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Birdsong: From behaviour to brain

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Abstract

Although vocal communication is wide-spread in animal kingdom, the use of learned (in contrast to innate) vocalization is very rare. We can find it only in few animal taxa: human, bats, whales and dolphins, elephants, parrots, hummingbirds, and songbirds. There are several parallels between human and songbird perception and production of vocal signals. Hence, many studies take interest in songbird singing for investigating the neural bases of learning and memory. Brain circuits controlling song learning and maintenance consist of two pathways — a vocal motor pathway responsible for production of learned vocalizations and anterior forebrain pathway responsible for learning and modifying the vocalizations. This review provides an overview of the song organization, its behavioural traits, and neural regulations. The recently expanding area of molecular mapping of the behaviour-driven gene expression in brain represents one of the modern approaches to the study the function of vocal and auditory areas for song learning and maintenance in birds.

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References

  • Bailey D. & Wade J. 2003. Differential expression of the immediate early genes FOS and ZENK following auditory stimulation in the juvenile male and female zebra finch. Mol. Brain Res. 116: 147–154. DOI 10.1016/S0169-328X(03)00288-2

    Article  PubMed  CAS  Google Scholar 

  • Bauer E., Coleman M., Roberts T., Roy A., Prather J. & Moone, R. 2008. A synaptic basis for auditory-vocal integration in the songbird. J. Neurosci. 28: 1509–1522. DOI 10.1523/JNEUROSCI.3838-07.2008

    Article  PubMed  CAS  Google Scholar 

  • Böhner J. 1990. Early acquisition of song in the zebra finch, Taeniopygia guttata. Anim. Behav. 39: 369–374. DOI 10.1016/S0003-3472(05)80883-8

    Article  Google Scholar 

  • Bolhuis J. & Gahr M. 2006. Neural mechanisms of birdsong memory. Nature Reviews Neuroscience 7: 347–357. DOI 10.1038/nrn1904

    Article  PubMed  CAS  Google Scholar 

  • Brainard M. & Doupe A. 2000. Auditory feedback in learning and maintenance of vocal behaviour. Nat. Rev. Neurosci. 1: 31–40. DOI 10.1038/35036205

    Article  PubMed  CAS  Google Scholar 

  • Brainard M. & Doupe A. 2001. Postlearning consolidation of birdsong: stabilizing effects of age and anterior forebrain lesions. J. Neurosci. 21: 2501–2517.

    PubMed  CAS  Google Scholar 

  • Brainard M. & Doupe A. 2002. What songbirds teach us about learning. Nature 417: 351–358. DOI 10.1038/417351a

    Article  PubMed  CAS  Google Scholar 

  • Brenowitz E., Margoliash D. & Nordeen K. 1997. An introduction to birdsong and the avian song system. J. Neurobiol. 33: 495–500. DOI 10.1002/(SICI)1097-4695(19971105)33:5〈495::AIDNEU1〉 3.0.CO;2-#

    Article  PubMed  CAS  Google Scholar 

  • Byers B. & Kroodsma D. 2009. Female mate choice and songbird song repertoires. Anim. Behav. 77: 13–22. DOI 10.1016/j.anbehav.2008.10.003

    Article  Google Scholar 

  • Catchpole C. 1987. Bird song, sexual selection and female choice. Trends Ecol. Evol. 2: 94–97. DOI 10.1016/0169-5347(87)90165-0

    Article  Google Scholar 

  • Catchpole C.K., Slater P.J.B. & Mann N. 2003. Bird Song: Biological Themes and Variations. Cambridge Univ Press, Cambridge, 248 pp.

    Google Scholar 

  • Cooper B. & Goller F. 2006. Physiological insights into the social-context-dependent changes in the rhythm of the song motor program. J. Neurophysiol. 95: 3798–3809. DOI 10.1152/jn.01123.2005

    Article  PubMed  Google Scholar 

  • Darwin C. 1871. The Descent of Man and Selection in Relation to Sex. Vol. II. John Murray, London, 475 pp.

