Neural Correlates of Human Sleep and Sleep-Dependent Memory Processing

Sleep, spindles; slow waves; rapid eye movement sleep; memory consolidation; positron emission tomography; functional resonance imaging; electroencephalography; magnetoencephalography

Abstract :

[en] Wakefulness and sleep are associated with distinct patterns of neural activity and neuromodulation. In humans, functional neuroimaging was used to characterize the related changes in regional brain metabolism and hemodynamics. Recent data combining EEG and fMRI described the transient responses associated with spindles and slow waves, as well as the changes in functional integration during NREM sleep. It was also shown that regional brain activity during sleep is influenced by the experience acquired during the preceding waking period. These data are currently interpreted in the framework of two theories. First, the use-dependent increase in slow oscillation during NREM sleep is associated with local synaptic homeostasis. Second, reactivations of memory traces during NREM sleep would reorganize declarative memories in hippocampal-neocortical networks, a systems-level memory consolidation which can be hindered by sleep deprivation. Collectively, these data reveal the dynamical changes in brain activity during sleep which support normal human cognition.

Research center :

GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège

Disciplines :

Biochemistry, biophysics & molecular biology
Neurosciences & behavior

Author, co-author :

Meyer, Christelle ; Université de Liège - ULiège > Centre de recherches du cyclotron

Muto, Vincenzo ; Université de Liège - ULiège > Centre de recherches du cyclotron

Jaspar, Mathieu ; Université de Liège - ULiège > Département de Psychologie : cognition et comportement > Neuropsychologie

Kussé, Caroline ; Université de Liège - ULiège > Centre de recherches du cyclotron

Foret, Ariane

Mascetti, Laura ; Université de Liège - ULiège > Centre de recherches du cyclotron

Maquet, Pierre ; Université de Liège - ULiège > Centre de recherches du cyclotron

Language :

English

Title :

Neural Correlates of Human Sleep and Sleep-Dependent Memory Processing

Publication date :

July 2012

Main work title :

Sleep and Brain Activity

Editor :

Frank, Marcos

Publisher :

Academic Press

ISBN/EAN :

9780123849960

Pages :

165-186

Peer reviewed :

Peer reviewed

Additional URL :

http://store.elsevier.com/product.jsp?isbn=9780123849960&locale=en_EU

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
FMRE - Fondation Médicale Reine Elisabeth [BE]
Research Fund of the University of Liège and “Interuniversity Attraction Poles Programme – Belgian State – Belgian Science Policy”.
Fonds Léon Fredericq [BE]

Available on ORBi :

