Skip to main content
Log in

Off-line processing of memory traces during human sleep: Contribution of functional neuroimaging

  • Review Article
  • Published:
Sleep and Biological Rhythms Aims and scope Submit manuscript

Abstract

Sleep is thought to participate in the consolidation of recent memory traces. We tested this hypothesis in humans by using functional neuroimaging (functional magnetic resonance imaging and positron emission tomography). First, following the training procedural visuo-motor learning task (pursuit task), total sleep deprivation on the first post-training night significantly deteriorates the gain in performance, which is usually observed after one complete night of sleep. In parallel, sleep deprivation hampers the changes in functional segregation and connectivity, which underpin the gain in performance usually observed in subjects allowed to sleep on the first post-training night. Second, following the training on an implicit memory task (probabilistic serial reaction time task), some brain areas are reactivated during rapid eye movement (REM) sleep on the first post-training night. The reactivation was shown to be related to the processing of high-level material and to be modulated by the amount of learning achieved during the training session. These changes in activity do not involve isolated brain areas but entire macroscopic cortico-subcortical networks. Taken together, the results suggest an off-line processing of recent memory traces during sleep.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. McGaugh JL. Memory — a century of consolidation. Science 2000; 287: 248–51.

    Article  CAS  PubMed  Google Scholar 

  2. Sutherland GR, McNaughton B. Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr. Opin. Neurobiol. 2000; 10: 180–6.

    Article  CAS  PubMed  Google Scholar 

  3. Fishbein W, Gutwein BM. Paradoxical sleep and memory storage processes. Behav. Biol. 1977; 19: 425–64.

    Article  CAS  PubMed  Google Scholar 

  4. Maquet P, Schwartz S, Passingham R, Frith CD. Sleep-Related Consolidation of a Visuo-Motor Skill: Brain Mechanisms as Assessed by fMRI. J. Neurosci. 2003; 23 (4): 1432–40.

    CAS  PubMed  Google Scholar 

  5. Frith C. Learning rhythmic hand movements. Q. J. Exp. Psychol. 1973; 25: 253–9.

    Article  CAS  PubMed  Google Scholar 

  6. Drummond SP, Brown GG, Gillin JC, Stricker JL, Wong EC, Buxton RB. Altered brain response to verbal learning following sleep deprivation. Nature 2000; 403: 655–7.

    Article  CAS  PubMed  Google Scholar 

  7. Stickgold R, James L, Hobson JA. Visual discrimination learning requires sleep after training. Nat. Neurosci. 2000; 3: 1237–8.

    Article  CAS  PubMed  Google Scholar 

  8. Cleeremans A, McClelland JL. Learning the structure of event sequences. J. Exp. Psychol. General 1991; 120: 235–53.

    Article  CAS  Google Scholar 

  9. Maquet P, Laureys S, Peigneux P et al. Experience-dependent changes in cerebral activation during human REM sleep. Nat. Neurosci. 2000; 3: 831–6.

    Article  CAS  PubMed  Google Scholar 

  10. Laureys S, Peigneux P, Phillips C et al. Experience-dependent changes in cerebral functional connectivity during human rapid eye movement sleep. Neuroscience 2001; 105: 521–5.

    Article  CAS  PubMed  Google Scholar 

  11. Bramham CR, Maho C, Laroche S. Suppression of longterm potentiation induction during alert wakefulness but not during ‘enhanced’ REM sleep after avoidance learning. Neuroscience 1994; 59: 501–9.

    Article  CAS  PubMed  Google Scholar 

  12. Hennevin E, Maho C, Hars B, Dutrieux G. Learning-induced plasticity in the medial geniculate nucleus is expressed during paradoxical sleep. Behav. Neurosci. 1993; 107: 1018–30.

    Article  CAS  PubMed  Google Scholar 

  13. Maho C, Hennevin E, Hars B, Poincheval S. Evocation in paradoxical sleep of a hippocampal conditioned cellular response acquired during waking. Psychobiology 1991; 19: 193–205.

    Google Scholar 

  14. Verschoor GJ, Holdstock TL. REM bursts and REM sleep following visual and auditory learning. S. Afr. J. Psychol. 1984; 14: 69–74.

    Article  Google Scholar 

  15. Meier-Koll A, Bussman B, Schmidt C, Neuschwander D. Walking through a maze alters the architecture of sleep. Percept. Mot. Skills 1999; 88: 1141–59.

    Article  CAS  PubMed  Google Scholar 

  16. Schubotz RI, von Cramon DY. Interval and ordinal properties of sequences are associated with distinct premotor areas. Cereb. Cortex 2001; 11: 210–22.

    Article  CAS  PubMed  Google Scholar 

  17. Grafton ST, Hazeltine E, Ivry R. Functional mapping of sequence learning in normal humans. J. Cognitive Neuroscience 1995; 7: 497–510.

    Article  CAS  Google Scholar 

  18. Rauch SL, Savage CR, Brown HD et al. A PET investigation of implicit and explicit sequence learning. Human Brain Mapping 1995; 3: 271–86.

    Article  Google Scholar 

  19. Rauch SL, Savage CR, Alpert NM et al. Probing striatal function in obsessive compulsive disorder using PET and a sequence learning task. J. Neuropsychiatry Clin. Neurosci. 1997; 9: 568–73.

    Article  CAS  PubMed  Google Scholar 

  20. Peigneux P, Maquet P, Meulemans T et al. Striatum forever despite sequence learning variability: a random effect analysis of PET data. Human Brain Mapping 2000; 10: 179–94.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pierre Maquet.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maquet, P., Peigneux, P., Laureys, S. et al. Off-line processing of memory traces during human sleep: Contribution of functional neuroimaging. Sleep Biol. Rhythms 1, 75–83 (2003). https://doi.org/10.1046/j.1446-9235.2003.00009.x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1046/j.1446-9235.2003.00009.x

Key words

Navigation