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Cortical reactivations during sleep spindles following declarative learning

Title:

Cortical reactivations during sleep spindles following declarative learning

Jegou, Aude, Schabus, Manuel, Gosseries, Olivia, Dahmen, Brigitte, Albouy, Geneviève, Desseilles, Martin, Sterpenich, Virginie, Phillips, Christophe, Maquet, Pierre, Grova, Christophe and Dang-Vu, Thien Thanh (2019) Cortical reactivations during sleep spindles following declarative learning. NeuroImage . ISSN 10538119 (In Press)

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Official URL: http://dx.doi.org/10.1016/j.neuroimage.2019.03.051

Abstract

Increasing evidence suggests that sleep spindles are involved in memory consolidation, but few studies have investigated the effects of learning on brain responses associated with spindles in humans. Here we used simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) during sleep to assess haemodynamic brain responses related to spindles after learning. Twenty young healthy participants were scanned with EEG/fMRI during (i) a declarative memory face sequence learning task, (ii) subsequent sleep, and (iii) recall after sleep (learning night). As a control condition an identical EEG/fMRI scanning protocol was performed after participants over-learned the face sequence task to complete mastery (control night). Results demonstrated increased responses in the fusiform gyrus both during encoding before sleep and during successful recall after sleep, in the learning night compared to the control night. During sleep, a larger response in the fusiform gyrus was observed in the presence of fast spindles during the learning as compared to the control night. Our findings support a cortical reactivation during fast spindles of brain regions previously involved in declarative learning and subsequently activated during memory recall, thereby promoting the cortical consolidation of memory traces.

Divisions:Concordia University > Faculty of Arts and Science > Health, Kinesiology and Applied Physiology
Item Type:Article
Refereed:Yes
Authors:Jegou, Aude and Schabus, Manuel and Gosseries, Olivia and Dahmen, Brigitte and Albouy, Geneviève and Desseilles, Martin and Sterpenich, Virginie and Phillips, Christophe and Maquet, Pierre and Grova, Christophe and Dang-Vu, Thien Thanh
Journal or Publication:NeuroImage
Date:28 March 2019
Funders:
  • Belgian National Funds for Scientific Research
  • Natural Sciences and Engineering Research Council of Canada
  • Canadian Institutes of Health Research
  • Fonds de Recherche du Québec – Santé
  • Erwin Schrödinger fellowship of the Austrian Science Fund
Digital Object Identifier (DOI):10.1016/j.neuroimage.2019.03.051
Keywords:Consolidation; EEG/fMRI; Memory; Oscillations; Replay; Sleep
ID Code:985153
Deposited By: Michael Biron
Deposited On:08 Apr 2019 18:09
Last Modified:23 Mar 2020 00:00

References:

P.J. Allen, O. Josephs, R. Turner A method for removing imaging artifact from continuous EEG recorded during functional MRI Neuroimage, 12 (2000), pp. 230-239

K.C. Andrade, V.I. Spoormaker, M. Dresler, R. Wehrle, F. Holsboer, P.G.Samann, M. Czisch Sleep spindles and hippocampal functional connectivity in human NREM sleep J. Neurosci. : Off. J/ Soc. Neurosci., 31 (2011), pp. 10331-10339

T.O. Bergmann, M. Molle, J. Diedrichs, J. Born, H.R. Siebner Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations Neuroimage, 59 (2012), pp. 2733-2742

M. Caporro, Z. Haneef, H.J. Yeh, A. Lenartowicz, C. Buttinelli, J. Parvizi, J.M. Stern Functional MRI of sleep spindles and K-complexes Clin. Neurophysiol., 123 (2012), pp. 303-309

V.P. Clark, J.M. Maisog, J.V. Haxby fMRI study of face perception and memory using random stimulus sequences J. Neurophysiol., 79 (1998), pp. 3257-3265

T.T. Dang Vu, M. Bonjean, M. Schabus, M. Boly, A. Darsaud, M.Desseilles, C. Degueldre, E. Balteau, C. Phillips, A. Luxen, T.J. Sejnowski, P. Maquet Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep Proc. Natl. Acad. Sci. U. S. A., 108 (2011), pp. 15438-15443

T.T. Dang-Vu, M. Schabus, M. Desseilles, G. Albouy, M. Boly, A. Darsaud, S. Gais, G. Rauchs, V. Sterpenich, G. Vandewalle, J. Carrier, G. Moonen, E. Balteau, C.Degueldre, A. Luxen, C. Phillips, P. Maquet Spontaneous neural activity during human slow wave sleep Proc. Natl. Acad. Sci. U. S. A., 105 (2008), pp. 15160-15165

L. De Gennaro, M. Ferrara Sleep spindles: an overview Sleep Med. Rev., 7 (2003), pp. 423-440

S. Diekelmann, J. Born The memory function of sleep Nat. Rev. Neurosci., 11 (2010), pp. 114-126

O. Eschenko, M. Molle, J. Born, S.J. Sara Elevated sleep spindle density after learning or after retrieval in rats J. Neurosci., 26 (2006), pp. 12914-12920

S. Fogel, G. Albouy, B.R. King, O. Lungu, C. Vien, A. Bore, B. Pinsard, H.Benali, J. Carrier, J. Doyon Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles PLoS One, 12 (2017), p. e0174755

S.M. Fogel, C.T. Smith The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation Neurosci. Biobehav. Rev., 35 (2011), pp. 1154-1165

K.J. Friston, P. Fletcher, O. Josephs, A. Holmes, M.D. Rugg, R. Turner Event-related fMRI: characterizing differential responses Neuroimage, 7 (1998), pp. 30-40

