Neuroendocrinology of Song Behavior and Avian Brain Plasticity: Multiple Sites of Action of Sex Steroid Hormones

doi:10.1006/frne.2002.0230

Frontiers in Neuroendocrinology

Volume 23, Issue 2, April 2002, Pages 137-178

https://doi.org/10.1006/frne.2002.0230 Get rights and content

Abstract

Seasonal changes in the brain of songbirds are one of the most dramatic examples of naturally occuring neuroplasticity that have been described in any vertebrate species. In males of temperate-zone songbird species, the volumes of several telencephalic nuclei that control song behavior are significantly larger in the spring than in the fall. These increases in volume are correlated with high rates of singing and high concentrations of testosterone in the plasma. Several song nuclei express either androgen receptors or estrogen receptors, therefore it is possible that testosterone acting via estrogenic or androgenic metabolites regulates song behavior by seasonally modulating the morphology of these song control nuclei. However, the causal links among these variables have not been established. Dissociations among high concentrations of testosterone, enlarged song nuclei, and high rates of singing behavior have been observed. Singing behavior itself can promote cellular changes associated with increases in the volume of the song control nuclei. Also, testosterone may stimulate song behavior by acting in brain regions outside of the song control system such as in the preoptic area or in catecholamine cell groups in the brainstem. Thus testosterone effects on neuroplasticity in the song system may be indirect in that behavioral activity stimulated by testosterone acting in sites that promote male sexual behavior could in turn promote morphological changes in the song system.

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The vocal control nucleus HVC in songbirds has emerged as a widespread model system to study adult brain plasticity in response to changes in the hormonal and social environment. I review here studies completed in my laboratory during the last decade that concern two aspects of this plasticity: changes in aggregations of extracellular matrix components surrounding the soma of inhibitory parvalbumin-positive neurons called perineuronal nets (PNN) and the production/incorporation of new neurons. Both features are modulated by the season, age, sex and endocrine status of the birds in correlation with changes in song structure and stability. Causal studies have also investigated the role of PNN and of new neurons in the control of song. Dissolving PNN with chondroitinase sulfate, a specific enzyme applied directly on HVC or depletion of new neurons by focalized X-ray irradiation both affected song structure but the amplitude of changes was limited and deserves further investigations.
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Monogamous, pair-bonded animals coordinate intra-pair behavior for spatially separated challenges including territorial defense and nest attendance. Paired California mice, a monogamous, territorial and biparental species, approach intruders together or separately, but often express behavioral convergence across intruder challenges. To gain a more systems-wide perspective of potential mechanisms contributing to behavioral convergence across two conspecific intruder challenges, we conducted an exploratory study correlating behavior and receptor mRNA (Days 10 and 17 post-pairing). We examined associations between convergence variability in pair time for intruder-oriented behaviors with a pair mRNA index for oxytocin (OXTR), androgen (AR), and estrogen alpha (ERα) receptors within the medial amygdala (MeA) and the anterior olfactory nucleus (AON), brain regions associated with social behavior. An intruder behavior index revealed a bimodal distribution of intruder-related behaviors in Challenge 1 and a unimodal distribution in Challenge 2, suggesting population behavioral convergence, but no significant correlations with neuroendocrine measures. However, OXTR, AR, and ERα mRNA in the MeA were positively associated with convergence in individual intruder-related behaviors, suggesting multiple mechanisms may influence convergence. Mice could also occupy the nest during intruder challenges and convergence in nest attendance was positively correlated with MeA OXTR. At an individual level, nest attendance was positively associated with MeA ERα. Vocalizations were positively associated with AR and ERα mRNA. No positive associations were found in the AON. Overall, neuroendocrine receptors were implicated in convergence of a monogamous pair’s defense behavior, highlighting the potential importance of the MeA as part of a circuit underlying convergence.
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Citation Excerpt :
Song functions to attract potential mates, defend territories from rivals, and maintain flock cohesion [6]. Many seasonally breeding male songbirds sing at high rates in the spring as compared to the other seasons [7]. Seasonal changes in song output are positively correlated with extensive changes in the neuroendocrine control of reproduction, and GnRH1 plasticity in particular [4,7].
Social cues modulate the neuroendocrine control of reproduction. However, the neural systems involved in the integration of social cues are not well described. Gonadotropin-releasing hormone 1 (GnRH1) cells in the preoptic area (POA) are the final common node that links the brain with peripheral reproductive physiology. These experiments investigated whether induction of the immediate early gene, EGR1, in anatomically localized GnRH1 cell populations in Border canaries is regulated by the social environment. First, we characterized behavioral modifications in singing behavior and found males paired with a female for 2 weeks significantly reduced many aspects of singing behavior. However, paired males had a significantly higher percentage of GnRH1 cells co-labeled with EGR1. The second experiment manipulated the social environment by pairing males and females in mixed sex dyads, same sex dyads or housed birds in isolation. Only when birds are paired in mixed sex dyads was there a significantly greater percentage of GnRH1 cells expressing EGR1 cells. Increased GnRH1-EGR1 co-expression was localized to the rostral POA. These data reveal that discrete GnRH1 cells are involved in the neural integration of specific social cues and support the hypothesis that the POA exhibits functional topography related to courtship and sexual behaviors.
Sex differences in seasonal brain plasticity and the neuroendocrine regulation of vocal behavior in songbirds
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Birdsong is controlled in part by a discrete network of interconnected brain nuclei regulated in turn by steroid hormones and environmental stimuli. This complex interaction results in neural changes that occur seasonally as the environment varies (e.g., photoperiod, food/water availability, etc.). Variation in environment, vocal behavior, and neuroendocrine control has been primarily studied in male songbirds in both laboratory studies of captive birds and field studies of wild caught birds. The bias toward studying seasonality in the neuroendocrine regulation of song in male birds comes from a historic focus on sexually selected male behaviors. In fact, given that male song is often loud and accompanied by somewhat extravagant courtship behaviors, female song has long been overlooked. To compound this bias, the primary model songbird species for studies in the lab, zebra finches (Taeniopygia guttata) and canaries (Serinus canaria), exhibit little or no female song. Therefore, understanding the degree of variation and neuroendocrine control of seasonality in female songbirds is a major gap in our knowledge. In this review, we discuss the importance of studying sex differences in seasonal plasticity and the song control system. Specifically, we discuss sex differences in 1) the neuroanatomy of the song control system, 2) the distribution of receptors for androgens and estrogens and 3) the seasonal neuroplasticity of the hypothalamo-pituitary-gonadal axis as well as in the neural and cellular mechanisms mediating song system changes. We also discuss how these neuroendocrine mechanisms drive sex differences in seasonal behavior. Finally, we highlight specific gaps in our knowledge and suggest experiments critical for filling these gaps.
Where to from here? Perspectives on steroid-induced and naturally-occurring singing in female songbirds
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In many species, male and female animals differ in the types and frequency of particular behaviors (e.g. reproductive behavior, parental behavior, etc.). These differences in behavior are quite often related to the neural and hormonal control of said behaviors. In the temperate zone it is commonly stated that male songbirds sing much more frequently and with much greater quality compared to their female counterparts. However, recent evidence has called these claims into question (Odom et al., 2014; Price et al., 2008; Webb et al., 2016). That said, neuroendocrine studies of song behavior have primarily focused on male birds and relatively little work has been done exclusively or comparatively with female songbirds. What we do know, however, is that there is wide variability in the vocal ability and capacity of female songbirds and that there is a developmental link between the hormonal milieu and neuro-social development that facilitate these behavioral phenotypes. Both testosterone and estradiol have been demonstrated to play pivotal roles in behavioral and neural differentiation of male and female song behavior profiles. Here we review a brief history of empirical investigation into steroid regulation of song in female birds, including the pattern of song activation, constraints on the ability of testosterone to induce singing, and the role of the anterior forebrain in supporting song learning. We conclude with a brief analysis of a major gap in the field's knowledge regarding naturally occurring female song and the neuroendocrine underpinnings of a socially salient learned behavior ripe for systematic investigation.
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^☆: Address correspondence and reprint requests to Gregory F. Ball, Department of Psychological and Brain Sciences, Johns Hopkins University, 3400 N. Charles Street, Baltimore, MD 21218. Fax: (410) 516-6008. E-mail: [email protected].

