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Sleep Homeostasis and Cortical Synchronization: III. A High-Density EEG Study of Sleep Slow Waves in Humans
Open accessAbstract
STUDY OBJECTIVES: The mechanisms responsible for the homeostatic decrease of slow-wave activity (SWA, defined in this study as electroencephalogram [EEG] power between 0.5 and 4.0 Hz) during sleep are unknown. In agreement with a recent hypothesis, in the first of 3 companion papers, large-scale computer simulations of the sleeping thalamocortical system showed that a decrease in cortical synaptic strength is sufficient to account for the decline in SWA. In the model, the reduction in SWA was accompanied by decreased incidence of high-amplitude slow waves, decreased wave slopes, and increased number of waves with multiple peaks. In a second companion paper in the rat, local field potential recordings during early and late sleep confirmed the predictions of the model. Here, we investigated the model's predictions in humans by using all-night high-density (hd)-EEG recordings to explore slow-wave parameters over the entire cortical mantle. DESIGN: 256-channel EEG recordings in humans over the course of an entire night's sleep. SETTING: Sound-attenuated sleep research room PATIENTS OR PARTICIPANTS: Seven healthy male subjects INTERVENTIONS: N/A. MEASUREMENTS AND RESULTS: During late sleep (non-rapid eye movement [NREM] episodes 3 and 4, toward morning), when compared with early sleep (NREM sleep episodes 1 and 2, at the beginning of the night), the analysis revealed (1) reduced SWA, (2) fewer large-amplitude slow waves, (3) decreased wave slopes, (4) more frequent multipeak waves. The decrease in slope between early and late sleep was present even when waves were directly matched by wave amplitude and slow-wave power in the background EEG. Finally, hd-EEG showed that multipeak waves have multiple cortical origins. CONCLUSIONS: In the human EEG, the decline of SWA during sleep is accompanied by changes in slow-wave parameters that were predicted by a computer model simulating a homeostatic reduction of cortical synaptic strength.
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“Independent of the decrease in amplitude, the slope of the slow waves also decreases from early to late sleep”
From About Sleep's Role in Memory (2013) · cites this paper as [994]
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“Traditionally, SWA is regarded as a marker of the homeostatically regulated sleep pressure, which increases after prolonged sleep deprivation and decreases from early to late sleep (111, 113, 994, 1269).”
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“possibly reflecting a decrease in the synchrony and speed of recruitment of neurons at the down-to-up state transition (87,360,994,1267).”
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“Specifically, the model predicted a decrease in the incidence of high-amplitude slow waves, a decrease in slope, as well as an increase in the number of multipeak waves from early to late sleep, which was con-firmed in related animal and human studies (994, 1269).”
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Sleep spindle and slow wave frequency reflect motor skill performance in primary school-age children
Astill, R. G., Piantoni, G., Raymann, R., Vis, J. C., Coppens, J. E., Walker, M. P., Stickgold, R., van der Werf, Y. D., & Someren, E. J. W. V. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00910 · Cited by 64
“Automated slow wave detection was performed using an algo-rithm based on previously published methods (Massimini et al., 2004; Riedner et al., 2007) implemented in Matlab (The Math-Works Inc, Natick, USA).”
MethodThe Impact of Visual Perceptual Learning on Sleep and Local Slow-Wave Initiation
Mascetti, L., Muto, V., Matarazzo, L., Foret, A., Ziegler, E., Albouy, G., Virginie Sterpenich, A., Schmidt, C., Degueldre, C., Leclercq, Y., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0763-12.2013 · Cited by 66
“They increase with the duration of the preceding wake and decrease during NREM sleep (Riedner et al., 2007; Vyazovskiy et al., 2009).”
BackgroundFocal lesions induce large-scale percolation of sleep-like intracerebral activity in awake humans
Russo, S., Pigorini, A., Mikulan, E., Sarasso, S., Rubino, A., Zauli, F. M., Parmigiani, S., d’Orio, P., Cattani, A., Francione, S., et al. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.117964 · Cited by 64
“Next, we applied a standard slow-wave detection algorithm based on zero-crossings and period criteria (Riedner et al. 2007a) on the same contacts.”
