Modulation by steroid hormones of a "sexy" acoustic signal in an Oscine species, the Common Canary Serinus canaria

The respective influence of testosterone and estradiol on the structure of the Common Canary Serinus canaria song was studied by experimentally controlling blood levels of steroid hormones in males and analyzing the consequent effects on acoustic parameters. A detailed acoustic analysis of the songs produced before and after hormonal manipulation revealed that testosterone and estradiol seem to control distinct song parameters independently. The presence of receptors for testosterone and estradiol in the brain neural pathway controlling song production strongly suggests that the observed effects are mediated by a steroid action at the neuronal level.<br>A influência da testosterona e do estradiol, respectivamente, na estrutura do canto do Canário-do-reino Serinus canaria foi estudada analisando o efeito da manipulação dos níveis sanguíneos de hormônios esteróides em machos nos parâmetros acústicos do canto. Uma analise detalhada dos cantos produzidos antes e depois da manipulação hormonal revelou que testosterona e estradiol parecem controlar independentemente parâmetros acústicos distintos. A presença de receptores para esses hormônios no circuito neuronal para controle da produção do canto sugere fortemente que os efeitos observados são mediados pela ação de esteróides a nivel neuronal

Own Song Selectivity in the Songbird Auditory Pathway: Suppression by Norepinephrine

Like human speech, birdsong is a learned behavior that supports species and individual recognition. Norepinephrine is a catecholamine suspected to play a role in song learning. The goal of this study was to investigate the role of norepinephrine in bird's own song selectivity, a property thought to be important for auditory feedback processes required for song learning and maintenance.Using functional magnetic resonance imaging, we show that injection of DSP-4, a specific noradrenergic toxin, unmasks own song selectivity in the dorsal part of NCM, a secondary auditory region.The level of norepinephrine throughout the telencephalon is known to be high in alert birds and low in sleeping birds. Our results suggest that norepinephrine activity can be further decreased, giving rise to a strong own song selective signal in dorsal NCM. This latent own song selective signal, which is only revealed under conditions of very low noradrenergic activity, might play a role in the auditory feedback and/or the integration of this feedback with the motor circuitry for vocal learning and maintenance

Rapid Effects of Hearing Song on Catecholaminergic Activity in the Songbird Auditory Pathway

Catecholaminergic (CA) neurons innervate sensory areas and affect the processing of sensory signals. For example, in birds, CA fibers innervate the auditory pathway at each level, including the midbrain, thalamus, and forebrain. We have shown previously that in female European starlings, CA activity in the auditory forebrain can be enhanced by exposure to attractive male song for one week. It is not known, however, whether hearing song can initiate that activity more rapidly. Here, we exposed estrogen-primed, female white-throated sparrows to conspecific male song and looked for evidence of rapid synthesis of catecholamines in auditory areas. In one hemisphere of the brain, we used immunohistochemistry to detect the phosphorylation of tyrosine hydroxylase (TH), a rate-limiting enzyme in the CA synthetic pathway. We found that immunoreactivity for TH phosphorylated at serine 40 increased dramatically in the auditory forebrain, but not the auditory thalamus and midbrain, after 15 min of song exposure. In the other hemisphere, we used high pressure liquid chromatography to measure catecholamines and their metabolites. We found that two dopamine metabolites, dihydroxyphenylacetic acid and homovanillic acid, increased in the auditory forebrain but not the auditory midbrain after 30 min of exposure to conspecific song. Our results are consistent with the hypothesis that exposure to a behaviorally relevant auditory stimulus rapidly induces CA activity, which may play a role in auditory responses

Noradrenergic control of auditory information processing in female canaries

An ethological procedure, based on the study of the sexual responsiveness of female canaries (Serinus canaria) to song playbacks was used to investigate the function of central noradrenergic inputs in the processing of auditory information. The effects of a noradrenergic denervation on sexual responses was analyzed in females exposed to playbacks of biological relevant auditory stimuli, i.e. sexually stimulating songs, presented alone or masked by auditory distractors. A decrease in behavioral responsiveness was observed as a function of the amount of masking distractors indicating that female canaries have the perceptual ability to discriminate and selectively attend to biologically relevant songs. After the systemic administration of DSP-4, a specific noradrenergic neurotoxin, females exhibited an overall decrease in sexual responsiveness to songs masked or not by distractors. No effect of DSP-4 were detected on the motor activity nor on reproductive behaviors. These results indicate that central noradrenergic inputs modulate the sexual behavior of female canaries by affecting the auditory processing of relevant information contained in sexually stimulating songs. (C) 2002 Elsevier Science B.V. All rights reserved

