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Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong


Significant trial-by-trial variation persists even in the most practiced skills. One prevalent view is that such variation is simply ‘noise’ that the nervous system is unable to control or that remains below threshold for behavioural relevance1,2,3. An alternative hypothesis is that such variation enables trial-and-error learning, in which the motor system generates variation and differentially retains behaviours that give rise to better outcomes. Here we test the latter possibility for adult bengalese finch song. Adult birdsong is a complex, learned motor skill that is produced in a highly stereotyped fashion from one rendition to the next4,5. Nevertheless, there is subtle trial-by-trial variation even in stable, ‘crystallized’ adult song6,7,8. We used a computerized system to monitor small natural variations in the pitch of targeted song elements and deliver real-time auditory disruption to a subset of those variations. Birds rapidly shifted the pitch of their vocalizations in an adaptive fashion to avoid disruption. These vocal changes were precisely restricted to the targeted features of song. Hence, birds were able to learn effectively by associating small variations in their vocal behaviour with differential outcomes. Such a process could help to maintain stable, learned song despite changes to the vocal control system arising from ageing or injury. More generally, our results suggest that residual variability in well learned skills is not entirely noise but rather reflects meaningful motor exploration that can support continuous learning and optimization of performance.

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Figure 1: Differential reinforcement can adaptively alter features of adult song.
Figure 2: Adaptive shifts in fundamental frequency occur rapidly and recover.
Figure 3: Changes are restricted to targeted features of song.
Figure 4: Delayed feedback prevents adaptive pitch shifts.
Figure 5: Incremental adjustment of threshold drives large pitch changes.


  1. Beers, R. J. V., Baraduc, P. & Wolpert, D. M. Role of uncertainty in sensorimotor control. Phil. Trans. R. Soc. Lond. B 357, 1137–1145 (2002)

    Article  Google Scholar 

  2. Todorov, E. Optimality principles in sensorimotor control. Nature Neurosci. 7, 907–915 (2004)

    CAS  Article  Google Scholar 

  3. Harris, C. M. & Wolpert, D. M. Signal-dependent noise determines motor planning. Nature 394, 780–784 (1998)

    ADS  CAS  Article  Google Scholar 

  4. Konishi, M. Birdsong: From behavior to neuron. Annu. Rev. Neurosci. 8, 125–170 (1985)

    CAS  Article  Google Scholar 

  5. Deregnaucourt, S. et al. How sleep affects the developmental learning of bird song. Nature 433, 710–716 (2005)

    ADS  CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  7. 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, 638–643 (2005)

    ADS  CAS  Article  Google Scholar 

  8. Kao, M. H. & Brainard, M. S. Lesions of an avian basal ganglia circuit prevent context-dependent changes to song variability. J. Neurophysiol. 96, 1441–1455 (2006)

    Article  Google Scholar 

  9. 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 

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

    CAS  Article  Google Scholar 

  11. Okanoya, K. & Yamaguchi, A. Adult Bengalese finches (Lonchura striata var. domestica) require real-time auditory feedback to produce normal song syntax. J. Neurobiol. 33, 343–356 (1997)

    CAS  Article  Google Scholar 

  12. Woolley, S. M. & Rubel, E. W. Bengalese finches Lonchura Striata domestica depend upon auditory feedback for the maintenance of adult song. J. Neurosci. 17, 6380–6390 (1997)

    CAS  Article  Google Scholar 

  13. Leonardo, A. & Konishi, M. Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399, 466–470 (1999)

    ADS  CAS  Article  Google Scholar 

  14. Zevin, J. D., Seidenberg, M. S. & Bottjer, S. W. Limits on reacquisition of song in adult zebra finches exposed to white noise. J. Neurosci. 24, 5849–5862 (2004)

    CAS  Article  Google Scholar 

  15. Sutton, R. S. & Barto, A. G. Reinforcement Learning: An Introduction (MIT Press, Cambridge, Massachusetts, 1998)

    MATH  Google Scholar 

  16. Doya, K. & Sejnowski, T. in The New Cognitive Neurosciences (ed. Gazzaniga, M.) 469–482 (MIT Press, Cambridge, Massachusetts, 2000)

    Google Scholar 

  17. Troyer, T. & Doupe, A. J. An associational model of birdsong sensorimotor learning. I. Efference copy and the learning of song syllables. J. Neurophys. 84, 1204–1223 (2000)

    CAS  Article  Google Scholar 

  18. Fiete, I. R., Fee, M. S. & Seung, H. S. Model of birdsong learning based on gradient estimation by dynamic perturbation of neural conductances. J. Neurophys. 98, 2038–2057 (2007)

