challenge hypothesis from a neuroendocrine perspective. For example, a rise in testosterone in response to a social aggressive stimulus might involve complex social information being processed by the brain and an appropriate signal sent to the gonadotrophin-releasing hormone (GnRH) neuronal system. Alternatively, social stimuli could more directly stimulate the testis and testosterone release via sympathetic innervation of the testis though such pathways have not been linked to a response to social behaviors. The social behavior decision network in the brain seems to play a key role in the regulation of aggressive behavior but how sensory information concerning aggressive behaviors is interpreted appropriately, processed by the social decision network and sent to the GnRH system is still not well understood. There are continuing questions about the extensive species variation in whether an increase in testosterone occurs in response to a territorial challenge, what its function might be and whether increases in testosterone are necessary to activate morphological changes, or the expression of sexual and aggressive behaviors associated with successful reproduction.
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http://dx.doi.org/10.1016/j.yhbeh.2019.104574DOI Listing
July 2020

New concepts in the study of the sexual differentiation and activation of reproductive behavior, a personal view.

Front Neuroendocrinol 2019 10 17;55:100785. Epub 2019 Aug 17.

GIGA Neurosciences, University of Liège, Belgium. Electronic address:

Since the beginning of this century, research methods in neuroendocrinology enjoyed extensive refinements and innovation. These advances allowed collection of huge amounts of new data and the development of new ideas but have not led to this point, with a few exceptions, to the development of new conceptual advances. Conceptual advances that took place largely resulted from the ingenious insights of several investigators. I summarize here some of these new ideas as they relate to the sexual differentiation and activation by sex steroids of reproductive behaviors and I discuss how our research contributed to the general picture. This selective review clearly demonstrates the importance of conceptual changes that have taken place in this field since beginning of the 21st century. The recent technological advances suggest that our understanding of hormones, brain and behavior relationships will continue to improve in a very fundamental manner over the coming years.
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http://dx.doi.org/10.1016/j.yfrne.2019.100785DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6858558PMC
October 2019

Testosterone or Estradiol When Implanted in the Medial Preoptic Nucleus Trigger Short Low-Amplitude Songs in Female Canaries.

eNeuro 2019 Mar/Apr;6(2). Epub 2019 May 8.

GIGA Neurosciences, University of Liege, 4000 Liège, Belgium

In male songbirds, the motivation to sing is largely regulated by testosterone (T) action in the medial preoptic area, whereas T acts on song control nuclei to modulate aspects of song quality. Stereotaxic implantation of T 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 T treatment. Systemic T also increases the occurrence of male-like song in female canaries. We hypothesized that this effect is also mediated by T action in the POM. Females were stereotaxically implanted with either T or with 17β-estradiol (E2) targeted at the POM and their singing activity was recorded daily during 2 h for 28 d until brains were collected for histological analyses. Following identification of implant localizations, three groups of subjects were constituted that had either T or E2 implanted in the POM or had an implant that had missed the POM (Out). T and E2 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 T in POM enhanced neurogenesis in HVC, as reflected by an increased density of doublecortin-immunoreactive (DCX-ir) multipolar neurons. These data indicate that, in female canaries, T acting in the POM plays a significant role in hormone-induced increases in the motivation to sing.
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http://dx.doi.org/10.1523/ENEURO.0502-18.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6506820PMC
February 2020

Rapid testosterone-induced growth of the medial preoptic nucleus in male canaries.

Physiol Behav 2019 05 7;204:20-26. Epub 2019 Feb 7.

GIGA Neurosciences, University of Liege, Liège, Belgium. Electronic address:

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 1-2 days in female canaries, while the increase in volume of song control nuclei takes at least 2 weeks. 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.
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http://dx.doi.org/10.1016/j.physbeh.2019.02.007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6475650PMC
May 2019

Site-specific effects of aromatase inhibition on the activation of male sexual behavior in male Japanese quail (Coturnix japonica).

Horm Behav 2019 02 9;108:42-49. Epub 2019 Jan 9.

GIGA Neurosciences, University of Liège, Belgium. Electronic address:

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 took longer 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.
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http://dx.doi.org/10.1016/j.yhbeh.2018.12.015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6377315PMC
February 2019

Steroid profiles in quail brain and serum: Sex and regional differences and effects of castration with steroid replacement.

J Neuroendocrinol 2019 02 1;31(2):e12681. Epub 2019 Feb 1.

GIGA Neurosciences, University of Liège, Liège, Belgium.

