Birdsong for neurobiologists

Song is a stereotyped behavior, yet its development depends on sensory feedback and learning. Early bird fanciers recognized that young birds must have a good tutor to become a good singer. They also knew that birds could be bred for more elaborate songs, as exemplified by different breeds of canaries selected for different ways of singing. Thus, variations in song between individuals and between species contain both heritable and experiential components. The study of the experiential component has shown that the nature and timing of auditory experience play an important role in shaping the outcome of song development. The ability of a bird to modify song in adulthood has drawn special attention because it implies neural plasticity in the adult brain. The discovery of the brain areas for the control of song has brought birdsong from the purely behavioral level of analysis to the interface between behavior and neurobiology. The song control system shows al I of the developmental events that attract much current research, such as neuronal growth, death, and migration, the specificity of neuronal connections, and the waiting compartment. Furthermore, sex steroids control some of these ontogenetic events as well as the expression of song and its neural substrates in adulthood. The main aim of this article is to review current research dealing with these topics.

[1]  M. Konishi,et al.  A critical period for estrogen action on neurons of the song control system in the zebra finch. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[2]  M. Konishi The role of auditory feedback in the control of vocalization in the white-crowned sparrow. , 1965, Zeitschrift fur Tierpsychologie.

[3]  A. Arnold,et al.  Ontogeny of brain nuclei controlling song learning and behavior in zebra finches , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  M. Gahr,et al.  Immunocytochemical localization of estrogen-binding neurons in the songbird brain , 1987, Brain Research.

[5]  D Margoliash,et al.  Preference for autogenous song by auditory neurons in a song system nucleus of the white-crowned sparrow , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  F. Nottebohm From bird song to neurogenesis. , 1989, Scientific American.

[7]  Klaus Immelmann,et al.  Sexual and Other Long-Term Aspects of Imprinting in Birds and Other Species , 1972 .

[8]  F. Nottebohm,et al.  Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. , 1986, Behavioral and neural biology.

[9]  L. A. Eales Do zebra finch males that have been raised by another species still tend to select a conspecific song tutor? , 1987, Animal Behaviour.

[10]  M. Konishi,et al.  Androgen increases protein synthesis within the avian brain vocal control system , 1981, Brain Research.

[11]  F. Nottebohm A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. , 1981, Science.

[12]  F. Nottebohm Neuronal Replacement in Adulthood , 1985, Annals of the New York Academy of Sciences.

[13]  E. Nordeen,et al.  Estrogen establishes sex differences in androgen accumulation in zebra finch brain , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  M. Konishi,et al.  Birdsong: from behavior to neuron. , 1985, Annual review of neuroscience.

[15]  R. Clower,et al.  Song-related brain regions in the red-winged blackbird are affected by sex and season but not repertoire size. , 1989, Journal of neurobiology.

[16]  B. McEwen Sexual differentiation of the brain , 1981, Nature.

[17]  J. S. McCasland,et al.  Neuronal control of bird song production , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  J. Wingfield,et al.  Sex differences in plasma concentrations of steroids during the sensitive period for brain differentiation in the zebra finch. , 1984, The Journal of endocrinology.

[19]  Donald E. Kroodsma,et al.  Vocal Virtuosity in the Brown Thrasher , 1977 .

[20]  W. Thorpe,et al.  The Process of Song-Learning in the Chaffinch as Studied by Means of the Sound Spectrograph , 1954, Nature.

[21]  M. Gurney Behavioral correlates of sexual differentiation in the zebra finch song system , 1982, Brain Research.

[22]  A. Gaunt An hypothesis concerning the relationship of syringeal structure to vocal abilities , 1983 .

[23]  S. Bottjer,et al.  Auditory and hormonal stimulation interact to produce neural growth in adult canaries. , 1986, Journal of neurobiology.

[24]  F. Nottebohm,et al.  Effect of testosterone on input received by an identified neuron type of the canary song system: a Golgi/electron microscopy/degeneration study , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  D. Margoliash Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  F. Nottebohm,et al.  Synaptogenesis and changes in synaptic morphology related to acquisition of a new behavior , 1985, Brain Research.

[27]  A. Arnold,et al.  Forebrain lesions disrupt development but not maintenance of song in passerine birds. , 1984, Science.

[28]  J. Wingfield,et al.  Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song. , 1987, Behavioral and neural biology.

[29]  P. Marler,et al.  Selective Vocal Learning in a Sparrow , 1977, Science.

[30]  A. Arnold,et al.  Sexual dimorphism in vocal control areas of the songbird brain. , 1976, Science.

[31]  P. Marler,et al.  Sensitive periods for song acquisition from tape recordings and live tutors in the swamp sparrow , 2010 .

[32]  P. Marler,et al.  Correlations between song acquisition, song production, and plasma levels of testosterone and estradiol in sparrows. , 1987, Journal of neurobiology.

[33]  F. Nottebohm,et al.  Projections of a telencephalic auditory nucleus– field L–in the canary , 1979, The Journal of comparative neurology.

[34]  N. Saito 5. The Control of Vocalization in Birds , 1983 .

[35]  Masakazu Konishi,et al.  The Role of Auditory Feedback in the Vocal Behavior of the Domestic Fowl1 , 1963, Zeitschrift für Tierpsychologie.

[36]  P. Marler,et al.  Song learning in canaries. , 1977 .

[37]  F. Nottebohm,et al.  Central control of song in the canary, Serinus canarius , 1976, The Journal of comparative neurology.

[38]  Masakazu Konishi,et al.  Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain , 1985, Nature.