    Google Scholar 

  • Devoogd T., Krebs J., Healy S. & Purvis A. 1993. Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds. Proc. R. Soc. Lond., Ser. B: Biol. Sci. 254: 75–82. DOI 10.1098/rspb.1993.0129

    Article  CAS  Google Scholar 

  • Doupe A. & Kuhl P. 1999. Birdsong and human speech: Common themes and mechanisms. Annu. Rev. Neurosci. 22: 567–631. DOI 10.1146/annurev.neuro.22.1567

    Article  PubMed  CAS  Google Scholar 

  • Endler J. 1993. Some general comments on the evolution and design of animal communication systems. Philos. Trans. R. Soc. Lond., Ser. B: Biol. Sci. 340: 215–225.

    Article  CAS  Google Scholar 

  • Gobes S. & Bolhuis J. 2007. Birdsong memory: a neural dissociation between song recognition and production. Curr. Biol. 17: 789–793.

    Article  PubMed  CAS  Google Scholar 

  • Goldman S. & Nottebohm F. 1983. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. U. S. A. 80: 2390–2394.

    Article  PubMed  CAS  Google Scholar 

  • Gurney M. & Konishi M. 1980. Hormone-induced sexual differentiation of brain and behavior in zebra finches. Science 208: 1380–1383.

    Article  PubMed  CAS  Google Scholar 

  • Haesler S., Rochefort C., Georgi B., Licznerski P., Osten P. & Scharff C. 2007. Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus area X. PLoS Biol. 5: e321.

    Article  PubMed  CAS  Google Scholar 

  • Haesler S., Wada K., Nshdejan A., Morrisey E., Lints T., Jarvis E. & Scharff C. 2004. FoxP2 expression in avian vocal learners and non-learners. J. Neurosci. 24: 3164–3175. DOI 10.1523/JNEUROSCI.4369-03.2004

    Article  PubMed  CAS  Google Scholar 

  • Hahnloser R.H.R., Kozhevnikov A.A. & Fee M.S. 2002. An ultra-sparse code underliesthe generation of neural sequences in a songbird. Nature 419: 65–70. DOI 10.1038/nature00974

    Article  PubMed  CAS  Google Scholar 

  • Herrmann K. & Arnold A. 1991. The development of afferent projections to the robust archistriatal nucleus in male zebra finches: a quantitative electron microscopic study. J. Neurosci. 11: 2063–2074.

    PubMed  CAS  Google Scholar 

  • Horita H., Wada K. & Jarvis E. 2008. Early onset of deafening-induced song deterioration and differential requirements of the pallial-basal ganglia vocal pathway. Eur. J. Neurosci. 28: 2519–2532. DOI 10.1111/j.1460-9568.2008.06535.x

    Article  PubMed  Google Scholar 

  • Jarvis E. 2004. Learned birdsong and the neurobiology of human language. Ann. N. Y. Acad. Sci. 1016: 749–777. DOI 10.1196/annals.1298.038

    Article  PubMed  Google Scholar 

  • Jarvis E., Güntürkün O., Bruce L., Csillag A., Karten H., Kuenzel W., Medina L., Paxinos G., Perkel D. & Shimizu T. 2005. Avian brains and a new understanding of vertebrate brain evolution. Nat. Rev. Neurosci. 6: 151–159. DOI 10.1038/nrn1606

    Article  PubMed  CAS  Google Scholar 

  • Jarvis E. & Mello C. 2000. Molecular mapping of brain areas involved in parrot vocal communication. J. Comp. Neurol. 419: 1–31.

    Article  PubMed  CAS  Google Scholar 

  • Jarvis E. & Nottebohm F. 1997. Motor-driven gene expression. Proc. Natl. Acad. Sci. U.S.A. 94: 4097–4102.

    Article  PubMed  CAS  Google Scholar 

  • Jarvis E., Ribeiro S., Da Silva M., Ventura, D., Vielliard J. & Mello C. 2000. Behaviourally driven gene expression reveals song nuclei in hummingbird brain. Nature 406: 628–632. DOI 10.1038/35020570

    Article  PubMed  CAS  Google Scholar 

  • Jarvis E., Scharff C., Grossman M., Ramos J. & Nottebohm F. 1998. For whom the bird sings: context-dependent gene expression. Neuron 21: 775–788.