since 14 January 2013

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Bibliography

Anderer P., Klosch G., Gruber G., Trenker E., Pascual-Marqui R.D., Zeitlhofer J., et al. Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex. Neuroscience 2001, 103(3):581-592.
Andersson J.L., Onoe H., Hetta J., Lidstrom K., Valind S., Lilja A., et al. Brain networks affected by synchronized sleep visualized by positron emission tomography. Journal of Cerebral Blood Flow and Metabolism 1998, 18(7):701-715.
Andrade K.C., Spoormaker V.I., Dresler M., Wehrle R., Holsboer F., Samann P.G., et al. Sleep Spindles and Hippocampal Functional Connectivity in Human NREM Sleep. The Journal of Neuroscience 2011, 31(28):10331-10339.
Braun A.R., Balkin T.J., Wesensten N.J., Gwadry F., Carson R.E., Varga M., et al. Dissociated pattern of activity in visual cortices and their projections during human rapid eye movement sleep. Science 1998, 279(5347):91-95.
Braun A.R., Balkin T.J., Wesenten N.J., Carson R.E., Varga M., Baldwin P., et al. Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study. Brain 1997, 120(Pt 7):1173-1197.
Buchsbaum M.S., Gillin J.C., Wu J., Hazlett E., Sicotte N., Dupont R.M., et al. Regional cerebral glucose metabolic rate in human sleep assessed by positron emission tomography. Life Sciences 1989, 45(15):1349-1356.
Bushey D., Tononi G., Cirelli C. Sleep and synaptic homeostasis: Structural evidence in Drosophila. Science 2011, 332(6037):1576-1581.
Clemens Z., Molle M., Eross L., Barsi P., Halasz P., Born J. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 2007, 130(Pt 11):2868-2878.
Contreras D., Destexhe A., Sejnowski T.J., Steriade M. Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 1996, 274(5288):771-774.
Critchley H.D., Corfield D.R., Chandler M.P., Mathias C.J., Dolan R.J. Cerebral correlates of autonomic cardiovascular arousal: A functional neuroimaging investigation in humans. The Journal of Physiology 2000, 523(Pt 1):259-270.
Damoiseaux J.S., Rombouts S.A., Barkhof F., Scheltens P., Stam C.J., Smith S.M., et al. Consistent resting-state networks across healthy subjects. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(37):13848-13853.
Dang-Vu T.T., Desseilles M., Laureys S., Degueldre C., Perrin F., Phillips C., et al. Cerebral correlates of delta waves during non-REM sleep revisited. Neuroimage 2005, 28(1):14-21.
Dang-Vu T.T., Schabus M., Desseilles M., Albouy G., Boly M., Darsaud A., et al. Spontaneous neural activity during human slow wave sleep. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(39):15160-15165.
De Gennaro L., Ferrara M. Sleep spindles: An overview. Sleep Medicine Reviews 2003, 7(5):423-440.
Debas K., Carrier J., Orban P., Barakat M., Lungu O., Vandewalle G., et al. Brain plasticity related to the consolidation of motor sequence learning and motor adaptation. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(41):17839-17844.
Dehghani N., Cash S.S., Rossetti A.O., Chen C.C., Halgren E. Magnetoencephalography demonstrates multiple asynchronous generators during human sleep spindles. Journal of Neurophysiology 2010, 104(1):179-188.
Desseilles M., Dang Vu T., Laureys S., Peigneux P., Degueldre C., Phillips C., et al. A prominent role for amygdaloid complexes in the Variability in Heart Rate (VHR) during Rapid Eye Movement (REM) sleep relative to wakefulness. Neuroimage 2006, 32:1008-1015.
Diekelmann S., Buchel C., Born J., Rasch B. Labile or stable: Opposing consequences for memory when reactivated during waking and sleep. Nature Neuroscience 2011, 14(3):381-386.
Ellenbogen J.M., Hulbert J.C., Stickgold R., Dinges D.F., Thompson-Schill S.L. Interfering with theories of sleep and memory: Sleep, declarative memory, and associative interference. Current Biology 2006, 16(13):1290-1294.
Eschenko, O., Magri, C., Panzeri, S., & Sara, S. J. (2012). Noradrenergic neurons of the locus coeruleus are phase locked to cortical up-down states during sleep. Cereb Cortex.
Euston D.R., Tatsuno M., McNaughton B.L. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 2007, 318(5853):1147-1150.
