Consolidation during sleep of perceptual learning of spoken language (original) (raw)

Nature volume 425, pages 614–616 (2003)Cite this article

Abstract

Memory consolidation resulting from sleep has been seen broadly: in verbal list learning1, spatial learning2,3, and skill acquisition in visual4,5,6,7,8 and motor9,10,11 tasks. These tasks do not generalize across spatial locations or motor sequences, or to different stimuli in the same location5,11,12. Although episodic rote learning constitutes a large part of any organism's learning, generalization is a hallmark of adaptive behaviour13. In speech, the same phoneme often has different acoustic patterns depending on context. Training on a small set of words improves performance on novel words using the same phonemes but with different acoustic patterns, demonstrating perceptual generalization14. Here we show a role of sleep in the consolidation of a naturalistic spoken-language learning task that produces generalization of phonological categories across different acoustic patterns. Recognition performance immediately after training showed a significant improvement that subsequently degraded over the span of a day's retention interval, but completely recovered following sleep. Thus, sleep facilitates the recovery and subsequent retention of material learned opportunistically at any time throughout the day. Performance recovery indicates that representations and mappings associated with generalization are refined and stabilized during sleep.

This is a preview of subscription content, access via your institution

Access options

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Additional access options:

Figure 1: Sleep effect on retention of learning for word identification.

Similar content being viewed by others

References

  1. Ficca, G., Lombardo, P., Rossi, L. & Salzarulo, P. Morning recall of verbal material depends on prior sleep organization. Behav. Brain Res. 112, 159–163 (2000)
    Article CAS Google Scholar
  2. Smith, C. & Rose, G. Posttraining paradoxical sleep in rats is increased after spatial learning in the Morris water maze. Behav. Neurosci. 111, 1197–1204 (1997)
    Article CAS Google Scholar
  3. Plihal, W. & Born, J. Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiol. 36, 571–582 (1999)
    Article CAS Google Scholar
  4. Karni, A., Tanne, D., Rubenstein, B. S., Askenasy, J. J. M. & Sagi, D. Dependence on REM sleep of overnight perceptual skill. Science 265, 679–682 (1994)
    Article ADS CAS Google Scholar
  5. Karni, A. & Sagi, D. The time course of learning a visual skill. Nature 365, 250–252 (1993)
    Article ADS CAS Google Scholar
  6. Mednick, S. C. et al. The restorative effect of naps on perceptual deterioration. Nature Neurosci. 5, 677–681 (2002)
    Article CAS Google Scholar
  7. Stickgold, R., James, L. & Hobson, J. A. Visual discrimination learning requires sleep after training. Nature Neurosci. 3, 1237–1238 (2000)
    Article CAS Google Scholar
  8. Stickgold, R., Whidbee, D., Schirmer, B., Patel, V. & Hobson, J. A. Visual discrimination task improvement: A multi-step process occurring during sleep. J. Cogn. Neurosci. 12, 246–254 (2000)
    Article CAS Google Scholar
  9. Brashers-Krug, T., Shadmehr, R. & Bizzi, E. Consolidation in human motor memory. Nature 382, 252–255 (1996)
    Article ADS CAS Google Scholar
  10. Walker, M. P., Brakefield, T., Morgan, A., Hobson, J. A. & Stickgold, R. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35, 205–211 (2002)
    Article CAS Google Scholar
  11. Karni, A. et al. The acquisition of skilled motor performance: Fast and slow experience-driven changes in primary motor cortex. Proc. Natl Acad. Sci. USA 95, 861–868 (1998)
    Article ADS CAS Google Scholar
  12. Karni, A. et al. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155–158 (1995)
    Article ADS CAS Google Scholar
  13. Karni, A. & Bertini, G. Learning perceptual skills: behavioral probes into adult cortical plasticity. Curr. Opin. Neurobiol. 7, 530–535 (1997)
    Article CAS Google Scholar
  14. Schwab, E. C., Nusbaum, H. C. & Pisoni, D. B. Some effects of training on the perception of synthetic speech. Hum. Factors 27, 395–408 (1985)
    Article CAS Google Scholar
  15. Greenspan, S. L., Nusbaum, H. C. & Pisoni, D. B. Perceptual learning of synthetic speech produced by rule. J. Exp. Psychol. Learn. Mem. Cogn. 14, 421–433 (1988)
    Article CAS Google Scholar
  16. Johnson, M. P. et al. Short-term memory, alertness and performance: a reappraisal of their relationship to body temperature. J. Sleep Res. 1, 24–29 (1992)
    Article CAS Google Scholar
  17. Gabrieli, J. D. E. Cognitive neuroscience of human memory. Annu. Rev. Psychol. 49, 87–115 (1998)
    Article CAS Google Scholar
  18. Liberman, A. M., Cooper, F. S., Shankweiler, D. P. & Studdert-Kennedy, M. Perception of the speech code. Psychol. Rev. 74, 431–461 (1967)
    Article CAS Google Scholar
  19. Ohman, S. E. Coarticulation in VCV utterances: Spectrographic measurements. J. Acoust. Soc. Am. 39, 151–168 (1966)
    Article ADS CAS Google Scholar
  20. Rudnicky, A. I. & Cole, R. A. Effect of subsequent context on syllable perception. J. Exp. Psychol. Hum. Percept. Perform. 4, 638–647 (1978)
    Article CAS Google Scholar
  21. Nusbaum, H. C. & Pisoni, D. B. Automatic measurement of speech recognition performance: A comparison of six speaker-dependent recognition devices. Comp. Speech Lang. 2, 87–108 (1987)
    Article Google Scholar
  22. Pisoni, D. B. in Handbook of Learning and Cognitive Processes Vol. 6 Linguistic Functions in Cognitive Theory (ed. Estes, W. K.) 167–233 (Lawrence Erlbaum Assoc., Hillsdale, New Jersey, 1978)
    Google Scholar
  23. Kolers, P. A. & Perkins, D. N. Orientation of letters and errors in their recognition. Percept. Psychophys. 5, 265–269 (1969)
    Article Google Scholar
  24. Egan, J. P. Articulation testing methods. Laryngoscope 58, 955–991 (1948)
    Article CAS Google Scholar

Download references

Acknowledgements

We thank E. Van Cauter, A. S. Henly and N. P. Issa for critiques of the manuscript. This work was supported by grants from the McCormick Tribune Foundation to H.C.N. and from the National Institutes of Health to D.M.

Author information

Authors and Affiliations

  1. Department of Psychology, The University of Chicago, Chicago, Illinois, 60637, USA
    Kimberly M. Fenn, Howard C. Nusbaum & Daniel Margoliash
  2. Department of Organismal Biology and Anatomy, The University of Chicago, Chicago, Illinois, 60637, USA
    Daniel Margoliash

Authors

  1. Kimberly M. Fenn
    You can also search for this author inPubMed Google Scholar
  2. Howard C. Nusbaum
    You can also search for this author inPubMed Google Scholar
  3. Daniel Margoliash
    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toKimberly M. Fenn.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

About this article

Cite this article

Fenn, K., Nusbaum, H. & Margoliash, D. Consolidation during sleep of perceptual learning of spoken language.Nature 425, 614–616 (2003). https://doi.org/10.1038/nature01951

Download citation

This article is cited by