    Article  PubMed  CAS  Google Scholar 

  • Jin H. & Clayton D.F. 1997. Localized changes in immediate-early gene regulation during sensory and motor learning in Zebra Finches. Neuron 19: 1049–1059.

    Article  PubMed  CAS  Google Scholar 

  • Johnson F. & Whitney O. 2005. Singing-driven gene expression in the developing songbird brain. Physiol. Behav. 86: 390–398. DOI 10.1016/j.physbeh.2005.08.009

    Article  PubMed  CAS  Google Scholar 

  • Kao M. & Brainard M. 2006. Lesions of an avian basal ganglia circuit prevent context-dependent changes to song variability. J. Neurophysiol. 96: 1441. DOI 10.1152/jn.01138.2005

    Article  PubMed  Google Scholar 

  • Kao M., Doupe A. & Brainard M. 2005. Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433: 638–643. DOI 10.1038/nature03127

    Article  PubMed  CAS  Google Scholar 

  • Kimpo R. & Doupe A. 1997. FOS is induced by singing in distinct neuronal populations in a motor network. Neuron 18: 315–326.

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi K., Uno H. & Okanoya K. 2001. Partial lesions in the anterior forebrain pathway affect song production in adult Bengalese finches. Neuroreport 12: 353–358.

    Article  PubMed  CAS  Google Scholar 

  • Konishi M. 1985. Birdsong: from behavior to neuron. Annu. Rev. Neurosci. 8: 125–170. DOI 10.1146/annurev.ne.08.030185. 001013

    Article  PubMed  CAS  Google Scholar 

  • Kroodsma D. & Parker L. 1977. Vocal virtuosity in the brown thrasher. The Auk 94: 783–785.

    Google Scholar 

  • Kubíková Ľ., Turner E., Scharff C. & Jarvis E. 2007. A predisposition to stutter and its recovery following basal ganglia damage. Soc. Neurosci. Abstr. 33: 430–436.

    Google Scholar 

  • Kuhl P. 2003. Human speech and birdsong: communication and the social brain. Proc. Natl. Acad. Sci. U.S.A. 100: 9645–9646.

    Article  PubMed  CAS  Google Scholar 

  • Lai C., Fisher S., Hurst J., Vargha-Khadem F. & Monaco A. 2001. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413: 519–523. DOI 10.1038/35097076

    Article  PubMed  CAS  Google Scholar 

  • Li X., Jarvis E., Alvarez-Borda B., Lim D. & Nottebohm F. 2000. A relationship between behavior, neurotrophin expression, and new neuron survival. Proc. Natl. Acad. Sci. U.S.A. 97: 8584–8589.

    Article  PubMed  CAS  Google Scholar 

  • Lombardino A. & Nottebohm F. 2000. Age at deafening affects the stability of learned song in adult male zebra finches. J. Neurosci. 20: 5054–5064.

    PubMed  CAS  Google Scholar 

  • London S., Dong S., Replogle K. & Clayton D. 2009. Developmental shifts in gene expression in the auditory forebrain during the sensitive period for song learning. Dev. Neurobiol. 69: 437–450.

    Article  PubMed  CAS  Google Scholar 

  • Marler P. 1981. Birdsong: the acquisition of a learned motor skill. Trends Neurosci. 4: 88–94.

    Article  Google Scholar 

  • Marler P. 1999. On innateness: are sparrow songs ‘learned’ or ‘innate’ ?, pp. 293–318. In: Hauser M. & Konishi M. (eds), The Design of Animal Communication, MIT Press, Cambridge, Massachusetts.

    Google Scholar 

  • Marler P. 2004. Bird calls: their potential for behavioral neurobiology. Ann. N. Y. Acad. Sci. 1016: 31–44. DOI 10.1196/annals. 1298.034

    Article  PubMed  Google Scholar 

  • Marler P. & Peters S. 1982. Developmental overproduction and selective attrition: new processes in the epigenesis of birdsong. Dev. Psychobiol. 15: 369–378.

