Testosterone regulates birdsong in an anatomically specific manner

doi:10.1016/j.anbehav.2016.09.013

Animal Behaviour

Volume 124, February 2017, Pages 291-298

https://doi.org/10.1016/j.anbehav.2016.09.013 Get rights and content

Highlights

•
Many aspect of song behaviour are profoundly regulated by testosterone.
•
Testosterone has distinct effects on song based on where in the brain it acts.
•
Testosterone promotes the motivation to sing by acting in the preoptic area.
•
Testosterone enhances song quality by acting in the song control nucleus HVC.
•
LMAN lesions block testosterone-induced song masculinization in female canaries.

The functions of birdsong include attracting a mate and repelling competitors. It is therefore not surprising that, in males in the temperate zone especially, birdsong is often produced in the context of reproduction. Testosterone of gonadal origin increases during the reproductive phase of the annual cycle and can significantly influence song production as well as song development via effects on song crystallization (testosterone secretion at the time of sexual maturity is essential for full crystallization to occur). In males, testosterone of gonadal origin can exert its effects in the brain on song and other reproductive behaviour via its oestrogenic and androgenic metabolites. The widespread distribution of nuclear androgen receptors in the song system and the occurrence of oestrogen receptors in one key forebrain nucleus in certain species as well as the presence of both receptor types in the diencephalon and the midbrain raises questions as to where and how testosterone is exerting its myriad effects on song. By selectively implanting testosterone into specific brain regions of castrated male canaries, Serinus canaria, we have identified the medial preoptic area as a critical site for the induction of a generalized increase in motivation that includes the motivation to sing. Testosterone action in the forebrain song nucleus HVC in contrast increases song stereotypy. Canaries receiving testosterone in the preoptic area and HVC sing stereotypic songs but at a much lower amplitude, indicating that testosterone's effects on amplitude are regulated elsewhere in the brain or the periphery. The lateral part of the magnocellular nucleus anterior nidopallium (LMAN) is a song nucleus that expresses a high density of androgen receptors and plays a role as a song variability generator during song learning. When adult female canaries are treated with testosterone, their song becomes more complex. Lesions to LMAN attenuate these effects on adult behavioural change, suggesting that testosterone may act in LMAN during song ontogeny to modulate changes associated with song crystallization. These anatomically specific effects illustrate how a single hormone can coordinate changes in many aspects of a complex behaviour to facilitate successful reproduction.

Section snippets

Steroid hormones and the regulation of birdsong

Communication behaviour occurs in a particular social and environmental context (Hauser, 1996, Wiley, 2015). It is often desirable from a fitness perspective for individuals to relay information to conspecifics about a wide variety of stimuli in the environment such as the availability of food, the presence of predators or one's motivation to mate (Hauser, 1996, Owings and Morton, 1998). The appropriate signals must therefore be coordinated with the occurrence of a variety of other exogenous

The song control system and the expression of androgen and oestrogen receptors

When studies on hormonal regulation of song were first conducted, it was discovered that song behaviour is mediated by a neural system of discrete brain nuclei (Nottebohm, Stokes, & Leonard, 1976; for a review of these initial studies, see; Nottebohm, 1980). This neural circuitry has many attributes that make it unique to members of the songbird suborder Passeres (e.g. Ball, 1994, Kroodsma and Konishi, 1991), although it is clearly derived from ancestral circuits still observable in extant

Anatomical location of testosterone action on birdsong

To address the basic question of what the consequences of testosterone action are in the variety of androgen-sensitive nuclei that might be involved in the regulation of song, a strategy of selectively implanting testosterone in brain nuclei was adopted. These studies utilized canaries, a songbird that exhibits robust seasonal changes in song behaviour that positively correlate with increases in circulating testosterone (Leitner et al., 2001, Voigt and Leitner, 2008). Implanting testosterone in