Self-citationD’Agostino, A., Castelnovo, A., Cavallotti, S., Casetta, C., Marcatili, M., Gambini, O., Canevini, M., Tononi, G., Riedner, B. A., Ferrarelli, F., et al. (2018) · Schizophrenia · doi:10.1038/s41537-018-0045-9 · Cited by 67
Self-citationOptimizing detection and analysis of slow waves in sleep EEG
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Self-citationBölsterli, B. K., Gardella, E., Pavlidis, E., Wehrle, F. M., Tassinari, C. A., Huber, R., & Rubboli, G. (2017) · Epilepsia · doi:10.1111/epi.13910 · Cited by 64
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Lustenberger, C., & Huber, R. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00077 · Cited by 66
“Several parameters of sleep slow waves, e.g., their slopes, seem to be sensitive markers for changes in synaptic strength (Riedner et al., 2007).”
BackgroundSelf-citationBölsterli, B. K., Fattinger, S., Kurth, S., LeBourgeois, M. K., Ringli, M., Bast, T., Critelli, H., Schmitt, B., & Huber, R. (2014) · Epilepsia · doi:10.1111/epi.12576 · Cited by 68
Self-citationSleep and olfactory cortical plasticity
Barnes, D. C., & Wilson, D. A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00134 · Cited by 68
“…periods of wakefulness, sleep pressure is greatest as evidenced by a shorter latency to enter SWS following sleep onset and an increased power of slow wave activity (SWA), which gradually decreases from early to late sleep (Borbély, 1982; Borbély and Achermann, 1999; Riedner et al., 2007).”
BackgroundLocal Use-Dependent Sleep in Wakefulness Links Performance Errors to Learning
Quercia, A., Zappasodi, F., Committeri, G., & Ferrara, M. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00122 · Cited by 70
“To investigate the possibility that task-related errors are the result of periods of neuronal silence, reflected in individual delta waves (Riedner et al., 2007; Nir et al., 2011, 2017; Vyazovskiy et al., 2011; Hung et al., 2013; Bernardi et al., 2015), we compared the number and the amplitude…”
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“It’s consistent to the experimental result that the thalamocortical neurons with high-synaptic-strength exhibited well-synchronized activities during early sleep but exhibited a weak synchronization during late sleep due to the decreasing synaptic strength (Esser et al., 2007; Riedner et al., 2007).”
ResultCharacterization of Topographically Specific Sleep Spindles in Mice
Kim, D., Hwang, E., Lee, M., Sung, H., & Choi, J. H. (2014) · SLEEP · doi:10.5665/sleep.4330 · Cited by 61
GABAB receptors: modulation of thalamocortical dynamics and synaptic plasticity
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“The cortex defaults to slow-wave activity due to changes in neuromodulation, as in sleep (Steriade et al., 2001; Riedner et al., 2007) or due to changes in the excitatory/inhibitory balance as in deep anesthesia (Steriade, Conteras et al.”
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BackgroundFunctional Structure of Spontaneous Sleep Slow Oscillation Activity in Humans
Menicucci, D., Piarulli, A., Debarnot, U., D’Ascanio, P., Landi, A., & Gemignani, A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007601 · Cited by 63
“[21], we still detected only full-fledged SSO events.”
BackgroundMethodInfluentialWakefulness delta waves increase after cortical plasticity induction
Assenza, G., Pellegrino, G., Tombini, M., Di Pino, G., & Di Lazzaro, V. (2015) · Clinical Neurophysiology · doi:10.1016/j.clinph.2014.09.029 · Cited by 59
“, 2007) and human studies (Riedner et al., 2007; Vyazovskiy et al., 2009) show that the amplitude and slope of DW are proportional to the number of cortical neurons entering such up/down states near-synchronously.”
BackgroundNight and day variations of sleep in patients with disorders of consciousness
Wisłowska, M., del Giudice, R., Lechinger, J., Wielek, T., Heib, D. P. J., Pitiot, A., Pichler, G., Michitsch, G., Donis, J. A., & Schabus, M. (2017) · Scientific Reports · doi:10.1038/s41598-017-00323-4 · Cited by 58
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Self-citationSleep in humans stabilizes pattern separation performance
Hanert, A., Weber, F. D., Pedersen, A., Born, J., & Bartsch, T. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.1189-17.2017 · Cited by 52
“For each individual and channel, the number of slow oscillations, their density (per minutes of non-REM sleep), mean amplitude, and slope (ratio between negative half-wave peak amplitude and the time between the negative peak to the next zero crossing; Riedner et al., 2007) were calculated.”
