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How sleep affects the developmental learning of bird song

Abstract

Sleep affects learning and development in humans and other animals, but the role of sleep in developmental learning has never been examined. Here we show the effects of night-sleep on song development in the zebra finch by recording and analysing the entire song ontogeny. During periods of rapid learning we observed a pronounced deterioration in song structure after night-sleep. The song regained structure after intense morning singing. Daily improvement in similarity to the tutored song occurred during the late phase of this morning recovery; little further improvement occurred thereafter. Furthermore, birds that showed stronger post-sleep deterioration during development achieved a better final imitation. The effect diminished with age. Our experiments showed that these oscillations were not a result of sleep inertia or lack of practice, indicating the possible involvement of an active process, perhaps neural song-replay during sleep. We suggest that these oscillations correspond to competing demands of plasticity and consolidation during learning, creating repeated opportunities to reshape previously learned motor skills.

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Figure 1: Tracing vocal changes.
Figure 2: Vocal changes during night-sleep.
Figure 3: Recovery of syllable structure during the morning.
Figure 4: Progression of song learning.
Figure 5: Vocal changes after song prevention and sleep manipulation.
Figure 6: Comparison of post-sleep deterioration and post-deafening deterioration.

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Acknowledgements

We thank D. Swigger for programming; J. Wallman for comments; P. Andrews for help with graphics; and T. Lints, K. Maul, A. Alexander and L. Dayani for help in analysing data. This work was supported by grants from the NIH to O.T. and P.P.M., by an NIH RCMI (National Institutes of Health Research Centers in Minority Institutions) grant to the City College of New York, by internal support from the Cold Spring Harbor Laboratory and the Robertson foundation to P.P.M., and from the Fondation Fyssen to S.D.

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Correspondence to Sébastien Derégnaucourt.

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Supplementary information

Supplementary Methods

1. Source separation in the case of live tutoring; 2. Observations on sleep; 3. Segmentation into syllables; 4. Computing syllable features; 5. Smoothing of duration histograms; 6. Clustering syllables and tracing the evolution of clusters; 7. Estimating vocal changes across timescales; 8. Similarity measurements. (PDF 97 kb)

Supplementary Data

1. Analysis of vocal changes triggered in adult birds; 2. Observations on sleep; 3. Analysis of sleep effect on syllable duration; 4. Comparison between birds trained from day 43 versus day 60; 5. Analysis of the causality chain between post-sleep deterioration and eventual similarity to the song model. (PDF 73 kb)

Supplementary Table 1

Relative contribution of syllable features to post-sleep deterioration. (PDF 77 kb)

Supplementary Figure 1

Developmental change in the structure of a syllable produced by a bird trained from day 43 (a) and a bird trained from day 90 (b) as captured by Wiener Entropy variance (EV). (PDF 37 kb)

Supplementary Figure 2

Cross-correlation analysis between post-sleep deterioration curves of birds trained from day 43 (n=12) and birds trained from day 60 (n=6). (PDF 58 kb)

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Derégnaucourt, S., Mitra, P., Fehér, O. et al. How sleep affects the developmental learning of bird song. Nature 433, 710–716 (2005). https://doi.org/10.1038/nature03275

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