Both systemic and local production contribute to the concentration of steroids measured in the brain. This idea was originally based on rodent studies and was later extended to other species, including humans and birds. In quail, a widely used model in behavioural neuroendocrinology, it was demonstrated that all enzymes needed to produce sex steroids from cholesterol are expressed and active in the brain, although the actual concentrations of steroids produced were never investigated. We carried out a steroid profiling in multiple brain regions and serum of sexually mature male and female quail by gas chromatography coupled with mass spectrometry. The concentrations of some steroids (eg, corticosterone, progesterone and testosterone) were in equilibrium between the brain and periphery, whereas other steroids (eg, pregnenolone (PREG), 5α/β-dihydroprogesterone and oestrogens) were more concentrated in the brain. In the brain regions investigated, PREG sulphate, progesterone and oestrogen concentrations were higher in the hypothalamus-preoptic area. Progesterone and its metabolites were more concentrated in the female than the male brain, whereas testosterone, its metabolites and dehydroepiandrosterone were more concentrated in males, suggesting that sex steroids present in quail brain mainly depend on their specific steroidogenic pathways in the ovaries and testes. However, the results of castration experiments suggested that sex steroids could also be produced in the brain independently of the peripheral source. Treatment with testosterone or oestradiol restored the concentrations of most androgens or oestrogens, respectively, although penetration of oestradiol in the brain appeared to be more limited. These studies illustrate the complex interaction between local brain synthesis and the supply from the periphery for the steroids present in the brain that are either directly active or represent the substrate of centrally located enzymes.
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http://dx.doi.org/10.1111/jne.12681DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6412023PMC
February 2019

Effects of a novel partner and sexual satiety on the expression of male sexual behavior and brain aromatase activity in quail.

Behav Brain Res 2019 02 18;359:502-515. Epub 2018 Nov 18.

Neuroendocrinology unit, GIGA Neurosciences, University of Liège, Belgium. Electronic address:

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 decrease 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.
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http://dx.doi.org/10.1016/j.bbr.2018.11.026DOI Listing
February 2019

Timing of perineuronal net development in the zebra finch song control system correlates with developmental song learning.

Proc Biol Sci 2018 07 18;285(1883). Epub 2018 Jul 18.

GIGA Neuroscience, University of Liege, Liege 4000, Belgium

The appearance of perineuronal nets (PNNs) 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 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.
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http://dx.doi.org/10.1098/rspb.2018.0849DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6083260PMC
July 2018

Rapid effects of steroids in the brain: Introduction to special issue.

Horm Behav 2018 08 22;104:1-3. Epub 2018 Jun 22.

GIGA Neurosciences, University of Liege, B-4000 Liège, Belgium. Electronic address:

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http://dx.doi.org/10.1016/j.yhbeh.2018.06.003DOI Listing
August 2018

Behavioral evidence for sex steroids hypersensitivity in castrated male canaries.

Horm Behav 2018 07 28;103:80-96. Epub 2018 Jun 28.

GIGA Neurosciences, University of Liege, Liège, Belgium. Electronic address:

In seasonally breeding songbirds such as canaries, singing behavior is predominantly under the control of testosterone and its metabolites. Short daylengths in the fall that break photorefractoriness are followed by increasing 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 activation by testosterone and its metabolites of multiple downstream neurochemical systems such as catecholamines, 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.
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http://dx.doi.org/10.1016/j.yhbeh.2018.06.004DOI Listing
July 2018

The regulation of birdsong by testosterone: Multiple time-scales and multiple sites of action.

Horm Behav 2018 08 23;104:32-40. Epub 2018 Apr 23.

Department of Psychology, University of Maryland, College Park, MD 20742, United States.

Contribution to Special Issue on Fast effects of steroids. 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" distinction 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 testosterone 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 correlated 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.
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http://dx.doi.org/10.1016/j.yhbeh.2018.04.010DOI Listing
August 2018

Rapid changes in auditory processing in songbirds following acute aromatase inhibition as assessed by fMRI.

Horm Behav 2018 08 7;104:63-76. Epub 2018 Apr 7.

Research Group in Behavioral Neuroendocrinology, GIGA Neurosciences, University of Liège, B-4000 Liège, Belgium.

Contribution to Special Issue on Fast effects of steroids. This review introduces functional MRI (fMRI) as an outstanding tool to assess rapid effects of sex steroids on auditory processing in seasonal songbirds. We emphasize specific advantages of this method as compared to other more conventional and invasive methods used for this purpose and summarize an exemplary auditory fMRI study performed on male starlings exposed to different types of starling song before and immediately after the inhibition of aromatase activity by an i.p. injection of Vorozole™. We describe how most challenges that relate to the necessity to anesthetize subjects and minimize image- and sound-artifacts can be overcome in order to obtain a voxel-based 3D-representation of changes in auditory brain activity to various sound stimuli before and immediately after a pharmacologically-induced depletion of endogenous estrogens. Analysis of the fMRI data by assumption-free statistical methods identified fast specific changes in activity in the auditory brain regions that were stimulus-specific, varying over different seasons, and in several instances lateralized to the left side of the brain. This set of results illustrates the unique features of fMRI that provides opportunities to localize and quantify the brain responses to rapid changes in hormonal status. fMRI offers a new image-guided research strategy in which the spatio-temporal profile of fast neuromodulations can be identified and linked to specific behavioral inputs or outputs. This approach can also be combined with more localized invasive methods to investigate the mechanisms underlying the observed neural changes.
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http://dx.doi.org/10.1016/j.yhbeh.2018.03.011DOI Listing
August 2018