    Article  PubMed  CAS  Google Scholar 

  • Marler P. & Sherman V. 1983. Song structure without auditory feedback: emendations of the auditory template hypothesis. J. Neurosci. 3: 517–531.

    PubMed  CAS  Google Scholar 

  • Marler P. & Sherman V. 1985. Innate differences in singing behaviour of sparrows reared in isolation from adult conspecific song. Anim. Behav. 33: 57–71. DOI 10.1016/S0003-3472(85)80120-2

    Article  Google Scholar 

  • McGregor P. & Peake T. 2000. Communication networks: social environments for receiving and signalling behaviour. Acta Ethol. 2: 71–81.

    Article  Google Scholar 

  • Mello C.V., Velho T.A.F. & Pinaud R. 2004. Song-induced gene expression: A window on song auditory processing and perception. Ann. N. Y. Acad. Sci. 1016: 263–281.

    Article  PubMed  CAS  Google Scholar 

  • Mello C., Vicario D. & Clayton D. 1992a. Song presentation induces gene expression in the songbird forebrain. Proc. Natl. Acad. Sci. U. S. A. 89: 6818–6822.

    Article  PubMed  CAS  Google Scholar 

  • Mello C., Vicario D. & Clayton D. 1992b. Song presentation induces gene expression in the songbird forebrain. Proc. Natl. Acad. Sci. U.S.A. 89: 6818–6822.

    Article  PubMed  CAS  Google Scholar 

  • Neubauer R. 1999. Super-normal length song preferences of female zebra finches (Taeniopygia guttata) and a theory of the evolution of bird song. Evol. Ecol. 13: 365–380.

    Article  Google Scholar 

  • Nixdorf-Bergweiler B.E., Lips M.B. & Heinemann U. 1995. Electrophysiological and morphological evidence for a new projection of LMAN-neurones towards area X. Neuroreport 6: 1729–1732.

    Article  PubMed  CAS  Google Scholar 

  • Nordeen K. & Nordeen E. 1992. Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav. Neural Biol. 57: 58–66.

    Article  PubMed  CAS  Google Scholar 

  • Nottebohm F. 1972. The origins of vocal learning. American Naturalist 106: 116–140.

    Article  Google Scholar 

  • Nottebohm F. & Arnold A. 1976. Sexual dimorphism in vocal control areas of the songbird brain. Science 194: 211–213.

    Article  PubMed  CAS  Google Scholar 

  • Nottebohm F., Stokes T. & Leonard C. 1976. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165: 457–486.

    Article  PubMed  CAS  Google Scholar 

  • Olveczky B., Andalman A. & Fee M. 2005. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol 3: e153.

    Article  PubMed  CAS  Google Scholar 

  • Pytte C., Gerson M., Miller J. & Kirn J. 2007. Increasing stereotypy in adult zebra finch song correlates with a declining rate of adult neurogenesis. Dev. Neurobiol. 67: 1699–1720.

    Article  PubMed  Google Scholar 

  • Reiner A., Perkel D., Bruce L., Butler A., Csillag A., Kuenzel W., Medina L., Paxinos G., Shimizu T., Striedter G., Wild M., Ball G., Durand S., Gütürkün O., Lee D., Mello C., Powers A., White S., Hough G., Kubikova L., Smulders T., Wada K., Dugas-Ford J., Husband S., Yamamoto K., Yu J., Siang C. & Jarvis E. 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473: 377–414.

    Article  PubMed  Google Scholar 

  • Replogle K., Arnold A., Ball G., Band M., Bensch S., Brenowitz E., Dong S., Drnevich J., Ferris M., George J., Gong G., Hasselquist D., Hernandez A., Kim R., Lewin H., Liu L., Lovell P., Mello C., Naurin S., Rodriguez-Zas S., Thimmapuram J., Wade J. & Clayton D. 2008. The Songbird Neurogenomics (SoNG) Initiative: Community-based tools and strategies for study of brain gene function and evolution. BMC Genomics 9: 131. DOI 10.1186/1471-2164-9-131

    Article  PubMed  CAS  Google Scholar 

  • Scharff C. & Nottebohm F. 1991. A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J. Neurosci. 11: 2896–2913.