Testosterone in the anterior forebrain pathway nucleus LMAN

The brain nucleus LMAN is a component of the anterior forebrain basal–ganglia pathway of the song system that is directly implicated in song development in juvenile male zebra finches (Aronov et al., 2008, Fee and Goldberg, 2011, Scharff and Nottebohm, 1991). Converging evidence from multiple research teams indicated that LMAN acts as an endogenous variability generator that serves to guide the trajectory of vocal motor learning in juvenile males (Kao et al., 2005, Olveczky et al., 2005,

Discussion

These findings illustrate that the hormonal regulation of song requires that a number of different components of song behaviour are simultaneously modulated by testosterone acting in distinct brain areas. It has been noted previously that song is a hormone-regulated behaviour that almost assuredly is regulated in multiple nonredundant ways given the distribution of relevant brain nuclei expressing receptors for the key regulatory steroid hormones: androgens and oestrogens (Arnold, 1981). The

Acknowledgments

This paper is dedicated to Peter Marler, the maestro of birdsong. For two of us (G.F.B. and J.B.), he was an inspirational scientist, mentor and friend. For B.A. and M.L.R., he is the grandfather of their academic tradition. Peter had a great career but we shall miss his advice, perspective and wisdom. Some of the work reviewed here was supported by a grant from the National Institutes of Health NIH/NINDS R01 NS35467 and by BELSPO grant SSTC PAI P7/17.

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Special Issue: Mechanisms & FunctionTestosterone regulates birdsong in an anatomically specific manner

Highlights

Section snippets

Steroid hormones and the regulation of birdsong

The song control system and the expression of androgen and oestrogen receptors

Anatomical location of testosterone action on birdsong

Testosterone in the anterior forebrain pathway nucleus LMAN

Discussion

Acknowledgments

Frontiers in Neuroendocrinology

Behavioural Brain Research

Advances in the Study of Behavior

Neuroscience

Animal Behaviour

General and Comparative Endocrinology

General and Comparative Endocrinology

Behavioral and Neural Biology

Hormones and Behavior

Hormones and Behavior

Hormones and Behavior

Animal Behaviour

Hormones and Behavior

Animal Behaviour

Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate

Proceedings of the National Academy of Sciences of the United States of America

Pleiotropic control by testosterone of a learned vocal behavior and its underlying neuroplasticity

eNeuro

The effects of castration and androgen replacement on song courtship, and aggression in zebra finches (Poephila guttata)

Journal of Experimental Zoology

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

American Zoologist

Gonadal steroid induction of structural sex differences in the central nervous system

Annual Review of Neuroscience

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

Journal of Comparative Neurology

A specialized forebrain circuit for vocal babbling in the juvenile songbird

Science

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

Brain Behavior and Evolution

Seasonal plasticity in the song control system: Multiple brain sites of steroid hormone action and the importance of variation in song behavior

Annals of the New York Academy of Sciences

Individual variation and the endocrine regulation of behaviour and physiology in birds: A cellular/molecular perspective

Philosophical Transactions of the Royal Society B: Biological Sciences

Sex differences in brain and behavior and the neuroendocrine control of the motivation to sing

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

Journal of Comparative Neurology

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

Endocrinology

Castration and antisteroid treatment impair vocal learning in male zebra finches

Journal of Neurobiology

Forebrain lesions disrupt development but not maintenance of song in passerine birds

Science

Translating birdsong: Songbirds as a model for basic and applied medical research

Annual Review of Neuroscience

Act locally and think globally: Intracerebral testosterone implants induce seasonal-like growth of adult avian song control circuits

Proceedings of the National Academy of Sciences of the United States of America

Bird song: Biological themes and variations

How sleep affects the developmental learning of bird song

Nature

The songbird brain in comparative perspective

The songbird as a model for the generation and learning of complex sequential behaviors

ILAR Journal

Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens

Journal of Neurobiology

Special Issue: Mechanisms & Function
Testosterone regulates birdsong in an anatomically specific manner