Fernandez-Mendoza J., Lozano B., Seijo F., Santamarta-Liebana E., Ramos-Platon M.J., Vela-Bueno A., et al. Evidence of subthalamic PGO-like waves during REM sleep in humans: A deep brain polysomnographic study. Sleep 2009, 32(9):1117-1126.
Fischer S., Nitschke M.F., Melchert U.H., Erdmann C., Born J. Motor memory consolidation in sleep shapes more effective neuronal representations. The Journal of Neuroscience 2005, 25(49):11248-11255.
Fogel S.M., Smith C.T. Learning-dependent changes in sleep spindles and stage 2 sleep. Journal of Sleep Research 2006, 15(3):250-255.
Fogel S.M., Smith C.T., Cote K.A. Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behavioural Brain Research 2007, 180(1):48-61.
Friston K.J., Frith C.D., Liddle P.F., Frackowiak R.S. Functional connectivity: The principal-component analysis of large (PET) data sets. Journal of Cerebral Blood Flow and Metabolism 1993, 13(1):5-14.
Gais S., Albouy G., Boly M., Dang-Vu T.T., Darsaud A., Desseilles M., et al. Sleep transforms the cerebral trace of declarative memories. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(47):18778-18783.
Gais S., Lucas B., Born J. Sleep after learning aids memory recall. Learning & Memory 2006, 13(3):259-262.
Gais S., Plihal W., Wagner U., Born J. Early sleep triggers memory for early visual discrimination skills. Nature Neuroscience 2000, 3(12):1335-1339.
Girardeau G., Benchenane K., Wiener S.I., Buzsaki G., Zugaro M.B. Selective suppression of hippocampal ripples impairs spatial memory. Nature Neuroscience 2009, 12(10):1222-1223.
Hagmann P., Cammoun L., Gigandet X., Meuli R., Honey C.J., Wedeen V.J., et al. Mapping the structural core of human cerebral cortex. PLoS Biology 2008, 6(7):e159.
Hong C.C., Harris J.C., Pearlson G.D., Kim J.S., Calhoun V.D., Fallon J.H., et al. fMRI evidence for multisensory recruitment associated with rapid eye movements during sleep. Human Brain Mapping 2009, 30(5):1705-1722.
Horovitz S.G., Braun A.R., Carr W.S., Picchioni D., Balkin T.J., Fukunaga M., et al. Decoupling of the brain's default mode network during deep sleep. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(27):11376-11381.
Huber R., Esser S.K., Ferrarelli F., Massimini M., Peterson M.J., Tononi G. TMS-Induced cortical potentiation during wakefulness locally increases slow wave activity during sleep. PLoS ONE 2007, 2:e276.
Huber R., Ghilardi M.F., Massimini M., Ferrarelli F., Riedner B.A., Peterson M.J., et al. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nature Neuroscience 2006, 9(9):1169-1176.
Huber R., Ghilardi M.F., Massimini M., Tononi G. Local sleep and learning. Nature 2004, 430(6995):78-81.
Huber R., Maatta S., Esser S.K., Sarasso S., Ferrarelli F., Watson A., et al. Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep. The Journal of Neuroscience 2008, 28(31):7911-7918.
Huber R., Tononi G., Cirelli C. Exploratory behavior, cortical BDNF expression, and sleep homeostasis. Sleep 2007, 30(2):129-139.
Inoué S., Saha U.K., Musha T. Spatio-temporal distribution of neuronal activities and REM sleep. Rapid eye movement sleep 1999, 214-220. Narosa Publishing, New Dehli. B.N. Mallick, S. Inoue (Eds.).
Ioannides A.A., Corsi-Cabrera M., Fenwick P.B., del Rio Portilla Y., Laskaris N.A., Khurshudyan A., et al. MEG tomography of human cortex and brainstem activity in waking and REM sleep saccades. Cerebral Cortex 2004, 14(1):56-72.
Isomura Y., Sirota A., Ozen S., Montgomery S., Mizuseki K., Henze D.A., et al. Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 2006, 52(5):871-882.
Ji D., Wilson M.A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nature Neuroscience 2007, 10(1):100-107.
Kajimura N., Uchiyama M., Takayama Y., Uchida S., Uema T., Kato M., et al. Activity of midbrain reticular formation and neocortex during the progression of human non-rapid eye movement sleep. The Journal of Neuroscience 1999, 19(22):10065-10073.
Kattler H., Dijk D.J., Borbely A.A. Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans. Journal of Sleep Research 1994, 3(3):159-164.
Kennedy C., Gillin J.C., Mendelson W., Suda S., Miyaoka M., Ito M., et al. Local cerebral glucose utilization in non-rapid eye movement sleep. Nature 1982, 297(5864):325-327.