MethodMander, B. A., Dave, A., Lui, K. K., Sprecher, K. E., Berisha, D. E., Chappel-Farley, M. G., Chen, I. Y., Riedner, B. A., Heston, M. B., Suridjan, I., et al. (2022) · SLEEP · doi:10.1093/sleep/zsac135 · Cited by 62
Self-citationThe Cortical Topography of Local Sleep
Murphy, M., Huber, R., Esser, S. K., Riedner, B. A., Massimini, M., Ferrarelli, F., Ghilardi, M. F., & Tononi, G. (2011) · Current Topics in Medicinal Chemistry · doi:10.2174/156802611797470303 · Cited by 57
“These waves are more complicated to characterize in terms of their cortical origins and propagation [14].”
BackgroundMethodInfluentialSelf-citationSprecher, K. E., Riedner, B. A., Smith, R., Tononi, G., Davidson, R. J., & Benca, R. M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149770 · Cited by 60
Self-citationSleepers track informative speech in a multitalker environment
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Synaptic Potentiation and Sleep Need: Clues from Molecular and Electrophysiological Studies
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“Both theoretical considerations [13], large-scale simulations [14], and empirical studies [15-17] indicate that the amplitude and slope of EEG slow waves is related to the number of neurons that enter an up state or a down state near-synchronously, and that synchrony is directly related to the number, strength, and ef…”
BackgroundSelf-citationVyazovskiy, V. V., Olcese, U., Cirelli, C., & Tononi, G. (2012) · Journal of Sleep Research · doi:10.1111/jsr.12009 · Cited by 57
Self-citationThe effects of morning training on night sleep: A behavioral and EEG study
Määttä, S., Landsness, E., Sarasso, S., Ferrarelli, F., Ferreri, F., Ghilardi, M. F., & Tononi, G. (2010) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2010.01.006 · Cited by 55
Self-citationThe Impact of EEG/MEG Signal Processing and Modeling in the Diagnostic and Management of Epilepsy
Lopes, F. H. D. S. (2008) · IEEE Reviews in Biomedical Engineering · doi:10.1109/rbme.2008.2008246 · Cited by 53
Mapping Slow Waves by EEG Topography and Source Localization: Effects of Sleep Deprivation
Bersagliere, A., Pascual-Marqui, R. D., Tarokh, L., & Achermann, P. (2017) · Brain Topography · doi:10.1007/s10548-017-0595-6 · Cited by 54
Barbero‐Castillo, A., Mateos‐Aparicio, P., Porta, L. D., Camassa, A., Perez-Mendez, L., & Sanchez-Vives, M. V. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1837-20.2021 · Cited by 53
“…(Casali et al., 2013; Comolatti et al., 2019) is a measure of cortical complexity that has been used to quantify consciousness levels, in awake/sleep, in anesthesia (Hudetz, 2012; Sarasso et al., 2015) and in patients with disorders of consciousness (Rosanova et al., 2012; Casarotto et al., 2016).”
BackgroundAn increase in sleep slow waves predicts better working memory performance in healthy individuals
Ferrarelli, F., Kaskie, R. E., Laxminarayan, S., Ramakrishnan, S., Jaques Reifman, A., & Germain, A. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.02.020 · Cited by 59
“There is also evidence that some of these slow waves enhancing interventions benefit cognitive functioning (Marshall et al., 2004; Rihm et al., 2014).”
Local targeted memory reactivation in human sleep
Bar, E., Marmelshtein, A., Arzi, A., Perl, O., Livne, E., Hizmi, E., Paz, R., Sobel, N., Dudai, Y., & Nir, Y. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.091 · Cited by 50
Overnight Changes in the Slope of Sleep Slow Waves during Infancy
Fattinger, S., Jenni, O. G., Schmitt, B., Achermann, P., & Huber, R. (2014) · SLEEP · doi:10.5665/sleep.3390 · Cited by 53
Self-citationWake slow waves in focal human epilepsy impact network activity and cognition
Sheybani, L., Vivekananda, U., Rodionov, R., Diehl, B., Chowdhury, F. A., McEvoy, A. W., Miserocchi, A., Bisby, J. A., Bush, D., Burgess, N., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42971-3 · Cited by 51
Zhang, Y., Quiñones, G. M., & Ferrarelli, F. (2019) · Schizophrenia Research · doi:10.1016/j.schres.2019.11.002 · Cited by 48
“In contrast, over the past several years the development of spindle and slow wave detection algorithms (Mensen et al., 2016; Riedner et al., 2007; Warby et al., 2014) has provided several advantages.”