Catecholaminergic inputs to aromatase cells in the canary auditory forebrain

The caudomedial nidopallium in songbirds is a specialized forebrain auditory region involved in the processing of species-typical vocalizations. It receives a prominent catecholaminergic projection with many fibers forming basket-like structures around non-immunoreactive cells. We investigated in male canaries the anatomical relationship between tyrosine hydroxylase and cells immunoreactive for the steroid metabolizing enzyme, aromatase, in the caudomedial nidopallium using double-label immunocytochemistry. Fibers immunoreactive for tyrosine hydroxylase established numerous close contacts with aromatase-immunoreactive cells and often encircled these cells to form basket-like structures. Aromatase containing cells in the caudomedial nidopallium are therefore a major target of catecholaminergic inputs in canary. Interactions between catecholaminergic systems and aromatase in the caudomedial nidopallium may provide one mechanism for the regulation of estrogens involved in song perception and memorization

Song activation by testosterone is associated with an increased catecholaminergic innervation of the song control system in female canaries

In canaries, singing and a large number of morphological features of the neural system that mediates the learning, perception and production of song exhibit marked sex differences. Although these differences have been mainly attributed to sex-specific patterns of the action of testosterone and its metabolites, the mechanisms by which sex steroids regulate brain and behavior are far from being completely understood. Given that the density of immunoreactive catecholaminergic fibers that innervate telencephalic song nuclei in canaries is higher in males, which sing, than in females, which usually do not sing, we hypothesized that some of the effects induced by testosterone on song behavior are mediated through the action of the steroid on the catecholaminergic neurons which innervate the song control nuclei. Therefore, we investigated in female canaries the effects of a treatment with exogenous testosterone on song production, on the volume of song control nuclei, and on the catecholaminergic innervation of these nuclei as assessed by immunocytochemical visualization of tyrosine hydroxylase. Testosterone induced male-like singing in all females and increased by about 80% the volume of two telencephalic song control nuclei, the high vocal center (HVC) and the nucleus robustus archistriatalis (RA). Testosterone also significantly increased the fractional area covered by tyrosine hydroxylase-immunoreactive structures (fibers and varicosities) in most telencephalic song control nuclei (HVC, the lateral and medial parts of the magnocellular nucleus of the anterior neostriatum, the nucleus interfacialis, and to a lesser extent RA). By contrast, testosterone did not affect the catecholaminergic innervation of the telencephalic areas adjacent to HVC and RA. Together these data demonstrate that, in parallel to its effects on song behavior and on the morphology of the song control system, testosterone also regulates the catecholaminergic innervation of most telencephalic song control nuclei in canaries. The endocrine regulation of singing may thus involve the neuromodulatory action of specialized dopaminergic and/or noradrenergic projections onto several key parts of the song control system. (C) 2003 IBRO. Published by Elsevier Ltd. All rights reserved

The Distribution of Tyrosine Hydroxylase in the Canary Brain: Demonstration of a Specific and Sexually Dimorphic Catecholaminergic Innervation of the Telencephalic Song Control Nulcei

Singing and the processing of auditory information related to song can be affected by experimental manipulations of catecholamine activity in the brain of zebra finches. We investigated, by immunocytochemistry in the brain of male and female canaries, the distribution of tyrosine hydroxylase (TH), the rate-limiting step in the synthesis of catecholamines. Fibers immunoreactive for TH (TH-ir) were particularly abundant in the lobus parolfactorius, the paleostriatum primitivum, and the nucleus septalis lateralis. A high density of TH-ir basket-like structures was observed in the caudomedial neostriatum, an area involved in song perception and recognition. In most males, a high density of TH-ir fibers outlined the telencephalic song control nuclei including the high vocal center, the nucleus robustus archistriatalis, the nucleus interfascialis, the lateral and medial parts of the magnocellular nucleus of the anterior neostriatum, and area X of the lobus parolfactorius. The higher density of fibers immunoreactive for TH in these nuclei, compared with the surrounding telencephalon, supports the notion that the morphological evolution of the song control nuclei was accompanied by a neurochemical specialization. This specific innervation of the song control regions was, in general, not found in females. The specific presence of high densities of TH-ir fibers in the song system of male canaries and the sex difference of this innervation provide anatomical evidence in support of the claim that dopamine and/or norepinephrine play important roles in the modulation of song learning and production

The origin of catecholaminergic inputs to the song control nucleus RA in canaries

Song control nuclei in oscines receive dense catecholaminergic inputs but their anatomical origin is poorly understood. We analyzed catecholaminergic inputs to the nucleus robustus archistriatalis (RA) in canaries by retrograde tract-tracing combined with immunocytochemistry for tyrosine hydroxylase. In both sexes, dopaminergic inputs to RA come mostly from the A1 1 (mesencephalic central gray) and A10 (area ventralis of Tsai) cell groups but the locus coeruleus and subcoeruleus (A6) also send noradrenergic projections to RA. No input originates in the hypothalamic and in the A5 to A1 catecholaminergic groups. These findings and previous work on the high vocal center (HVc) indicate that the two major nuclei of the motor pathway controlling song production (RA and HVc) receive catecholaminergic inputs of similar origins