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Decrystallization of adult birdsong by perturbation of auditory feedback

Abstract

Young birds learn to sing by using auditory feedback to compare their own vocalizations to a memorized or innate song pattern; ifthey are deafened as juveniles, they will not develop normal songs1,2. The completion of song development is called crystallization. After this stage, song shows little variation in its temporal or spectral properties. However, the mechanisms underlying this stability are largely unknown. Here we present evidence that auditory feedback is actively used in adulthood to maintain the stability of song structure. We found that perturbing auditory feedback during singing in adult zebra finches caused their songto deteriorate slowly. This ‘decrystallization’ consisted of a marked loss of the spectral and temporal stereotypy seen in crystallized song, including stuttering, creation, deletion and distortion ofsong syllables. After normal feedback was restored, these deviations gradually disappeared and the original song was recovered. Thus, adult birds that do not learn new songs nevertheless retain a significant amount of plasticity in the brain.

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Figure 1: Protocols for constructing the feedback signals.
Figure 2: Normal and decrystallized birdsong spectrograms.
Figure 3: Decrystallization of a single syllable.
Figure 4: Time course of decrystallization and recovery.

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References

  1. 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 

  2. Nottebohm, F. Auditory experience and song development in the chaffinch, Fringilla coelebs. Ibis 110, 549–569 (1968).

    Article  Google Scholar 

  3. Sossinka, R. & Bohner, J. Song types in the zebra finch. Z. Tierpsychol. 53, 123–132 (1980).

    Article  Google Scholar 

  4. Marler, P. & Peters, S. Asensitive period for song acquisition in the song sparrow, Melospize melodia —a case of age limited learning. Ethology 76, 89–100 (1987).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  6. Okanoya, K. & Yamaguchi, A. Adult bengalese finches require real-time auditory feedback to produce normal song syntax. J. Neurobiol. 33, 343–356 (1997).

    Article  CAS  Google Scholar 

  7. Wooley, S. & Rubel, E. Bengalese finches Lonchura-striata-domestica depend on auditory feedback for the maintenance of song. J. Neurosci. 17, 6380–6390 (1997).

    Article  Google Scholar 

  8. Suthers, R. Contributions to birdsong from the left and right sides of the intact syrinx. Nature 347, 473–477 (1990).

    Article  ADS  Google Scholar 

  9. Fee, M. S., Shraiman, B., Pesaran, B. & Mitra, P. P. The role of nonlinear dynamics of the syrinx in birdsong production. Nature 395, 67–71 (1998).

    Article  ADS  CAS  Google Scholar 

  10. Houde, J. F. & Jordan, M. I. Sensorimotor adaptation in speech production. Science 279, 1213–1216 (1998).

    Article  ADS  CAS  Google Scholar 

  11. Feller, W. An Introduction to Probability Theory and its Applications(Wiley, New York, (1968).

    MATH  Google Scholar 

  12. Cover, T. M. & Thomas, J. A. Elements of Information Theory(Wiley, New York, (1991).

    Book  Google Scholar 

  13. Ho, C. E., Pesaran, B., Fee, M. S. & Mitra, P. P. Characterization of the structure and variability of zebra finch song elements. Proc. 5th Joint Symp. on Neural Computation 76–83 (1998).

  14. Thomson, D. J. Spectrum estimation and harmonic analysis. Proc. IEEE 70, 1055–1096 (1982).

    Article  ADS  Google Scholar 

  15. Selim, S. Z. & Ismail, M. A. K-means-type algorithms: a generalized convergence theorem and characterization of local optimality. IEEE Trans. Pattern Anal. Mach. Intell. 1, 81–87 (1984).

    Article  Google Scholar 

  16. Bradley, E. An Introduction to the Bootstrap(Chapman & Hall, New York, (1993).

    MATH  Google Scholar 

Download references

Acknowledgements

We thank B. Pesaran and M. Sahani for discussions on data analysis, and R. Egnor, M. Fee, G. Laurent and M. Schmidt for comments on the manuscript. This work was supported by a grant from the NIMH.

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Correspondence to Anthony Leonardo.

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Leonardo, A., Konishi, M. Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399, 466–470 (1999). https://doi.org/10.1038/20933

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