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Sleep and sensorimotor integration during early vocal learning in a songbird

Abstract

Behavioural studies widely implicate sleep in memory consolidation in the learning of a broad range of behaviours1,2,3,4. During sleep, brain regions are reactivated5,6, and specific patterns of neural activity are replayed7,8,9,10, consistent with patterns observed in previous waking behaviour. Birdsong learning is a paradigmatic model system for skill learning11,12,13,14. Song development in juvenile zebra finches (Taeniopygia guttata) is characterized by sleep-dependent circadian fluctuations in singing behaviour, with immediate post-sleep deterioration in song structure followed by recovery later in the day15. In sleeping adult birds, spontaneous bursting activity of forebrain premotor neurons in the robust nucleus of the arcopallium (RA) carries information about daytime singing16. Here we show that, in juvenile zebra finches, playback during the day of an adult ‘tutor’ song induced profound and tutor-song-specific changes in bursting activity of RA neurons during the following night of sleep. The night-time neuronal changes preceded tutor-song-induced changes in singing, first observed the following day. Interruption of auditory feedback greatly reduced sleep bursting and prevented the tutor-song-specific neuronal remodelling. Thus, night-time neuronal activity is shaped by the interaction of the song model (sensory template) and auditory feedback, with changes in night-time activity preceding the onset of practice associated with vocal learning. We hypothesize that night-time bursting induces adaptive changes in premotor networks during sleep as part of vocal learning. By this hypothesis, adaptive changes driven by replay of sensory information at night and by evaluation of sensory feedback during the day interact to produce the complex circadian patterns seen early in vocal development.

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Figure 1: High-frequency bursting in RA.
Figure 2: Tutor songs shape RA bursting.
Figure 3: RA sleep activity in absence of auditory feedback (white noise or muted).
Figure 4: Entropy variance changes after a night of sleep.

References

  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)

    ADS  CAS  Article  PubMed  Google Scholar 

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

    ADS  CAS  Article  PubMed  Google Scholar 

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

    ADS  CAS  Article  PubMed  Google Scholar 

  4. Walker, M. P. & Stickgold, R. Sleep, memory, and plasticity. Annu. Rev. Psychol. 57, 139–166 (2006)

    Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  6. Rasch, B., Buchel, C., Gais, S. & Born, J. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315, 1426–1429 (2007)

    ADS  CAS  Article  PubMed  Google Scholar 

  7. Ji, D. & Wilson, M. A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nature Neurosci. 10, 100–107 (2007)

    CAS  Article  PubMed  Google Scholar 

  8. Qin, Y. L., McNaughton, B. L., Skaggs, W. E. & Barnes, C. A. Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Phil. Trans. R. Soc. Lond. B 352, 1525–1533 (1997)

    ADS  CAS  Article  Google Scholar 

  9. Nadasdy, Z., Hirase, H., Czurko, A., Csicsvari, J. & Buzsaki, G. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19, 9497–9507 (1999)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Hennevin, E., Huetz, C. & Edeline, J. M. Neural representations during sleep: from sensory processing to memory traces. Neurobiol. Learn. Mem. 87, 416–440 (2007)

    Article  PubMed  Google Scholar 

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

    ADS  CAS  Article  PubMed  Google Scholar 

  12. 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 

  13. 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 

  14. Zeigler, H. P. & Marler, P. R. (eds) Behavioral Neurobiology of Birdsong (Ann. NY Acad. Sci., 2004)

    Google Scholar 

  15. Derégnaucourt, S., Mitra, P. P., Feher, O., Pytte, C. & Tchernichovski, O. How sleep affects the developmental learning of bird song. Nature 433, 710–716 (2005)

    ADS  Article  PubMed  Google Scholar 

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

    ADS  CAS  Article  PubMed  Google Scholar 

  17. Low, P. S., Shank, S. S., Sejnowski, T. J. & Margoliash, D. Mammalian-like features of sleep structure in zebra finches. Proc. Natl Acad. Sci. USA 105, 9081–9086 (2008)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Roper, A. & Zann, R. The onset of song learning and song tutor selection in fledgling zebra finches. Ethology 112, 458–470 (2006)

    Article  Google Scholar 

  19. 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)

    ADS  CAS  Article  PubMed  Google Scholar 

  20. Crandall, S. R., Adam, M., Kinnischtzke, A. K. & Nick, T. A. HVC neural sleep activity increases with development and parallels nightly changes in song behavior. J. Neurophysiol. 98, 232–240 (2007)

    Article  PubMed  Google Scholar 

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

    ADS  CAS  Article  PubMed  Google Scholar 

  22. Hultsch, H. & Todt, D. Memorization and reproduction of songs in nightingales (Luscinia megarhynchos): evidence for package formation. J. Comp. Physiol. A 165, 197–203 (1989)

    Article  Google Scholar 

  23. Funabiki, Y. & Konishi, M. Long memory in song learning by zebra finches. J. Neurosci. 23, 6928–6935 (2003)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    ADS  CAS  Article  PubMed  Google Scholar 

  25. Konishi, M. in Perception and Experience (eds Walk, R. D. & Pick, H. L. J.) 105–118 (Plenum, 1978)

    Book  Google Scholar 

  26. Adret, P. & Margoliash, D. Metabolic and neural activity in the song system nucleus robustus archistriatalis: effect of age and gender. J. Comp. Neurol. 454, 409–423 (2002)

    Article  PubMed  Google Scholar 

  27. 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)

    Article  PubMed  Google Scholar 

  28. Evarts, E. V., Bental, E., Bihari, B. & Huttenlocher, P. R. Spontaneous discharge of single neurons during sleep and waking. Science 135, 726–728 (1962)

    ADS  CAS  Article  PubMed  Google Scholar 

  29. Pastalkova, E., Itskov, V., Amarasingham, A. & Buzsáki, G. Internally generated cell assembly sequences in the rat hippocampus. Science 321, 1322–1327 (2008)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Gelbard-Sagiv, H., Mukamel, R., Harel, M., Malach, R. & Fried, I. Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322, 96–101 (2008)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Rattenborg, N. C. et al. Migratory sleeplessness in the white-crowned sparrow (Zonotrichia leucophrys gambelii). PLoS Biol. 2, E212 (2004)

    Article  PubMed  PubMed Central  Google Scholar 

  32. Pytte, C. L. & Suthers, R. A. A bird’s own song contributes to conspecific song perception. Neuroreport 10, 1773–1778 (1999)

    CAS  Article  PubMed  Google Scholar 

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

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 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)

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

We thank M. Fukushima for extensive discussions, and J.-M. Ramirez, H. C. Nusbaum, S. M. Sherman and M. Konishi for comments on the manuscript. A. S. Dave and M.F. designed and implemented the white noise recording/cancellation environment.

Author Contributions S.S.S. performed the experimental work.

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Correspondence to Daniel Margoliash.

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This file contains Supplementary Table 1, Supplementary Methods, Supplementary Data, Supplementary Figures S1-S6 with Legends and Supplementary References. (PDF 2150 kb)

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Shank, S., Margoliash, D. Sleep and sensorimotor integration during early vocal learning in a songbird. Nature 458, 73–77 (2009). https://doi.org/10.1038/nature07615

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