Alward, B. A.; Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, United States, Department of Psychology, University of Maryland, College ParkMD, United States
Rouse, M. L.; Jr., Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, United States, Department of Reproductive Medicine, University of California – San Diego, La Jolla, CA, United States
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Ball, G. F.; Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, United States, Department of Psychology, University of Maryland, College ParkMD, United States
Language :
English
Title :
Testosterone regulates birdsong in an anatomically specific manner
Publication date :
2017
Journal title :
Animal Behaviour
ISSN :
0003-3472
eISSN :
1095-8282
Publisher :
Academic Press
Volume :
124
Pages :
291-298
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
Grant from the National Institutes of Health NIH/NINDS R01 NS35467; BELSPO grant SSTC PAI P7/17
Funders :
NIH - National Institutes of Health BELSPO - Politique scientifique fédérale
Alward, B.A., Balthazart, J., Ball, G.F., 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 110 (2013), 19573–19578.
Alward, B.A., Madison, F.N., Parker, S.E., Balthazart, J., Ball, G.F., Pleiotropic control by testosterone of a learned vocal behavior and its underlying neuroplasticity. eNeuro, 3, 2016 0145-15.2016.
Arnold, A.P., The effects of castration and androgen replacement on song courtship, and aggression in zebra finches (Poephila guttata). Journal of Experimental Zoology 191 (1975), 309–326.
Arnold, A.P., Logical levels of steroid hormone action in the control of vertebrate behavior. American Zoologist 21 (1981), 233–242.
Arnold, A.P., Gorski, R.A., Gonadal steroid induction of structural sex differences in the central nervous system. Annual Review of Neuroscience 7 (1984), 413–442.
Arnold, A.P., Nottebohm, F., Pfaff, D.W., Hormone concentrating cells in vocal control areas of the brain of the zebra finch (Poephila guttata). Journal of Comparative Neurology 165 (1976), 487–512.
Aronov, D., Andalman, A.S., Fee, M.S., A specialized forebrain circuit for vocal babbling in the juvenile songbird. Science 320 (2008), 630–634.
Ball, G.F., Neurochemical specializations associated with vocal learning and production in songbirds and budgerigars. Brain Behavior and Evolution 44 (1994), 234–246.
Ball, G.F., Auger, C.J., Bernard, D.J., Charlier, T.D., Sartor, J.J., Riters, L.V., et al. 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 1016 (2004), 586–610.
Ball, G.F., Balthazart, J., 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 363 (2008), 1699–1710.
Ball, G.F., Riters, L.V., Balthazart, J., Neuroendocrinology of song behavior and avian brain plasticity: Multiple sites of action of sex steroid hormones. Frontiers in Neuroendocrinology 23 (2002), 137–178.
Ball, G.F., Riters, L.V., MacDougall-Shackleton, S.A., Balthazart, J., Sex differences in brain and behavior and the neuroendocrine control of the motivation to sing. Zeigler, H.P., Marler, P., (eds.) Neuroscience of birdsong, 2008, Cambridge University Press, Cambridge, U.K., 320–331.
Balthazart, J., Foidart, A., Wilson, E.M., Ball, G.F., Immunocytochemical localization of androgen receptors in the male songbird and quail brain. Journal of Comparative Neurology 317 (1992), 407–420.
Benton, S., Nelson, D.A., Marler, P., DeVoogd, T.J., Anterior forebrain pathway is needed for stable song expression in adult male white-crowned sparrows (Zonotrichia leucophrys). Behavioural Brain Research 96 (1998), 135–150.
Bernard, D.J., Bentley, G.E., Balthazart, J., Turek, F.W., Ball, G.F., Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinology 140 (1999), 4633–4643.
Bottjer, S.W., Hewer, S.J., Castration and antisteroid treatment impair vocal learning in male zebra finches. Journal of Neurobiology 23 (1992), 337–353.
Bottjer, S.W., Miesner, E.A., Arnold, A.P., Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224 (1984), 901–903.
Brainard, M.S., Doupe, A.J., Translating birdsong: Songbirds as a model for basic and applied medical research. Annual Review of Neuroscience 36 (2013), 489–517.
Brenowitz, E.A., Lent, K., 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 99 (2002), 12421–12426.
Catchpole, C.K., Slater, P.J.B., Bird song: Biological themes and variations. 2008, Cambridge University Press, Cambridge, U.K.
Collins, S., Vocal fighting and flirting: The functions of birdsong. Marler, P., Slabbekoorn, H., (eds.) Nature's music: The science of birdsong, 2004, Elsevier, Amsterdam, The Netherlands, 39–79.
Derégnaucourt, S., Mitra, P.P., Fehér, O., Pytte, C., Tchernichovski, O., How sleep affects the developmental learning of bird song. Nature 433 (2005), 710–716.
Eens, M., Understanding the complex song of the European starling: An integrated ethological approach. Advances in the Study of Behavior 26 (1997), 355–434.
