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Species-typical songs in white-crowned sparrows tutored with only phrase pairs


Modern theories of learned vocal behaviours, such as human speech and singing in songbirds1, posit that acoustic communication signals are reproduced from memory, using auditory feedback2. The nature of these memories, however, is unclear. Here we propose and test a model for how complex song structure can emerge from sparse sequence information acquired during tutoring. In this conceptual model, a population of combination-sensitive (phrase-pair) detectors is shaped by early exposure to song and serves as the minimal representation of the template necessary for generating complete song. As predicted by the model, birds that were tutored with only pairs of normally adjacent song phrases were able to assemble full songs in which phrases were placed in the correct order; birds that were tutored with reverse-ordered phrase pairs sang songs with reversed phrase order. Birds that were tutored with all song phrases, but presented singly, failed to produce normal, full songs. These findings provide the first evidence for a minimal requirement of sequence information in the acoustic model that can give rise to correct song structure.

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Figure 1: Sound spectrograms of songs of two white-crowned sparrows and tutor models.
Figure 2: Sound spectrograms of representative crystallized songs.
Figure 3: Sound spectrograms of representative songs of birds that were tutored with the phrase pairs DE, CD, BC and AB, presented in that order (see Fig. 1b).
Figure 4: Sound spectrograms of representative songs of birds that were tutored with the phrase pairs BA, CB, DC, ED, presented in that order.
Figure 5: Song development for birds tutored with forward (bird 48) or reversed-order (birds 67 and 84) phrase pairs.


  1. 1

    Doupe, A. J. & Kuhl, P. K. Birdsong and human speech: Common themes and mechanisms. Annu. Rev. Neurosci. 22, 567–631 (1999)

    CAS  Article  Google Scholar 

  2. 2

    Konishi, M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol. 22, 770–783 (1965)

    CAS  PubMed  Google Scholar 

  3. 3

    Thorpe, W. H. Birdsong (Cambridge Univ. Press, London, 1961)

    Google Scholar 

  4. 4

    Konishi, M. Perception and Experience (Plenum, New York, 1978)

    Google Scholar 

  5. 5

    Hultsch, H. & Todt, D. Discontinuous and incremental processes in the song learning of birds: Evidence for the primer effect. J. Comp. Physiol. 179, 291–299 (1996)

    Article  Google Scholar 

  6. 6

    Marler, P. & Peters, S. Sparrows learn adult song and more from memory. Science 213, 780–782 (1981)

    CAS  Article  Google Scholar 

  7. 7

    Soha, J. A. & Marler, P. Vocal syntax development in the white-crowned sparrow (Zonotrichia leucophrys). J. Comp. Psychol. 115, 172–180 (2001)

    CAS  Article  Google Scholar 

  8. 8

    Marler, P. & Tamura, M. Song ‘dialects’ in three populations of white-crowned sparrows. Condor 64, 363–399 (1962)

    Article  Google Scholar 

  9. 9

    Marler, P. & Tamura, M. Culturally transmitted patterns of vocal behavior in sparrows. Science 146, 1483–1486 (1964)

    CAS  Article  Google Scholar 

  10. 10

    Marler, P. A comparative approach to vocal learning: Song development in white-crowned sparrows. J. Comp. Physiol. Psychol. 71, 1–25 (1970)

    Article  Google Scholar 

  11. 11

    Tchernichovski, O., Mitra, P. P., Lints, T. & Nottebohm, F. Dynamics of the vocal imitation process: How a zebra finch learns its song. Science 291, 2564–2569 (2001)

    CAS  Article  Google Scholar 

  12. 12

    Margoliash, D. Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J. Neurosci. 3, 1039–1057 (1983)

    CAS  Article  Google Scholar 

  13. 13

    Margoliash, D. & Fortune, E. S. Temporal and harmonic combination sensitive neurons in the zebra finch's HVc. J. Neurosci. 12, 4309–4326 (1992)

    CAS  Article  Google Scholar 

  14. 14

    Lewicki, M. S. & Arthur, B. J. Hierarchical organization of auditory temporal context sensitivity. J. Neurosci. 16, 6987–6998 (1996)

    CAS  Article  Google Scholar 

  15. 15

    Lewicki, M. S. & Konishi, M. Mechanisms underlying the sensitivity of songbird forebrain neurons to temporal order. Proc. Natl Acad. Sci. USA 92, 5582–5586 (1995)

    CAS  Article  Google Scholar 

  16. 16

    Lewicki, M. S. Intracellular characterization of song-specfic neurons in the zebra finch auditory forebrain. J. Neurosci. 16, 5854–5863 (1996)

    CAS  Article  Google Scholar 

  17. 17

    Mooney, R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J. Neurosci. 20, 5420–5436 (2000)

    CAS  Article  Google Scholar 

  18. 18

    Doupe, A. Song- and order-selective neurons in the songbird anterior forebrain and their emergence during vocal development. J. Neurosci. 17, 1147–1167 (1997)

    CAS  Article  Google Scholar 

  19. 19

    Volman, S. F. Development of neural selectivity for birdsong during vocal learning. J. Neurosci. 13, 4737–4747 (1993)

    CAS  Article  Google Scholar 

  20. 20

    Solis, M. M. & Doupe, A. Anterior forebrain neurons develop selectivity by an intermediate stage of song learning. J. Neurosci. 17, 6447–6462 (1997)

    CAS  Article  Google Scholar 

  21. 21

    Bottjer, S. W., Miesner, E. A. & Arnold, A. P. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224, 901–903 (1984)

    CAS  Article  Google Scholar 

  22. 22

    Aldridge, J. W. & Berridge, K. C. Coding of serial order by neostriatal neurons: a “natural action” approach to movement sequence. J. Neurosci. 7, 2777–2787 (1998)

    Article  Google Scholar 

  23. 23

    Klein, D., Zatorre, R. J., Milner, B., Meyer, E. & Evans, A. C. Left putaminal activation when speaking a second language: evidence from PET. Neuroreport 5, 2295–2297 (1994)

    CAS  Article  Google Scholar 

  24. 24

    Griffiths, R., Double, M. C., Orr, K. & Dawson, R. J. G. A DNA test to sex most birds. Mol. Ecol. 7, 1071–1075 (1998)

    CAS  Article  Google Scholar 

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This work was supported by grants from the University of Utah and NIH. We thank T. Dance for technical assistance, E. Haskell for guidance in statistical analyses, J. Whittington for molecular sexing of birds and R. Dendukuri for writing computer programs used in analysis and presentation of data.

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Correspondence to Gary J. Rose.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure, Legend and Text

A detailed description of the model proposed and tested in our experiment whereby birds tutored with phrase pairs are able to assemble complete songs. The figure represents a graphical depiction of the model for a song consisting of three phrases. (DOC 139 kb)

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Rose, G., Goller, F., Gritton, H. et al. Species-typical songs in white-crowned sparrows tutored with only phrase pairs. Nature 432, 753–758 (2004).

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