Korman M., Doyon J., Doljansky J., Carrier J., Dagan Y., Karni A. Daytime sleep condenses the time course of motor memory consolidation. Nature Neuroscience 2007, 10(9):1206-1213.
Kudrimoti H.S., Barnes C.A., McNaughton B.L. Reactivation of hippocampal cell assemblies: Effects of behavioral state, experience, and EEG dynamics. The Journal of Neuroscience 1999, 19(10):4090-4101.
Kuriyama K., Stickgold R., Walker M.P. Sleep-dependent learning and motor-skill complexity. Learning & Memory 2004, 11(6):705-713.
Larson-Prior L.J., Zempel J.M., Nolan T.S., Prior F.W., Snyder A.Z., Raichle M.E. Cortical network functional connectivity in the descent to sleep. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(11):4489-4494.
Laureys S., Peigneux P., Phillips C., Fuchs S., Degueldre C., Aerts J., et al. Experience-dependent changes in cerebral functional connectivity during human rapid eye movement sleep. Neuroscience 2001, 105(3):521-525.
Le Van Quyen M., Staba R., Bragin A., Dickson C., Valderrama M., Fried I., et al. Large-scale microelectrode recordings of high-frequency gamma oscillations in human cortex during sleep. The Journal of Neuroscience 2010, 30(23):7770-7782.
Lim A.S., Lozano A.M., Moro E., Hamani C., Hutchison W.D., Dostrovsky J.O., et al. Characterization of REM-sleep associated ponto-geniculo-occipital waves in the human pons. Sleep 2007, 30(7):823-827.
Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysio-logical investigation of the basis of the fMRI signal. Nature 2001, 412(6843):150-157.
Louie K., Wilson M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 2001, 29(1):145-156.
Lu J., Sherman D., Devor M., Saper C.B. A putative flip-flop switch for control of REM sleep. Nature 2006, 441(7093):589-594.
Lydic R., Baghdoyan H.A., Hibbard L., Bonyak E.V., DeJoseph M.R., Hawkins R.A. Regional brain glucose metabolism is altered during rapid eye movement sleep in the cat: A preliminary study. The Journal of Comparative Neurology 1991, 304(4):517-529.
Madsen P.L., Schmidt J.F., Holm S., Vorstrup S., Lassen N.A., Wildschiodtz G. Cerebral oxygen metabolism and cerebral blood flow in man during light sleep (stage 2). Brain Research 1991, 557(1-2):217-220.
Madsen P.L., Schmidt J.F., Wildschiodtz G., Friberg L., Holm S., Vorstrup S., et al. Cerebral O2 metabolism and cerebral blood flow in humans during deep and rapid-eye-movement sleep. Journal of Applied Physiology 1991, 70(6):2597-2601.
Madsen P.L., Vorstrup S. Cerebral blood flow and metabolism during sleep. Cerebrovascular and Brain Metabolism Reviews 1991, 3(4):281-296.
Maquet P. Functional neuroimaging of normal human sleep by positron emission tomography. Journal of Sleep Research 2000, 9(3):207-231.
Maquet P., Degueldre C., Delfiore G., Aerts J., Peters J.M., Luxen A., et al. Functional neuroanatomy of human slow wave sleep. The Journal of Neuroscience 1997, 17(8):2807-2812.
Maquet P., Dive D., Salmon E., Sadzot B., Franco G., Poirrier R., et al. Cerebral glucose utilization during stage 2 sleep in man. Brain Research 1992, 571(1):149-153.
Maquet P., Dive D., Salmon E., Sadzot B., Franco G., Poirrier R., et al. Cerebral glucose utilization during sleep-wake cycle in man determined by positron emission tomography and [18F]2-fluoro-2-deoxy-D-glucose method. Brain Research 1990, 513(1):136-143.
Maquet P., Laureys S., Peigneux P., Fuchs S., Petiau C., Phillips C., et al. Experience-dependent changes in cerebral activation during human REM sleep. Nature Neuroscience 2000, 3(8):831-836.
Maquet P., Peters J., Aerts J., Delfiore G., Degueldre C., Luxen A., et al. Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature 1996, 383(6596):163-166.
Maquet P., Phillips C. Functional brain imaging of human sleep. Journal of Sleep Research 1998, 7(Suppl. 1):42-47.
Maquet P., Ruby P., Maudoux A., Albouy G., Sterpenich V., Dang-Vu T., et al. Human cognition during REM sleep and the activity profile within the frontal and parietal cortices: A reappraisal of functional neuroimaging data. Progress in brain research 2005, Vol. 150:219-227. Amsterdam: Elsevier.
Marr D. A theory for cerebral neocortex. Proceedings of the Royal Society London B: Biological Sciences 1970, 176(43):161-234.
