Elsevier

Neuroscience

Volume 121, Issue 3, 15 October 2003, Pages 801-814
Neuroscience

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

https://doi.org/10.1016/S0306-4522(03)00496-2Get rights and content

Abstract

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.

Section snippets

Subjects and neuroendocrine procedures

This study was performed on adult female canaries (Serinus canaria) bought from a local dealer in Liège, Belgium (SPRL G. Guisset & Fils) in the fall (October). Birds were maintained in indoor aviaries in unisexual groups with a maximum of 10 subjects per cage under a photoperiod of 11 h of light: 13 h of dark per day, with food and water available ad libitum. In this way we maintained the birds in a photosensitive reproductive state indicative of late winter– early spring (Nicholls et al., 1988

Morphological and physiological effects of T

A two-way ANOVA with one independent (treatments: T and Control) and one repeated (periods: before and after T) factor identified a significant effect of the hormone treatment (F1,13=12.147, P<0.01), of the period (F1,13=15.598, P<0.01) and of their interaction (F1,13=31.715, P<0.0001) on the cloacal protuberance area. Post hoc comparisons (Tukey HSD) indicated that the mean area of the cloacal protuberance in birds treated with T was significantly different before and after hormonal treatment (

Discussion

In this study, TH immunocytochemistry was used to investigate the potential effects of T in the regulation the CAergic innervation of the telencephalic areas of the SCS in adult female canaries. As previously reported, T stimulated song production and increased the volume of the song control nuclei, HVC and RA (e.g. Nottebohm, 1980). The masculinization of these behavioral and morphological features was however incomplete as attested by the fact that T-treated females sang simpler and shorter

Acknowledgements

This research was supported by grants from the NINDS (NS-35467) to GFB and JB and grants from the Belgian FRFC (2.4555.01), the French Community of Belgium (ARC 99/04–241), and the University of Liège (Fonds Spéciaux pour la Recherche) to JB. DA is research fellow with the FNRS.

References (89)

  • T.J. DeVoogd et al.

    Synaptogenesis and changes in synaptic morphology related to acquisitive new behavior

    Brain Res

    (1985)
  • D. Durstewitz et al.

    The dopaminergic innervation of the avian telencephalon

    Prog Neurobiol

    (1999)
  • M. Gahr et al.

    Testosterone-dependent increase of gap-junctions in HVC neurons of adult female canaries

    Brain Res

    (1996)
  • E. Hampson

    Variations in sex related cognitive abilities across the menstrual cycle

    Brain Cogn

    (1990)
  • S.J. Kelly et al.

    Gender differences in brain and behaviorhormonal and neural bases

    Pharmacol Biochem Behav

    (1999)
  • S. Leitner et al.

    Seasonal activation and inactivation of song motor memories in wild canaries is not reflected in neuroanatomical changes of forebrain song areas

    Horm Behav

    (2001)
  • D.L. Maney et al.

    Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem

    Neurosci Lett

    (2001)
  • F. Nottebohm

    Testosterone triggers growth of brain vocal control nuclei in adult female canaries

    Brain Res

    (1980)
  • F. Nottebohm et al.

    Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song

    Behav Neural Biol

    (1987)
  • S. Rasika et al.

    BDNF mediates the effects of testosterone on the survival of new neurons in an adult brain

    Neuron

    (1999)
  • A.G. Reznikov et al.

    Catecholamines in steroid-dependent brain development

    J Steroid Biochem Mol Biol

    (1995)
  • L.V. Riters et al.

    Sex differences in the densities of alpha 2-adrenergic receptors in the song control system, but not the medial preoptic nucleus in zebra finches

    J Chem Neuroanat

    (2002)
  • H. Sakaguchi et al.

    The acetylcholine and catecholamine contents in song control nuclei of zebra finch during song ontogeny

    Dev Brain Res

    (1989)
  • T.W. Troyer et al.

    Birdsongmodels and mechanisms

    Curr Opin Neurobiol

    (2001)
  • R. Weiler et al.

    Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine

    Brain Res Rev

    (2000)
  • D. Appeltants et al.

    The distribution of tyrosine hydroxylase in the canary braindemonstration of a specific and sexually dimorphic catecholaminergic innervation of the telencephalic song control nuclei

    Cell Tissue Res

    (2001)
  • D. Appeltants et al.

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

    Neuroreport

    (2002)
  • A.P. Arnold

    The passerine bird song system as a model in neuroendocrine research

    J Exp Zool

    (1990)
  • A.P. Arnold et al.

    Hormone concentrating cells in vocal control and other areas of the brain of the zebra finch (Poephila guttata)

    J Comp Neurol

    (1976)
  • T. Bailhache et al.

    The catecholaminergic system of the quail brainimmunocytochemical studies of dopamine β-hydroxylase and tyrosine hydroxylase

    J Comp Neurol

    (1993)
  • G.F. Ball

    Neurochemical specializations associated with vocal learning and production in songbirds and budgerigars

    Brain Behav Evol

    (1994)
  • G.F. Ball et al.

    Peptidergic delineations of nucleus interface reveal a sex difference in volume

    Neuroreport

    (1995)
  • G.F. Ball et al.

    Bird song

    Am Psychol

    (1998)
  • G.F. Ball

    Neuroendocrine basis of seasonal changes in vocal behavior among songbirds

  • J. Balthazart et al.

    Immunocytochemical localization of androgen receptors in the male song bird and quail brain

    J Comp Neurol

    (1992)
  • D.J. Bernard et al.

    Two histological markers reveal a similar photoperiodic differences in the volume of the high vocal center in male European starling

    J Comp Neurol

    (1995)
  • D.J. Bernard et al.

    Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starling

    Endocrinology

    (1999)
  • C. Beyer et al.

    Sex steroids and afferent inputtheir roles in brain sexual differentiation

    Annu Rev Physiol

    (1987)
  • S.W. Bottjer et al.

    Auditory and hormonal stimulation interact to produce neural growth in adult canaries

    J Neurobiol

    (1986)
  • S.W. Bottjer et al.

    Joint hormonal and sensory stimulation modulate neuronal number in adult canary brains

    J Neurobiol

    (1988)
  • S.W. Bottjer et al.

    Testosterone and the incidence of hormone target cells in song-control nuclei of adult canaries

    J Neurobiol

    (1991)
  • S.W. Bottjer

    The distribution of tyrosine hydroxylase in the brains of male and female zebra finches

    J Neurobiol

    (1993)
  • S.W. Bottjer et al.

    Sex differences in neuropeptide staining of song-control nuclei in zebra finch brains

    Brain Behav Evol

    (1997)
  • S.W. Bottjer et al.

    Circuits, hormones, and learningvocal behavior in songbirds

    J Neurobiol

    (1997)
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