Farries, M.A., Perkel, D.J., The songbird brain in comparative perspective. Zeigler, H.P., Marler, P., (eds.) Neuroscience of birdsong, 2008, Cambridge University Press, Cambridge, U.K., 63–71.
Fee, M.S., Goldberg, J.H., A hypothesis for basal ganglia-dependent reinforcement learning in the songbird. Neuroscience 198 (2011), 152–170.
Fee, M.S., Scharf, C., The songbird as a model for the generation and learning of complex sequential behaviors. ILAR Journal 51 (2010), 362–377.
Fusani, L., Van't Hof, T., Hutchison, J.B., Gahr, M., Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens. Journal of Neurobiology 43 (2000), 254–268.
Gahr, M., Localization of androgen receptors and estrogen receptors in the same cells of the songbird brain. Proceedings of the National Academy of Sciences of the United States of America 87 (1990), 9445–9448.
Harding, C.F., Hormonal modulation of singing behavior: Methodology and principles of hormone action. Zeigler, H.P., Marler, P., (eds.) Neuroscience of birdsong, 2008, Cambridge University Press, Cambridge, U.K., 305–319.
Hauser, M.D., The evolution of communication. 1996, MIT Press, Cambridge, MA.
Kao, M.H., Doupe, A.J., Brainard, M.S., Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song. Nature 433 (2005), 638–643.
Kelley, D.B., Pfaff, D.W., Generalizations from comparative studies on neuroanatomical and endocrine mechanisms of sexual behaviour. Hutchison, J.B., (eds.) Biological determinants of sexual behaviour, 1978, J. Wiley, Chichester, U.K., 225–254.
Korsia, S., Bottjer, S.W., Chronic testosterone treatment impairs vocal learning in male zebra finches during a restricted period of development. Journal of Neuroscience 11 (1991), 2362–2371.
Kroodsma, D.E., Vocal behavior., 2nd ed. Podulka, S., Rohrbaugh, R.W. Jr., Bonney, R., (eds.) Handbook of bird biology, Vol. 7, 2004, Princeton University Press, Princeton, NJ, 1–98.
Kroodsma, D.E., Byers, B.E., The functions of bird song. American Zoologist 31 (1991), 318–328.
Kroodsma, D., Konishi, M., A suboscine bird (eastern phoebe, Sayornis phoebe) develops normal song without auditory feedback. Animal Behaviour 42 (1991), 477–487.
Lee, A.W., Pfaff, D.W., Hormone effects on specific and global brain functions. Journal of Physiological Sciences 58 (2008), 213–220.
Leitner, S., Voigt, C., Gahr, M., Seasonal changes in the song pattern of the non-domesticated canary (Serinus canaria), a field study. Behaviour 138 (2001), 885–904.
Lieberburg, I., Nottebohm, F., High-affinity androgen binding proteins in synrigeal tissues of songbirds. General and Comparative Endocrinology 37 (1979), 286–293.
Liu, W.-C., Wada, K., Jarvis, E.D., Nottebohm, F., Rudimentary substrates for vocal learning in a suboscine. Nature Communications, 4, 2013, 2082, 10.1038/ncomms3082.
Madison, F.N., Rouse, M.L. Jr., Balthazart, J., Ball, G.F., 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 215 (2015), 61–75.
Marler, P., Sensitive periods and the roles of specific and general sensory stimulation in birdsong learning. Rauschecker, J.P., Marler, P., (eds.) Imprinting and cortical plasticity, 1987, J. Wiley, New York, NY, 99–135.
Marler, P., Peters, S., Ball, G.F., Dufty, A.M., Wingfield, J.C., The role of sex steroids in the acquisition and production of birdsong. Nature 336 (1988), 770–772.
McEwen, B.S., Biegon, A., Fischette, C.T., Luine, V.N., Parsons, B., Rainbow, T.C., Toward a neurochemical basis of steroid action. Martini, L., Ganong, W.F., (eds.) Frontiers in neuroendocrinology, 1984, Raven Press, New York, NY, 153–176.
McEwen, B.S., Gray, J.D., Nasca, C., 60 years of neuroendocrinology: Redefining neuroendocrinology: Stress, sex and cognitive and emotional regulation. Journal of Endocrinology 226 (2015), T67–T83.
Meitzen, J., Moore, I.T., Lent, K., Brenowitz, E.A., Perkel, D.J., Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. Journal of Neuroscience 27 (2007), 12045–12057.
Metzdorf, R., Gahr, M., Fusani, L., Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds. Journal of Comparative Neurology 407 (1999), 115–129.
Nottebohm, F., Brain pathways for vocal learning in birds: A review of the first 10 years. Sprague, J.M., Epstein, A.N., (eds.) Progress in psychobiology and physiological psychology, Vol. 9, 1980, Academic Press, New York, NY, 85–214.