[39]  L. A. Eales Song learning in female-raised zebra finches: another look at the sensitive phase , 1987, Animal Behaviour.

[40]  M. Konishi,et al.  Hormonal control of cell death in a sexually dimorphic song nucleus in the zebra finch. , 1987, Ciba Foundation symposium.

[41]  EJ Nordeen,et al.  Sex and regional differences in the incorporation of neurons born during song learning in zebra finches , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  P. Marler,et al.  Sparrows Learn Adult Song and More from Memory , 1981, Science.

[43]  Fernando Nottebohm,et al.  Organization of the zebra finch song control system: I. Representation of syringeal muscles in the hypoglossal nucleus , 1988, The Journal of comparative neurology.

[44]  F. Nottebohm,et al.  Connections of vocal control nuclei in the canary telencephalon , 1982, The Journal of comparative neurology.

[45]  S. Okuhata,et al.  Synaptic connections of thalamo-cerebral vocal nuclei of the canary , 1987, Brain Research Bulletin.

[46]  F. Nottebohm,et al.  Androgen affects cholinergic enzymes in syringeal motor neurons and muscle , 1980, Brain Research.

[47]  F. Nottebohm,et al.  Gonadal hormones induce dendritic growth in the adult avian brain. , 1981, Science.

[48]  P. Kuhl Auditory perception and the evolution of speech , 1988 .

[49]  M. Konishi,et al.  Developmental changes in estrogen-sensitive neurons in the forebrain of the zebra finch. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[50]  F. Nottebohm,et al.  Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[51]  F. Nottebohm,et al.  Cells born in adult canary forebrain are local interneurons , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  F. Nottebohm,et al.  Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[53]  F. Nottebohm,et al.  Modification of synapses in androgen-sensitive muscle. I. Hormonal regulation of acetylcholine receptor number in the songbird syrinx , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  F. Nottebohm,et al.  Neurons generated in the adult brain are recruited into functional circuits. , 1984, Science.

[55]  P. Marler,et al.  Song Development in Hand-Raised Oregon Juncos , 1962 .

[56]  Eliot A. Brenowitz,et al.  Interspecific comparisons of the size of neural song control regions and song complexity in duetting birds: evolutionary implications , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  W. Calder,et al.  Respiration during song in the canary (Serinus canaria). , 1970, Comparative biochemistry and physiology.

[58]  Eliot A. Brenowitz,et al.  Small sex differences in song control dendrites are associated with minimal differences in song capacity. , 1988, Journal of neurobiology.

[59]  A. Arnold,et al.  Hormone concentrating cells in vocal control and other areas of the brain of the zebra finch (Poephila guttata) , 1976, The Journal of comparative neurology.

[60]  L. C. Katz,et al.  Auditory responses in the zebra finch's motor system for song , 1981, Brain Research.

[61]  H. Williams,et al.  Auditory responses in avian vocal motor neurons: a motor theory for song perception in birds. , 1985, Science.

[62]  A. Arnold,et al.  Sexual dimorphism and lack of seasonal changes in vocal control regions of the white-crowned sparrow brain , 1984, Brain Research.

[63]  J. S. McCasland,et al.  Interaction between auditory and motor activities in an avian song control nucleus. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[64]  M. Gurney,et al.  Hormone-Induced Sexual Differentiation of Brain and Behavior in Zebra Finches , 1980, Science.

[65]  L. Baptista,et al.  Social interaction, sensitive phases and the song template hypothesis in the white-crowned sparrow , 1984, Animal Behaviour.

[66]  E. Nordeen,et al.  Sexual differentiation of androgen accumulation within the zebra finch brain through selective cell loss and addition , 1987, The Journal of comparative neurology.

[67]  F. Nottebohm,et al.  Population differences in complexity of a learned skill are correlated with the brain space involved. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[68]  E. Nordeen,et al.  Projections of androgen-accumulating neurons in a nucleus controlling avian song , 1989, Brain Research.

[69]  M. Gurney,et al.  Hormonal control of cell form and number in the zebra finch song system , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  N. Saito,et al.  Correlation between the size of song control nuclei and plumage color change in orange bishop birds , 1989, Neuroscience Letters.

[71]  F. Nottebohm,et al.  High-affinity androgen binding proteins in syringeal tissues of songbirds. , 1979, General and comparative endocrinology.

[72]  J. Wingfield Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia. I. Temporal organization of the breeding cycle. , 1984, General and comparative endocrinology.

[73]  Peter Marler,et al.  The role of sex steroids in the acquisition and production of birdsong , 1988, Nature.

[74]  J. Wingfield,et al.  Control of seasonal reproduction in temperate-zone birds. , 1980 .

[75]  Fernando Nottebohm,et al.  Migration of young neurons in adult avian brain , 1988, Nature.

[76]  J. A. Paton,et al.  Respiratory gating of activity in the avian vocal control system , 1982, Brain Research.

[77]  F. Nottebohm Birdsong as a Model in Which to Study Brain Processes Related to Learning , 1984 .

[78]  M. Gahr,et al.  Delineation of a brain nucleus: Comparisons of cytochemical, hodological, and cytoarchitectural views of the song control nucleus HVC of the adult canary , 1990, The Journal of comparative neurology.

[79]  B. Parsons,et al.  Androgen receptor levels in hypothalamic and vocal control nuclei in the male zebra finch , 1984, Brain Research.

[80]  Sandra A. Brown,et al.  Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches , 1989, The Journal of comparative neurology.

[81]  S. Breedlove Cellular analyses of hormone influence on motoneuronal development and function. , 1986, Journal of neurobiology.