[en] We have previously shown that several brain areas are activated both during sequence learning at wake and during subsequent rapid-eye-movements (REM) sleep (Nat. Neurosci. 3 (2000) 831-836), suggesting that REM sleep participates in the reprocessing of recent memory traces in humans. However, the nature of the reprocessed information remains open. Here, we show that regional cerebral reactivation during posttraining REM sleep is not merely related to the acquisition of basic visuomotor skills during prior practice of the serial reaction time task, but rather to the implicit acquisition of the probabilistic rules that defined stimulus sequences. Moreover, functional connections between the reactivated cuneus and the striatum-the latter being critical for implicit sequence learning-are reinforced during REM sleep after practice on a probabilistic rather than on a random sequence of stimuli. Our results therefore support the hypothesis that REM sleep is deeply involved in the reprocessing and optimization of the high-order information contained in the material to be learned. In addition, we show that the level of acquisition of probabilistic rules attained prior to sleep is correlated to the increase in regional cerebral blood flow during subsequent REM sleep. This suggests that posttraining cerebral reactivation is modulated by the strength of the memory traces developed during the learning episode. Our data provide the first experimental evidence for a link between behavioral performance and cerebral reactivation during REM sleep. (C) 2003 Elsevier Inc. All rights reserved.
Research Center/Unit :
GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
Peigneux, Philippe ; Université de Liège - ULiège > Département des sciences cognitives > Département des sciences cognitives
Laureys, Steven ; Université de Liège - ULiège > Centre de recherches du cyclotron
Fuchs, Sonia
Destrebecqz, Arnaud
Collette, Fabienne ; Université de Liège - ULiège > Département des sciences cognitives > Neuropsychologie
Delbeuck, Xavier
Phillips, Christophe ; Université de Liège - ULiège > Centre de recherches du cyclotron
Aerts, Joël ; Université de Liège - ULiège > Centre de recherches du cyclotron
Del Fiore, Guy
Degueldre, Christian ; Université de Liège - ULiège > Centre de recherches du cyclotron
Luxen, André ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie organique de synthèse - Centre de recherches du cyclotron
Cleeremans, Axel
Maquet, Pierre ; Université de Liège - ULiège > Centre de recherches du cyclotron
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Bramham C.R., Maho C., Laroche S. Suppression of long-term potentiation induction during alert wakefulness but not during "enhanced" REM sleep after avoidance learning. Neuroscience. 59:1994;501-509.
Braun A.R., Balkin T.J., Wesensten N.J., Gwadry F., Carson R.E., Varga M., Baldwin P., Belenky G., Herscovitch P. Dissociated pattern of activity in visual cortices and their projections during human rapid eye movement sleep. Science. 279:1998;91-95.
Brett M., Bloomfield P., Brooks D.J., Stein J.F., Grasby P. Scan order effects in PET activation studies are caused by motion artefact. NeuroImage. 9:1999;S56.
Cajochen C., Knoblauch V., Kraüchi K., Graw P., Wirz-Justice A., Wallach D. Sequence learning depends on sleep, the level of sleep pressure and circadian phase. J. Sleep Res. 11:2002;30-31.
Cleeremans A., McClelland J.L. Learning the structure of event sequences. J. Exp. Psychol. Gen. 120:1991;235-253.
Dujardin K., Guerrien A., Leconte P. Sleep, brain activation and cognition. Physiol. Behav. 47:1990;1271-1278.
Frackowiak R.S.J., Friston K.J., Frith C.D., Dolan R.J., Mazziotta J.C. Human Brain Function. 1997;Academic Press, San Diego.
Friston K. Beyond phrenology what can neuroimaging tell us about distributed circuitry? Annu. Rev. Neurosci. 25:2002;221-250.
Friston K., Holmes A., Worsley K.J. How many subjects constitute a study? NeuroImage. 10:1999;1-5.
Friston K.J., Buechel C., Fink G.R., Morris J., Rolls E., Dolan R.J. Psychophysiological and modulatory interactions in neuroimaging. NeuroImage. 6:1997;218-229.
Gais S., Plihal W., Wagner U., Born J. Early sleep triggers memory for early visual discrimination skills. Nat. Neurosci. 3:2000;1335-1339.
Giuditta A., Ambrosini M.V., Montagnese P., Mandile P., Cotugno M., Zucconi G.G., Vescia S. The sequential hypothesis of the function of sleep. Behav. Brain Res. 69:1995;157-166.
Grafton S.T., Hazeltine E., Ivry R. Functional mapping of sequence learning in normal humans. J. Cogn. Neurosci. 7:1995;497-510.