Nottebohm, F., Nottebohm, M.E., Crane, L., Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. Behavioral and Neural Biology 46 (1986), 445–471.
Nottebohm, F., Stokes, T.M., Leonard, C.M., Central control of song in the canary, Serinus canarius. Journal of Comparative Neurology 165 (1976), 457–486.
Numan, M., Neurobiology of social behavior. Toward an understanding of the prosocial and antisocial brain. 2014, Elsevier, Amsterdam, The Netherlands.
Olveczky, B.P., Andalman, A.S., Fee, M.S., Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biology, 3, 2005, e153.
Owings, D.H., Morton, E.S., Animal vocal communication: A new approach. 1998, Cambridge University Press, New York, NY.
Pesch, A., Güttinger, H.R., Der Gesang des weiblichen Kanarienvogels. Journal fuer Ornithologie 126 (1985), 108–110.
Pfaff, D.W., Kow, L.M., Loose, M.D., Flanagan-Cato, L.M., Reverse engineering the lordosis behavior circuit. Hormones and Behavior 54 (2008), 347–354.
Pröve, E., Der Einfluss von Kastration und Testosteronsubstitution auf das Verhalten manlicher Zebrafinken. Journal fuer Ornithologie 115 (1974), 338–347.
Riters, L.V., Alger, S.J., Neuroanatomical evidence for indirect connections between the medial preoptic nucleus and the song control system: Possible neural substrates for sexually motivated song. Cell & Tissue Research 316 (2004), 35–44.
Riters, L.V., Ball, G.F., Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris). Hormones and Behavior 36 (1999), 276–286.
Riters, L.V., Eens, M., Pinxten, R., Duffy, D.L., Balthazart, J., Ball, G.F., Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Hormones and Behavior 38 (2000), 250–261.
Rouse, M.L. Jr., Ball, G.F., Lesions targeted to the anterior forebrain disrupt vocal variability associated with testosterone-induced sensorimotor song development in adult female canaries, Serinus canaria. Developmental Neurobiology 76 (2016), 3–18.
Sakata, J.T., Vehrencamp, S.L., Integrating perspectives on vocal performance and consistency. Journal of Experimental Biology 215 (2012), 201–209.
Scharff, C., Nottebohm, F., A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: Implications for vocal learning. Journal of Neuroscience 11 (1991), 2896–2913.
Schlinger, B.A., Brenowitz, E.A., Neural and hormonal control of birdsong. Pfaff, D.W., Arnold, A.P., Etgen, A.M., Fahrbach, S.E., Rubin, R.T., (eds.) Hormones, brain and behavior, 2009, Academic Press, San Diego, CA, 898–941.
Schwabl, H., Dowling, J., Baldassarre, D.T., Gahr, M., Lindsay, W.R., Webster, M.S., Variation in song system anatomy and androgen levels does not correspond to song characteristics in a tropical songbird. Animal Behaviour 104 (2015), 39–50.
Searcy, W.A., Andersson, M., Sexual selection and the evolution of song. Annual Review of Ecology and Systematics 17 (1986), 507–533.
Tchernichovski, O., Mitra, P.P., Lints, T., Nottebohm, F., Dynamics of vocal imitation process: How a zebra finch learns its song. Science 291 (2001), 2564–2569.
Thompson, J.A., Basista, M.J., Wu, W., Bertram, R., Johnson, F., Dual pre-motor contribution to songbird syllable variation. Journal of Neuroscience 31 (2011), 322–330.
Vallet, E., Kreutzer, M., Gahr, M., Testosterone induces sexual release quality in the song of female canaries. Ethology 102 (1996), 617–628.
Voigt, C., Leitner, S., Seasonality in song behaviour revisited: Seasonal and annual variants and invariants in the song of the domesticated canary (Serinus canaria). Hormones and Behavior 54 (2008), 373–378.
Whaling, C.S., Nelson, D.A., Marler, P., Testosterone-induced shortening of the storage phase of song development in birds interferes with vocal learning. Developmental Psychobiology 28 (1995), 367–376.
Whaling, C.S., Soha, J.A., Nelson, D.A., Lasley, B., Marler, P., Photoperiod and tutor access affect the process of vocal learning. Animal Behaviour 56 (1998), 1075–1082.
White, G., The natural history and antiquities of Selbourne. 1789, Chiswick Press, London, U.K.
Wild, J.M., Goller, F., Suthers, R.A., Inspiratory muscle activity during bird song. Journal of Neurobiology 36 (1998), 441–453.
Wiley, R.H., Noise matters: The evolution of communication. 2015, Harvard University Press, Cambridge, MA.
Wingfield, J.C., Hegner, R.E., Dufty, A.M., Ball, G.F., The ‘challenge hypothesis’: Theoretical implications for patterns of testosterone secretion, mating systems and breedings strategies. American Naturalist 136 (1990), 829–846.