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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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References

  1. 1

    Karni, A., Tanne, D., Rubenstein, B. S., Askenasy, J. J. & Sagi, D. Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265, 679–682 (1994)

  2. 2

    Wilson, M. A. & Mc Naughton, B. L. Reactivation of hippocampal ensemble memories during sleep. Science 265, 676–679 (1994)

  3. 3

    Maquet, P. The role of sleep in learning and memory. Science 294, 1048–1052 (2001)

  4. 4

    Peigneux, P., Laureys, S., Delbeuck, X. & Maquet, P. Sleeping brain, learning brain. The role of sleep for memory systems. Neuroreport 12, 111–124 (2001)

  5. 5

    Stickgold, R., Hobson, J. A., Fosse, R. & Fosse, M. Sleep, learning, and dreams: off-line memory reprocessing. Science 294, 1052–1057 (2001)

  6. 6

    Fenn, K. M., Nusbaum, H. C. & Margoliash, D. Consolidation during sleep of perceptual learning of spoken language. Nature 425, 614–616 (2003)

  7. 7

    Walker, M. P., Brakefield, T., Hobson, A. & Stickgold, R. Dissociable stages of human memory consolidation and reconsolidation. Nature 425, 616–620 (2003)

  8. 8

    Wagner, U., Gals, S.,, Halder, H., Verleger, R. & Born, J. Sleep inspires insight. Nature 427, 352–355 (2004)

  9. 9

    Walker, M. P. & Stickgold, R. Sleep-dependent learning and memory consolidation. Neuron 44, 121–133 (2004)

  10. 10

    Huber, R., Ghilardi, M. F., Massimini, M. & Tononi, G. Local sleep and learning. Nature 430, 78–81 (2004)

  11. 11

    Peigneux, P. et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44, 535–545 (2004)

  12. 12

    Frank, M. G., Issa, N. P. & Stryker, M. P. Sleep enhances plasticity in the developing visual cortex. Neuron 30, 275–287 (2001)

  13. 13

    Zuckerman, B., Stevenson, J. & Bailey, V. Sleep problems in early childhood: continuities, predictive factors, and behavioral correlates. Pediatrics 80, 664–671 (1987)

  14. 14

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

  15. 15

    Brainard, M. S. & Doupe, A. J. What songbirds teach us about learning. Nature 417, 351–358 (2002)

  16. 16

    Immelmann, K. in Bird Vocalizations (ed. Hinde, R. A.) 61–74 (Cambridge Univ. Press, Cambridge, 1969)

  17. 17

    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)

  18. 18

    Tchernichovski, O. & Mitra, P. P. Towards quantification of vocal imitation in the zebra finch. J. Comp. Physiol. [A] 188, 867–878 (2002)

  19. 19

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

  20. 20

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

  21. 21

    Bottjer, S. W. & Johnson, F. Circuits, hormones, and learning: vocal behavior in songbirds. J. Neurobiol. 33, 602–618 (1997)

  22. 22

    Schmidt, M. F. & Konishi, M. Gating of auditory responses in the vocal control system of awake songbirds. Nature Neurosci. 1, 513–518 (2001)

  23. 23

    Nick, T. A. & Konishi, M. Dynamic control of auditory activity during sleep: correlation between song response and EEG. Proc. Natl Acad. Sci. USA 98, 14012–14016 (2001)

  24. 24

    Rauske, P. L., Shea, S. D. & Margoliash, D. State and neuronal class-dependent reconfiguration in the avian song system. J. Neurophysiol. 89, 1688–1701 (2003)

  25. 25

    Nick, T. A. & Konishi, M. Neural song preference during vocal learning in the zebra finch depends on age and state. J. Neurobiol. 62, 231–242 (2005)

  26. 26

    Dave, A. S. & Margoliash, D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290, 812–816 (2000)

  27. 27

    Hahnloser, R. H., Kozhevnikov, A. A. & Fee, M. S. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419, 65–70 (2002)

  28. 28

    Margoliash, D. Evaluating theories of bird song learning: implications for future directions. J. Comp. Physiol. A 188, 851–866 (2002)

  29. 29

    Tchernichovski, O., Nottebohm, F., Ho, C. E., Pesaran, B. & Mitra, P. P. A procedure for an automated measurement of song similarity. Anim. Behav. 59, 1167–1176 (2000)

  30. 30

    Tchernichovski, O., Lints, T., Derégnaucourt, S., Cimenser, A. & Mitra, P. P. Studying the song development process: rationale and methods. Ann. NY Acad. Sci. 1016, 348–363 (2004)

  31. 31

    Tchernichovski, O. & Mitra, P. P. Sound analysis Pro user manual. http://ofer.sci.ccny.cuny.edu (2004).

  32. 32

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

  33. 33

    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)

  34. 34

    Tassi, P. & Muzet, A. Sleep inertia. Sleep Med. Rev. 4, 341–353 (2000)

  35. 35

    Jarvis, E. D. & Nottebohm, F. Motor-driven gene expression. Proc. Natl Acad. Sci. USA 94, 4097–4102 (1997)

  36. 36

    Nordeen, K. W. & Nordeen, E. J. Projection neurons within a vocal motor pathway are born during song learning in zebra finches. Nature 334, 149–151 (1988)

  37. 37

    Wang, N., Hurley, P., Pytte, C. & Kirn, J. R. Vocal control neuron incorporation decreases with age in the adult zebra finch. J. Neurosci. 22, 10864–10870 (2002)

  38. 38

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

  39. 39

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

  40. 40

    Keasar, M., Motro, U., Shur, Y. & Schmida, A. Overnight memory retention of foraging skills by bumblebees is imperfect. Anim. Behav. 52, 95–104 (1996)

  41. 41

    Golani, I. A mobility gradient in the organization of vertebrate movement: the perception of movement through symbolic language. Behav. Brain Sci. 15, 249–308 (1992)

  42. 42

    Tchernichovski, O., Benjamini, Y. & Golani, I. The dynamics of long-term exploration in the rat. Part I. A phase-plane analysis of the relationship between location and velocity. Biol. Cybern. 78, 423–432 (1998)

  43. 43

    Marinari, E. & Parisi, G. Simulated tempering: a new Monte Carlo scheme. Europhys. Lett. 19, 451–458 (1992)

  44. 44

    Kirkpatrick, S., Gelatt, C. D. & Vecchi, M. P. Optimization by simulated annealing. Science 220, 671–680 (1983)

  45. 45

    Ho, C. E., Pesaran, B., Fee, M. S. & Mitra, P. P. in Proc. Joint Symposium on Neural Computation Vol. 5, 76–83 (Univ. California Press, San Diego, 1998)

  46. 46

    Loader, C. Local Regression and Likelihood (Springer, New York, 1999)

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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.

Author information

Correspondence to Sébastien Derégnaucourt.

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The authors declare that they have no competing financial interests.

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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Further reading

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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