S. Gais, M. Molle, K. Helms, J. Born Learning-dependent increases in sleep spindle density J. Neurosci., 22 (2002), pp. 6830-6834

K. Grill-Spector, N. Knouf, N. Kanwisher The fusiform face area subserves face perception, not generic within-category identification Nat. Neurosci., 7 (2004), pp. 555-562

C. Iber, S. Ancoli-Israel, A.L. Chesson, S.F. Quan The AASM Manual for the Scoring of Sleep and Associated Events American Academy of Sleep Medicine, Westchester (2007)

N. Kanwisher, J. McDermott, M.M. Chun The fusiform face area: a module in human extrastriate cortex specialized for face perception J. Neurosci., 17 (1997), pp. 4302-4311

N. Ketz, A.P. Jones, N.B. Bryant, V.P. Clark, P.K. Pilly Closed-loop slow-wave tACS improves sleep-dependent long-term memory generalization by modulating endogenous oscillations J. Neurosci., 38 (2018), pp. 7314-7326

P.C. Koo, M. Molle, L. Marshall Efficacy of slow oscillatory-transcranial direct current stimulation on EEG and memory - contribution of an inter-individual factor Eur. J. Neurosci., 47 (2018), pp. 812-823

D. Kumaran, E.A. Maguire The dynamics of hippocampal activation during encoding of overlapping sequences Neuron, 49 (2006), pp. 617-629

Y. Leclercq, E. Balteau, T. Dang-Vu, M. Schabus, A. Luxen, P. Maquet, C.Phillips Rejection of pulse related artefact (PRA) from continuous electroencephalographic (EEG) time series recorded during functional magnetic resonance imaging (fMRI) using constraint independent component analysis (cICA) Neuroimage, 44 (2009), pp. 679-691

Y. Leclercq, J. Schrouff, Q. Noirhomme, P. Maquet, C. Phillips fMRI artefact rejection and sleep scoring toolbox Comput. Intell. Neurosci., 2011 (2011), p. 598206

C. Lustenberger, M.R. Boyle, S. Alagapan, J.M. Mellin, B.V. Vaughn, F.Frohlich Feedback-controlled transcranial alternating current stimulation reveals a functional role of sleep spindles in motor memory consolidation Curr. Biol., 26 (2016), pp. 2127-2136

A. Luthi Sleep spindles: where they come from, what they do Neuroscientist, 20 (2014), pp. 243-256

L. Marshall, M. Molle, M. Hallschmid, J. Born Transcranial direct current stimulation during sleep improves declarative memory J. Neurosci., 24 (2004), pp. 9985-9992

M. Molle, T.O. Bergmann, L. Marshall, J. Born Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing Sleep, 34 (2011), pp. 1411-1421

M. Molle, O. Eschenko, S. Gais, S.J. Sara, J. Born The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats Eur. J. Neurosci., 29 (2009), pp. 1071-1081

M. Molle, L. Marshall, S. Gais, J. Born Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep
J. Neurosci., 22 (2002), pp. 10941-10947

P. Peigneux, S. Laureys, S. Fuchs, F. Collette, F. Perrin, J. Reggers, C.Phillips, C. Degueldre, G. Del Fiore, J. Aerts, A. Luxen, P. Maquet Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron, 44 (2004), pp. 535-545

G. Pourtois, S. Schwartz, M.L. Seghier, F. Lazeyras, P. Vuilleumier View-independent coding of face identity in frontal and temporal cortices is modulated by familiarity: an event-related fMRI study Neuroimage, 24 (2005), pp. 1214-1224

B. Rasch, J. Born About sleep's role in memory Physiol. Rev., 93 (2013), pp. 681-766

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

M. Schabus, T.T. Dang-Vu, G. Albouy, E. Balteau, M. Boly, J. Carrier, A.Darsaud, C. Degueldre, M. Desseilles, S. Gais, C. Phillips, G. Rauchs, C. Schnakers, V.Sterpenich, G. Vandewalle, A. Luxen, P. Maquet Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep Proc. Natl. Acad. Sci. U. S. A., 104 (2007), pp. 13164-13169

M. Schabus, G. Gruber, S. Parapatics, C. Sauter, G. Klosch, P. Anderer, W.Klimesch, B. Saletu, J. Zeitlhofer Sleep spindles and their significance for declarative memory consolidation Sleep, 27 (2004), pp. 1479-1485

M. Schabus, K. Hodlmoser, G. Gruber, C. Sauter, P. Anderer, G. Klosch, S.Parapatics, B. Saletu, W. Klimesch, J. Zeitlhofer Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities Eur. J. Neurosci., 23 (2006), pp. 1738-1746

A. Sirota, J. Csicsvari, D. Buhl, G. Buzsaki Communication between neocortex and hippocampus during sleep in rodents Proc. Natl. Acad. Sci. U. S. A., 100 (2003), pp. 2065-2069

M. Steriade, D.A. McCormick, T.J. Sejnowski Thalamocortical oscillations in the sleeping and aroused brain Science, 262 (1993), pp. 679-685

R. Stickgold Parsing the role of sleep in memory processing Curr. Opin. Neurobiol., 23 (2013), pp. 847-853

P. Vuilleumier, J.L. Armony, J. Driver, R.J. Dolan Effects of attention and emotion on face processing in the human brain: an event-related fMRI study Neuron, 30 (2001), pp. 829-841

M. Wislowska, D.P. Heib, H. Griessenberger, K. Hoedlmoser, M.Schabus Individual baseline memory performance and its significance for sleep-dependent memory consolidation Sleep Spindles Cortical Up States, 1 (2016), pp. 2-13
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