Experience-dependent changes in cerebral activation during human REM sleep


The function of rapid-eye-movement (REM) sleep is still unknown. One prevailing hypothesis suggests that REM sleep is important in processing memory traces. Here, using positron emission tomography (PET) and regional cerebral blood flow measurements, we show that waking experience influences regional brain activity during subsequent sleep. Several brain areas activated during the execution of a serial reaction time task during wakefulness were significantly more active during REM sleep in subjects previously trained on the task than in non-trained subjects. These results support the hypothesis that memory traces are processed during REM sleep in humans.

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Figure 1: Average reaction times (and standard deviations) for pre- and post-sleep sessions (group 2).
Figure 2: Statistical parametric maps of different contrasts.


  1. 1

    Tobler, I. Is sleep fundamentally different between mammalian species? Behav. Brain Res. 69, 35–41 ( 1995).

    CAS  Article  Google Scholar 

  2. 2

    Rechtschaffen, A., Bergmann, B. M., Everson, C. A., Kushida, C. A. & Gilliland, M. A. Sleep deprivation in the rat: X. Integration and discussion of the findings. Sleep 12, 68–87 (1989).

    CAS  Article  Google Scholar 

  3. 3

    Webb, W. B. in Sleep Mechanisms and Functions in Humans and Animals—An Evolutionary Perspective (ed. Mayes, A. R.) 1–17 (Van Nostrand Reinhold, Wokingham, 1983).

    Google Scholar 

  4. 4

    Borbely, A. A. & Achermann, P. Sleep homeostasis and models of sleep regulation. J. Biol. Rhythms 14, 557 –568 (1999).

    CAS  PubMed  Google Scholar 

  5. 5

    Steriade, M. Central core modulation of spontaneous oscillations and sensory transmission in thalamocortical systems. Curr. Opin. Neurobiol. 3, 619–625 (1993).

    CAS  Article  Google Scholar 

  6. 6

    Maquet, P. et al. Functional neuroanatomy of human rapid eye movement sleep and dreaming. Nature 383, 163– 166 (1996).

    CAS  Article  Google Scholar 

  7. 7

    Maquet, P. et al. Functional neuroanatomy of human slow wave sleep. J. Neurosci. 17, 2807–2812 (1997).

    CAS  Article  Google Scholar 

  8. 8

    Rechtschaffen, A. & Kales, A. A. A manual of standardized terminology, techniques and scoring system for sleep stages of human sujects . (US Department of Health, Education and Welfare, Bethesda, Maryland, 1968).

    Google Scholar 

  9. 9

    Krueger, J. M. & Obal, F. A neuronal group theory of sleep function . J. Sleep Res. 2, 63–69 (1993).

    CAS  Article  Google Scholar 

  10. 10

    Kavanau, J. L. Memory, sleep and the evolution of mechanisms of synaptic efficacy maintenance . Neuroscience 79, 7–44 (1997).

    CAS  Article  Google Scholar 

  11. 11

    Ribeiro, S., Goyal, V., Mello, C. V. & Pavlides, C. Brain gene expression during REM sleep depends on prior waking experience. Learn. Mem. 6, 500–508 ( 1999).

    CAS  Article  Google Scholar 

  12. 12

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

    CAS  Article  Google Scholar 

  13. 13

    Skaggs, W. E. & McNaughton, B. L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271, 1870–1873 ( 1996).

    CAS  Article  Google Scholar 

  14. 14

    Shen, J., Kudrimoti, H. S., McNaughton, B. L. & Barnes, C. A. Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience. J. Sleep Res. 7 Suppl. 1, 6–16 (1998).

    Article  Google Scholar 

  15. 15

    Skaggs, W. E. & McNaughton, B. L. Spatial firing properties of hippocampal CA1 populations in an environment containing two visually identical regions. J. Neurosci. 18, 8455– 8466 (1998).

    CAS  Article  Google Scholar 

  16. 16

    Kudrimoti, H. S., Barnes, C. A. & McNaughton, B. L. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 19, 4090–4101 ( 1999).

    CAS  Article  Google Scholar 

  17. 17

    Hennevin, E., Hars, B., Maho, C. & Bloch, V. Processing of learned information in paradoxical sleep: relevance for memory. Behav. Brain Res. 69, 125–135 ( 1995).

    CAS  Article  Google Scholar 

  18. 18

    Smith, C. Sleep states and memory processes. Behav. Brain Res. 69, 137–145 (1995).

    CAS  Article  Google Scholar 

  19. 19

    Schacter, D. & Tulving, E. (eds.) Memory Systems 1994 (MIT Press, Cambridge, Massachusetts, 1994).

    Google Scholar 

  20. 20

    Cleeremans, A. & Destrebecqz, A. Implicit learning: News from the front. Trends Cog. Sci. 2, 406–416 (1998).

    CAS  Article  Google Scholar 

  21. 21

    Stickgold, R. Sleep: off-line memory reprocessing. Trends Cogn. Sci. 2, 484–492 (1998).

    CAS  Article  Google Scholar 

  22. 22

    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).

    CAS  Article  Google Scholar 

  23. 23

    Plihal, W. & Born, J. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 9, 534–547 ( 1997).

    CAS  Article  Google Scholar 

  24. 24

    Cleeremans, A. & McClelland, J. L. Learning the structure of event sequences. J. Exp. Psychol. Gen. 120, 235–253 (1991).

    CAS  Article  Google Scholar 

  25. 25

    Jimenez, L., Mendez, C. & Cleeremans, A. Comparing direct and indirect measures of sequence learning . J. Exp. Psychol. Learn. Mem. Cognit. 22, 948–969 (1996).

