Special Issue: Mechanisms & FunctionTestosterone regulates birdsong in an anatomically specific manner
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.
References (75)
- et al.
Neuroendocrinology of song behavior and avian brain plasticity: Multiple sites of action of sex steroid hormones
Frontiers in Neuroendocrinology
(2002) - et al.
Anterior forebrain pathway is needed for stable song expression in adult male white-crowned sparrows (Zonotrichia leucophrys)
Behavioural Brain Research
(1998) Vocal fighting and flirting: The functions of birdsong
Understanding the complex song of the European starling: An integrated ethological approach
Advances in the Study of Behavior
(1997)- et al.
A hypothesis for basal ganglia-dependent reinforcement learning in the songbird
Neuroscience
(2011) - et al.
A suboscine bird (eastern phoebe, Sayornis phoebe) develops normal song without auditory feedback
Animal Behaviour
(1991) - et al.
High-affinity androgen binding proteins in synrigeal tissues of songbirds
General and Comparative Endocrinology
(1979) - et al.
Reversing song behavior phenotype: Testosterone driven induction of singing and measures of song quality in adult male and female canaries (Serinus canaria)
General and Comparative Endocrinology
(2015) - et al.
Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei
Behavioral and Neural Biology
(1986) - et al.
Reverse engineering the lordosis behavior circuit
Hormones and Behavior
(2008)
Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris)
Hormones and Behavior
Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris)
Hormones and Behavior
Variation in song system anatomy and androgen levels does not correspond to song characteristics in a tropical songbird
Animal Behaviour
Seasonality in song behaviour revisited: Seasonal and annual variants and invariants in the song of the domesticated canary (Serinus canaria)
Hormones and Behavior
Photoperiod and tutor access affect the process of vocal learning
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
Cited by (32)
Male Cope's gray treefrogs (Hyla chrysoscelis) in amplexus have elevated and correlated steroid hormones compared to solitary males
2024, General and Comparative EndocrinologySocial regulation of androgenic hormones and gestural display behavior in a tropical frog
2023, Hormones and BehaviorPhotoperiodic control of singing behavior and reproductive physiology in male Fife fancy canaries
2022, Hormones and BehaviorSong learning and plasticity in songbirds
2021, Current Opinion in Neurobiology