Marr D. Simple memory: A theory for archicortex. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 1971, 262(841):23-81.
Massimini M., Huber R., Ferrarelli F., Hill S., Tononi G. The sleep slow oscillation as a traveling wave. The Journal of Neuroscience 2004, 24(31):6862-6870.
McCarley R.W., Winkelman J.W., Duffy F.H. Human cerebral potentials associated with REM sleep rapid eye movements: Links to PGO waves and waking potentials. Brain Research 1983, 274(2):359-364.
McClelland J.L., McNaughton B.L., O'Reilly R.C. Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychological Review 1995, 102(3):419-457.
Mena-Segovia J., Sims H.M., Magill P.J., Bolam J.P. Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. The Journal of Physiology 2008, 586(Pt 12):2947-2960.
Miyauchi S., Misaki M., Kan S., Fukunaga T., Koike T. Human brain activity time-locked to rapid eye movements during REM sleep. Experimental Brain Research 2009, 192(4):657-667.
Molle M., Born J. Hippocampus whispering in deep sleep to prefrontal cortex-for good memories?. Neuron 2009, 61(4):496-498.
Molle M., Marshall L., Gais S., Born J. Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. The Journal of Neuroscience 2002, 22(24):10941-10947.
Molle M., Yeshenko O., Marshall L., Sara S.J., Born J. Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. Journal of Neurophysiology 2006, 96(1):62-70.
Morin A., Doyon J., Dostie V., Barakat M., Hadj Tahar A., Korman M., et al. Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. Sleep 2008, 31(8):1149-1156.
Murphy M., Riedner B.A., Huber R., Massimini M., Ferrarelli F., Tononi G. Source modeling sleep slow waves. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(5):1608-1613.
Nadasdy Z., Hirase H., Czurko A., Csicsvari J., Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus. The Journal of Neuroscience 1999, 19(21):9497-9507.
Nir Y., Staba R.J., Andrillon T., Vyazovskiy V.V., Cirelli C., Fried I., et al. Regional slow waves and spindles in human sleep. Neuron 2011, 70(1):153-169.
Nofzinger E.A., Mintun M.A., Wiseman M., Kupfer D.J., Moore R.Y. Forebrain activation in REM sleep: An FDG PET study. Brain Research 1997, 770(1-2):192-201.
Peigneux P., Laureys S., Fuchs S., Collette F., Perrin F., Reggers J., et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep?. Neuron 2004, 44(3):535-545.
Peigneux P., Laureys S., Fuchs S., Delbeuck X., Degueldre C., Aerts J., et al. Generation of rapid eye movements during paradoxical sleep in humans. Neuroimage 2001, 14(3):701-708.
Peigneux P., Laureys S., Fuchs S., Destrebecqz A., Collette F., Delbeuck X., et al. Learned material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep. Neuroimage 2003, 20(1):125-134.
Pennartz C.M., Lee E., Verheul J., Lipa P., Barnes C.A., McNaughton B.L. The ventral striatum in off-line processing: Ensemble reactivation during sleep and modulation by hippocampal ripples. The Journal of Neuroscience 2004, 24(29):6446-6456.
Peyrache A., Khamassi M., Benchenane K., Wiener S.I., Battaglia F.P. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nature Neuroscience 2009, 12(7):919-926.
Phelps M.E., Mazziotta J.C. Positron emission tomography: Human brain function and biochemistry. Science 1985, 228(4701):799-809.
Picchioni D., Horovitz S.G., Fukunaga M., Carr W.S., Meltzer J.A., Balkin T.J., et al. Infraslow EEG oscillations organize large-scale cortical-subcortical interactions during sleep: A combined EEG/fMRI study. Brain Research 2011, 1374:63-72.
Plihal W., Born J. Effects of early and late nocturnal sleep on declarative and procedural memory. Journal of Cognitive Neuroscience 1997, 9:534-547.
Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(2):676-682.
Ramm P., Frost B.J. Regional metabolic activity in the rat brain during sleep-wake activity. Sleep 1983, 6(3):196-216.
Ramm P., Frost B.J. Cerebral and local cerebral metabolism in the cat during slow wave and REM sleep. Brain Research 1986, 365(1):112-124.
Rasch B., Buchel C., Gais S., Born J. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 2007, 315(5817):1426-1429.