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Regular ArticleNeuroendocrinology of Song Behavior and Avian Brain Plasticity: Multiple Sites of Action of Sex Steroid Hormones☆

Abstract

Horm Behav

J Chem Neuroanat

Anim Behav

Psychoneuroendocrinology

Brain Res

Brain Res

Brain Res Bull

Trends Endocrinol Metab

J Chem Neuroanat

J Steroid Biochem Mol Biol

Brain Res

Brain Res

Pharmacol Biochem Behav

Behav Brain Res

Gen Comp Endocrinol

Brain Res

Horm Behav

Brain Res.

Semin Neurosci

Brain Res

Horm Behav

Adv Study Anim Behav

Neuroscience

Brain Res

Trends Neurosci

Brain Res Bull

Anim Behav

Distribution and developmental change in [3H]MK-801 binding within zebra finch song nuclei

J Neurobiol

Early isolation from conspecific song does not affect the normal developmental decline of N-methyl-d-aspartate receptor binding in an avian song nucleus

J Neurobiol

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

Cell Tissue Res

The effects of castration and androgen replacement on song courtship, and aggression in zebra finches

J Exp Zool

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

J Comp Neurol

Sexual difference in pattern of hormone accumulation in the brain of a song bird

Science

Logical levels of steroid hormone action in the control of vertebrate behavior

Am Zool

The passerine bird song system as a model in neuroendocrine research

J Exp Zool

Developmental plasticity in neural circuits controlling birdsong: Sexual differentiation and the neural basis of learning

J Neurobiol

Immunohistochemical localization of neuropeptides in the vocal control regions of two songbird species

J Comp Neurol

Chemical neuroanatomical studies of the steroid-sensitive songbird vocal control system: A comparative approach

Steroid modulation of muscarinic cholinergic and alpha2-adrenergic receptor density in the nucleus intercollicularis of the Japanese quail

Eur J Neurosci

Muscarinic cholinergic receptors in the songbird and quail brain: A quantitative autoradiographic study

J Comp Neurol

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

Brain Behav Evol

Peptidergic delineations of nucleus interface reveal a sex difference in volume

NeuroReport

How should brain nuclei be delineated? They don't need to be!

Trends Neurosci

Bird song

Am Psych

Neuroendocrine basis of seasonal changes in vocal behavior among songbirds

Steroid sensitive sites in the avian brain: Does the distribution of the estrogen receptor alpha and beta types provide insight into their function?

Brain Behav Evol

Steroid metabolism and the activation of social behavior

Immunocytochemical localization of androgen receptors in the male songbird and quail brain

J Comp Neurol

Regular Article
Neuroendocrinology of Song Behavior and Avian Brain Plasticity: Multiple Sites of Action of Sex Steroid Hormones☆

Distribution and developmental change in [³H]MK-801 binding within zebra finch song nuclei