Hennevin E., Maho C., Hars B., Dutrieux G. Learning-induced plasticity in the medial geniculate nucleus is expressed during paradoxical sleep. Behav. Neurosci. 107:1993;1018-1030.
Hennevin E., Hars B., Maho C., Bloch V. Processing of learned information in paradoxical sleep relevance for memory . Behav. Brain Res. 69:1995;125-135.
Jimenez L., Mendez C., Cleeremans A. Comparing direct and indirect measures of sequence learning. J. Exp. Psychol. Learn. Mem. Cogn. 22:1996;948-969.
Louie K., Wilson M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron. 29:2001;145-156.
Maho C., Hennevin E., Hars B., Poincheval S. Evocation in paradoxical sleep of a hippocampal conditioned cellular response acquired during waking. Psychobiology. 19:1991;193-205.
Maquet P. The role of sleep in learning and memory. Science. 294:2001;1048-1052.
Maquet P., Péters J.-M., Aerts J., Delfiore G., Degueldre C., Luxen A., Franck G. Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature. 383:1996;163-166.
Maquet P., Laureys S., Peigneux P., Fuchs S., Petiau C., Phillips C., Aerts J., Delfiore G., Degueldre C., Meulemans T., Luxen A., Franck G., Van der Linden M., Smith C., Cleeremans A. Experience-dependent changes in cerebral activation during human REM sleep. Nat. Neurosci. 3:2000;831-836.
Meier-Koll A., Bussman B., Schmidt C., Neuschwander D. Walking through a maze alters the architecture of sleep. Percept. Mot. Skills. 88:1999;1141-1159.
Merikle P.M., Reingold E.M. Comparing direct (explicit) and indirect (implicit) measures to study unconscious memory. J. Exp. Psychol. Learn. Mem. Cogn. 17:1991;224-233.
Nadasdy Z., Hirase H., Czurko A., Csicsvari J., Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19:1999;9497-9507.
Paul K., Dittrichova J. Sleep patterns following learning in infants. Levin P., Koella W.D. Sleep 1974, Second European Congress on Sleep Research. 1975;388-390 Karger, Basel.
Peigneux P., Laureys S., Delbeuck X., Maquet P. Sleeping brain, learning brain. The role of sleep for memory systems. NeuroReport. 12:2001;A111-A124.
Peigneux P., Maquet P., Meulemans T., Destrebecqz A., Laureys S., Degueldre C., Delfiore G., Luxen A., Franck G., Van der Linden M., Cleeremans A. Striatum forever despite sequence learning variability a random effect analysis of PET data . Hum. Brain Mapp. 10:2000;179-194.
Plihal W., Born J. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 9:1997;534-547.
Plihal W., Born J. Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology. 36:1999;571-582.
Poe G.R., Nitz D.A., McNaughton B.L., Barnes C.A. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res. 855:2000;176-180.
Qin Y.L., McNaughton B.L., Skaggs W.E., Barnes C.A. Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Philos. T. R. Soc. B. 352:1997;1525-1533.
Rauch S.L., Savage C.R., Brown H.D., Curran T., Alpert N.M., Kendrick A., Fischman A.J., Kosslyn S.M. A PET investigation of implicit and explicit sequence learning. Hum. Brain Mapp. 3:1995;271-286.
Rauch S.L., Savage C.R., Alpert N.M., Dougherty D., Kendrick A., Curran T., Brown H.D., Manzo P., Fischman A.J., Jenike M.A. Probing striatal function in obsessive compulsive disorder using PET and a sequence learning task. J. Neuropsy. Clin. Neurosci. 9:1997;568-573.
Rechtschaffen A., Kales A.A. A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. 1968;U.S. Department of Health, Education and Welfare, Bethesda, MO.
Schubotz R.I., von Cramon D.Y. Interval and ordinal properties of sequences are associated with distinct premotor areas. Cereb. Cortex. 11:2001;210-222.
Segalowitz S.J., Segalowitz N. Skilled performance, practice, and the differentiation of speed-up from automatization effects evidence from second language word recognition . Appl. Psycholinguist. 14:1993;369-385.
Skaggs W.E., McNaughton B.L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 271:1996;1870-1873.
Smith C. Sleep states and memory processes. Behav. Brain Res. 69:1995;137-145.
Smith C. Sleep states and memory processes in humans procedural versus declarative memory systems . Sleep Med. Rev. 5:2001;491-506.
Stickgold R., Hobson J.A., Fosse R., Fosse M. Sleep, learning, and dreams off-line memory reprocessing . Science. 294:2001;1052-1057.
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. 12:2000;246-254.
Verschoor G.J., Holdstock T.L. REM bursts and REM sleep following visual and auditory learning. S. Afr. J. Psychol. 14:1984;69-74.
Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science. 265:1994;676-679.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.