Rauchs G., Feyers D., Landeau B., Bastin C., Luxen A., Maquet P., et al. Sleep contributes to the strengthening of some memories over others, depending on hippocampal activity at learning. The Journal of Neuroscience 2011, 31(7):2563-2568.
Ribeiro S., Gervasoni D., Soares E.S., Zhou Y., Lin S.C., Pantoja J., et al. Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biology 2004, 2(1):E24.
Robertson E.M., Pascual-Leone A., Press D.Z. Awareness modifies the skill-learning benefits of sleep. Current Biology 2004, 14(3):208-212.
Salzarulo P., Lairy G.C., Bancaud J., Munari C. Direct depth recording of the striate cortex during REM sleep in man: Are there PGO potentials?. EEG Clinical Neurophysiology 1975, 38:199-202.
Schabus M., Dang-Vu T.T., Albouy G., Balteau E., Boly M., Carrier J., et al. Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(32):13164-13169.
Sokoloff L. Localization of functional activity in the central nervous system by measurement of glucose utilization with radioactive deoxyglucose. Journal of Cerebral Blood Flow and Metabolism 1981, 1(1):7-36.
Spoormaker V.I., Schroter M.S., Gleiser P.M., Andrade K.C., Dresler M., Wehrle R., et al. Development of a large-scale functional brain network during human non-rapid eye movement sleep. The Journal of Neuroscience 2010, 30(34):11379-11387.
Steriade M., Amzica F., Nunez A. Cholinergic and noradrenergic modulation of the slow (approximately 0.3Hz) oscillation in neocortical cells. Journal of Neurophysiology 1993, 70(4):1385-1400.
Steriade M., McCarley R.W. Brain control of wakefulness and sleep 2005, Kluwer Academic, New York.
Steriade M., Nunez A., Amzica F. Intracellular analysis of relations between the slow (<1Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. The Journal of Neuroscience 1993, 13(8):3266-3283.
Steriade M., Nunez A., Amzica F. A novel slow (<1Hz) oscillation of neocortical neurons in vivo: Depolarizing and hyperpolarizing components. The Journal of Neuroscience 1993, 13(8):3252-3265.
Sterpenich V., Albouy G., Boly M., Vandewalle G., Darsaud A., Balteau E., et al. Sleep-related hippocampo-cortical interplay during emotional memory recollection. PLoS Biology 2007, 5(11):e282.
Sterpenich V., Albouy G., Darsaud A., Schmidt C., Vandewalle G., Dang Vu T.T., et al. Sleep promotes the neural reorganization of remote emotional memory. The Journal of Neuroscience 2009, 29(16):5143-5152.
Stickgold R., James L., Hobson J.A. Visual discrimination learning requires sleep after training. Nature Neuroscience 2000, 3(12):1237-1238.
Takahashi K. [Regional cerebral blood flow and oxygen consumption during normal human sleep]. No To Shinkei 1989, 41(9):919-925.
Takashima A., Petersson K.M., Rutters F., Tendolkar I., Jensen O., Zwarts M.J., et al. From the Cover: Declarative memory consolidation in humans: A prospective functional magnetic resonance imaging study. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(3):756-761.
Tononi G., Cirelli C. Sleep and synaptic homeostasis: A hypothesis. Brain Research Bulletin 2003, 62(2):143-150.
Tononi G., Cirelli C. Sleep function and synaptic homeostasis. Sleep Medicine Reviews 2006, 10(1):49-62.
Tononi G., Massimini M., Riedner B.A. Sleepy dialogues between cortex and hippocampus: Who talks to whom?. Neuron 2006, 52(5):748-749.
Vyazovskiy V.V., Cirelli C., Pfister-Genskow M., Faraguna U., Tononi G. Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nature Neuroscience 2008, 11(2):200-208.
Vyazovskiy V.V., Olcese U., Lazimy Y.M., Faraguna U., Esser S.K., Williams J.C., et al. Cortical firing and sleep homeostasis. Neuron 2009, 63(6):865-878.
Walker M.P., Brakefield T., Morgan A., Hobson J.A., Stickgold R. Practice with sleep makes perfect: Sleep-dependent motor skill learning. Neuron 2002, 35(1):205-211.
Walker M.P., Stickgold R., Alsop D., Gaab N., Schlaug G. Sleep-dependent motor memory plasticity in the human brain. Neuroscience 2005, 133(4):911-917.
Wehrle R., Czisch M., Kaufmann C., Wetter T.C., Holsboer F., Auer D.P., et al. Rapid eye movement-related brain activation in human sleep: A functional magnetic resonance imaging study. Neuroreport 2005, 16(8):853-857.
Wierzynski C.M., Lubenov E.V., Gu M., Siapas A.G. State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 2009, 61(4):587-596.