    Article  Google Scholar 

  26. 26

    Price, C. J. & Friston, K. J. Cognitive conjunction: a new approach to brain activation experiments. Neuroimage 5, 261–270 (1997).

    CAS  Article  Google Scholar 

  27. 27

    Haxby, J. V. et al. Dissociation of object and spatial visual processing pathways in human extrastriate cortex. Proc. Natl. Acad. Sci. USA 88, 1621–1625 (1991).

    CAS  Article  Google Scholar 

  28. 28

    Corbetta, M., Miezin, F. M., Shulman, G. L. & Petersen, S. E. A PET study of visuospatial attention. J. Neurosci. 13, 1202–1226 (1993).

    CAS  Article  Google Scholar 

  29. 29

    Stephan, K. M. et al. Functional anatomy of the mental representation of upper extremity movements in healthy subjects. J. Neurophysiol. 73, 373–386 (1995).

    CAS  Article  Google Scholar 

  30. 30

    Matelli, M. et al. Activation of precentral and mesial motor areas during the execution of elementary proximal and distal arm movements: a PET study. Neuroreport 4, 1295–1298 (1993).

    CAS  Article  Google Scholar 

  31. 31

    Lejeune, H. et al. The basic pattern of activation in motor and sensory temporal tasks: positron emission tomography data. Neurosci. Lett. 235, 21–24 (1997).

    CAS  Article  Google Scholar 

  32. 32

    Grafton, S. T., Fagg, A. H., Woods, R. P. & Arbib, M. A. Functional anatomy of pointing and grasping in humans. Cereb. Cortex 6, 226–237 ( 1996).

    CAS  Article  Google Scholar 

  33. 33

    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).

    CAS  Article  Google Scholar 

  34. 34

    Jueptner, M. & Weiller, C. Review: does measurement of regional cerebral blood flow reflect synaptic activity? Implications for PET and fMRI . Neuroimage 2, 148–156 (1995).

    CAS  Article  Google Scholar 

  35. 35

    Karni, A. & Bertini, G. Learning perceptual skills: behavioral probes into adult cortical plasticity. Curr. Opin. Neurobiol. 7, 530–535 (1997).

    CAS  Article  Google Scholar 

  36. 36

    Brashers-Krug, T., Shadmehr, R. & Bizzi, E. Consolidation in human motor memory. Nature 382, 252–255 ( 1996).

    CAS  Article  Google Scholar 

  37. 37

    Shadmehr, R. & Holcomb, H. H. Neural correlates of motor memory consolidation. Science 277, 821– 825 (1997).

    CAS  Article  Google Scholar 

  38. 38

    McGaugh, J. L. Memory—a century of consolidation. Science 287 , 248–251 (2000).

    CAS  Article  Google Scholar 

  39. 39

    Bailey, C. H., Bartsch, D. & Kandel, E. R. Toward a molecular definition of long-term memory storage. Proc. Natl. Acad. Sci. USA 93, 13445–13452 (1996).

    CAS  Article  Google Scholar 

  40. 40

    Bailey, C. H. & Kandel, E. R. in The Cognitive Neurosciences (eds. Gazzaniga, M. S. & Bizzi, E.) 19–36 (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  41. 41

    Kleim, J. A., Lussnig, E., Schwarz, E. R., Comery, T. A. & Greenough, W. T. Synaptogenesis and FOS expression in the motor cortex of the adult rat after motor skill learning. J. Neurosci. 16, 4529–4535 (1996).

    CAS  Article  Google Scholar 

  42. 42

    Marks, G. A., Shaffery, J. P., Oksenberg, A., Speciale, S. G. & Roffwarg, H. P. A functional role for REM sleep in brain maturation. Behav. Brain Res. 69, 1–11 (1995).

    CAS  Article  Google Scholar 

  43. 43

    Steriade, M. & McCarley, R. W. Brainstem Control of Wakefulness and Sleep (Plenum, New York, 1990).

    Google Scholar 

  44. 44

    Delacour, J., Houcine, O. & Costa, J. C. Evidence for a cholinergical mechanism of “learned” changes in responses of barrel field neurons of the awake and undrugged rat . Neuroscience 34, 1–8 (1990).

    CAS  Article  Google Scholar 

  45. 45

    Bakin, J. S. & Weinberger, N. M. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc. Natl. Acad. Sci. USA 93, 11219– 11224 (1996).

    CAS  Article  Google Scholar 

  46. 46

    Juliano, S. L., Ma, W. & Eslin, D. Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex. Proc. Natl. Acad. Sci. USA 88, 780 –784 (1991).

    CAS  Article  Google Scholar 

  47. 47

    Frackowiak, R. S. J., Friston, K. J., Frith, C., Dolan, R. J. & Mazziotta, J. C. Human Brain Function (Academic, San Diego, California, 1997).

    Google Scholar 

  48. 48

    Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (George Thieme, Stuttgart, 1988).

    Google Scholar 

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We thank R.S.J. Frackowiak, K.J. Friston and their colleagues for providing the SPM and C. Mesters, G. and J. Hodiaumont, P. Hawotte and J.L. Genon for technical assistance. We are also grateful to C. Frith for comments on a previous version of this manuscript. P.M. and A.C. are Senior Research Associate and Research Associate at the Fonds National de la Recherche Scientifique de Belgique (FNRS), respectively. P.P. is supported by the Interuniversitary Poles of Attraction, program P4/22. This research was supported by FNRS grants, by Special Funds for Scientific Research of the University of Liège and by the Queen Elisabeth Medical Foundation.

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Correspondence to Pierre Maquet.

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Maquet, P., Laureys, S., Peigneux, P. et al. Experience-dependent changes in cerebral activation during human REM sleep. Nat Neurosci 3, 831–836 (2000). https://doi.org/10.1038/77744

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