    PubMed  CAS  Google Scholar 

  • Stapley J., Birkhead T.R., Burke T. & Slate J. 2008. A linkage map of the zebra finch Taeniopygia guttata provides new insights into avian genome evolution. Genetics 179: 651–667. DOI 10.1534/genetics.107.086264

    Article  PubMed  CAS  Google Scholar 

  • Stripling R., Kruse A.A. & Clayton D.F. 2001. Development of song responses in the zebra finch caudomedial neostriatum: Role of genomic and electrophysiological activities. J. Neurobiol. 48: 163–180. DOI 10.1002/neu.1049

    Article  PubMed  CAS  Google Scholar 

  • Theunissen F., Amin N., Shaevitz S., Woolley S., Fremouw T. & Hauber M. 2004. Song selectivity in the song system and in the auditory forebrain. Ann. N. Y. Acad. Sci. 1016: 222–245. DOI 10.1196/annals.1298.023

    Article  PubMed  Google Scholar 

  • Thorpe W. 1958. The learning of song patterns by birds, with especial reference to the song of the chaffinch Fringilla coelebs. Ibis 100: 535–570.

    Article  Google Scholar 

  • Vates G. & Nottebohm F. 1995. Feedback circuitry within a song-learning pathway. Proc. Natl. Acad. Sci. U. S. A. 92: 5139–5143.

    Article  PubMed  CAS  Google Scholar 

  • Vicario D. & Yohay K. 1993. Song-selective auditory input to a forebrain vocal control nucleus in the zebra finch. J. Neurobiol. 24: 488–505. DOI 10.1002/neu.480240407

    Article  PubMed  CAS  Google Scholar 

  • Wada K., Howard J., McConnell P., Whitney O., Lints T., Rivas M., Horita H., Patterson M., White S. & Scharff C. 2006. A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc. Natl. Acad. Sci. U.S.A. 103: 15212–15217. DOI 10.1073/pnas.0607098103

    Article  PubMed  CAS  Google Scholar 

  • Whitney O., Soderstrom K. & Johnson F. 2000. Post-transcriptional regulation of zenk expression associated with zebra finch vocal development. Mol. Brain Res. 80: 279–290. DOI 10.1016/S0169-328X(00)00178-9

    Article  PubMed  CAS  Google Scholar 

  • Wild J. 1997. Neural pathways for the control of birdsong production. J. Neurobiol. 33: 653–670. DOI 10.1002/(SICI)1097-4695(199711.05)33:5〈653::AID-NEU11〉3.0.CO;2-A

    Article  PubMed  CAS  Google Scholar 

  • Yamashita Y., Takahasi M., Okumura T., Ikebuchi M., Yamada H., Suzuki M., Okanoya K. & Tani J. 2008. Developmental learning of complex syntactical song in the Bengalese finch: A neural network model. Neural Netw. 21: 1224–1231. DOI 10.1016/j.neunet.2008.03.003

    Article  PubMed  Google Scholar 

  • Yu A. & Margoliash D. 1996. Temporal hierarchical control of singing in birds. Science 273: 1871–1875.

    Article  PubMed  CAS  Google Scholar 

  • Zann R. 1996. The Zebra Finch: A Synthesis of Field and Laboratory Studies. Oxford University Press, Oxford, 352 pp.

    Google Scholar 

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  1. Laboratory of Neurobiology and Physiology of Behaviour, Institute of Animal Biochemistry and Genetics, Slovak Academy of Sciences, Moyzesova 61, 900 28, Ivanka pri Dunaji, Slovakia

    Eva Bosíková, Ľubor Košťál & Ľubica Kubíková

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  1. Eva Bosíková
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  3. Ľubica Kubíková
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Correspondence to Ľubica Kubíková.

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Bosíková, E., Košťál, Ľ. & Kubíková, Ľ. Birdsong: From behaviour to brain. Biologia 65, 379–387 (2010). https://doi.org/10.2478/s11756-010-0047-1

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