    Article  Google Scholar 

  19. Olveczky, B. P., Andalman, A. S. & Fee, M. S. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol. 3, e153 (2005)

    Article  Google Scholar 

  20. Hessler, N. A. & Doupe, A. J. Social context modulates singing-related neural activity in the songbird forebrain. Nature Neurosci. 2, 209–211 (1999)

    CAS  Article  Google Scholar 

  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)

    ADS  CAS  Article  Google Scholar 

  22. 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. J. Neurosci. 11, 2896–2913 (1991)

    CAS  Article  Google Scholar 

  23. Amir, O., Amir, N. & Kishon-Rabin, L. The effect of superior auditory skills on vocal accuracy. J. Acoust. Soc. Am. 113, 1102–1108 (2003)

    ADS  Article  Google Scholar 

  24. Sundberg, J., Prame, E. & Iwarsson, J. in Vocal Fold Physiology, Controlling Complexity and Chaos (eds Davis, P. & Fletcher, N.) 291–306 (Singular Publishing Group, San Diego, 1996)

    Google Scholar 

  25. Dent, M. L., Dooling, R. J. & Pierce, A. S. Frequency discrimination in budgerigars (Melopsittacus undulatus): Effects of tone duration and tonal context. J. Acoust. Soc. Am. 107, 2657–2664 (2000)

    ADS  CAS  Article  Google Scholar 

  26. Fiete, I. R., Hahnloser, R. H., Fee, M. S. & Seung, H. S. Temporal sparseness of the premotor drive is important for rapid learning in a neural network model of birdsong. J. Neurophysiol. 92, 2274–2282 (2004)

    Article  Google Scholar 

  27. Sakata, J. T. & Brainard, M. S. Real-time contributions of auditory feedback to avian vocal motor control. J. Neurosci. 26, 9619–9628 (2006)

    CAS  Article  Google Scholar 

  28. Held, R., Efstathiou, A. & Greene, M. Adaptation to displaced and delayed visual feedback from the hand. J. Exp. Psychol. 72, 887–891 (1966)

    Article  Google Scholar 

  29. Churchland, M. M., Afshar, A. & Shenoy, K. V. A central source of movement variability. Neuron 52, 1085–1096 (2006)

    CAS  Article  Google Scholar 

  30. Churchland, M. M., Santhanam, G. & Shenoy, K. V. Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach. J. Neurophysiol. 96, 3130–3146 (2006)

    Article  Google Scholar 

  31. Leonardo, A. Experimental test of the birdsong error-correction model. Proc. Natl Acad. Sci. USA 101, 16935–16940 (2004)

    ADS  CAS  Article  Google Scholar 

  32. Kozhevnikov, A. & Fee, M. S. Singing-related activity of identified HVC neurons in the zebra finch. J. Neurophysiol. 97, 4271–4283 (2007)

    Article  Google Scholar 

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We thank A. Doupe, L. Frank, T. Warren, M. Wohlgemuth, S. Sober, J. Sakata, C. Hampton and J. Wong for comments. This work was supported by an NIDCD NRSA postdoctoral fellowship and the Sloan-Swartz Foundation (E.C.T.) and by an NIDCD R01 award, an NIMH Conte Center for Neuroscience Research award and a McKnight Foundation Scholars Award (M.S.B).

Author Contributions E.C.T. performed the experiments and analysis; E.C.T. and M.S.B. designed the experiments and wrote the manuscript.

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Correspondence to Evren C. Tumer.

Supplementary information

Supplementary Information

This file contains Supplementary Notes with Supplementary Figures S1-S3 showing: details of differential reinforcement; relationship between baseline variation and capacity for adaptive change and how non-contingent feedback did not alter song. (PDF 254 kb)

Supplementary Audio 1

This file contains Supplementary Audio 1 demonstrating the stereotypy of normal adult Bengalese finch song. Three separate songs are played corresponding to the spectrograms of Figure 1a. (WAV 310 kb)

Supplementary Video 1

This file contains Supplementary Video 1 demonstrating the salience of changes driven by progressively increasing the reinforcement threshold. Points and sounds reflect pitch of 20 randomly selected syllables from each of 2 days of baseline data and 13 days of differential reinforcement. Blue line indicates reinforcement threshold. Data from experiment of Figure 5a. (MOV 454 kb)

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Tumer, E., Brainard, M. Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong. Nature 450, 1240–1244 (2007).

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