BackgroundDiazepam effects on local cortical neural activity during sleep in mice
McKillop, L. E., Fisher, S. P., Milinski, L., Krone, L. B., & Vyazovskiy, V. V. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114515 · Cited by 49
“…between slow waves and their neuronal counterparts, where lower SWA spectral power is a result of reduced occurrence of slow waves and population OFF periods (Esser et al., 2007; Panagiotou et al., 2017; Riedner et al., 2007; Steriade, 2006; Steriade et al., 1993; Vyazovskiy et al., 2009, 2007).”
BackgroundResultSelf-citationBaird, B., Castelnovo, A., Riedner, B. A., Lutz, A., Ferrarelli, F., Boly, M., Davidson, R. J., & Tononi, G. (2018) · eneuro · doi:10.1523/eneuro.0293-18.2018 · Cited by 45
Self-citationKohtala, S., Alitalo, O., Rosenholm, M., Rozov, S. V., & Rantamäki, T. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107741 · Cited by 47
Attenuated Fast Steady-State Visual Evoked Potentials During Human Sleep
Sharon, O., & Nir, Y. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx043 · Cited by 47
“To this end, we detected K-complexes as in previous studies (Riedner et al. 2007; Nir et al. 2011).”
Fluid boundaries between wake and sleep. experimental evidence from Stereo-EEF recordings
Sarasso, S. (2015) · ARCHIVES ITALIENNES DE BIOLOGIE · doi:10.12871/0002982920142311 · Cited by 55
Developmental Patterns of Sleep Slow Wave Activity and Synaptic Density in Adolescent Mice
de Vivo, L., Faraguna, U., Nelson, A. B., Pfister‐Genskow, M., Klapperich, M. E., Tononi, G., & Cirelli, C. (2014) · SLEEP · doi:10.5665/sleep.3570 · Cited by 45
Self-citationReduced frontal slow wave density during sleep in first-episode psychosis
Kaskie, R. E., Gill, K. M., & Ferrarelli, F. (2018) · Schizophrenia Research · doi:10.1016/j.schres.2018.10.024 · Cited by 41
Reduced sleep pressure in young children with autism
Arazi, A., Meiri, G., Danan, D., Michaelovski, A., Flusser, H., Menashe, I., Tarasiuk, A., & Dinstein, I. (2019) · SLEEP · doi:10.1093/sleep/zsz309 · Cited by 42
Large-Scale Cortical Dynamics of Sleep Slow Waves
Botella‐Soler, V., Valderrama, M., Crépon, B., Navarro, V., & Quyen, M. L. V. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030757 · Cited by 42
“K-complexes of stage 2 and delta oscillations of stages 3–4) or the effect of the sleep pressure at the beginning of sleep [21].”
BackgroundMethodBrain Plasticity, Sleep and Aging
Cirelli, C. (2012) · Gerontology · doi:10.1159/000336149 · Cited by 43
Rattenborg, N. C., Lima, S. L., & Lesku, J. A. (2012) · The Neuroscientist · doi:10.1177/1073858412441086 · Cited by 41
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Self-citationChanges in sleep EEG with aging in humans and rodents
Campos-Beltrán, D., & Marshall, L. (2021) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-021-02545-y · Cited by 38
Lechat, B., Hansen, K. L., Melaku, Y. A., Vakulin, A., Micic, G., Adams, R. J., Appleton, S., Eckert, D. J., CATCHESIDE, P. G., & Zajamšek, B. (2021) · Annals of the American Thoracic Society · doi:10.1513/annalsats.202103-315oc · Cited by 42
Individual slow-wave morphology is a marker of aging
Ujma, P. P., Simor, P., Steiger, A., Dresler, M., & Bódizs, R. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.04.002 · Cited by 36
Electroencephalographic correlates of Chronic Fatigue Syndrome
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Cortical and subcortical hemodynamic changes during sleep slow waves in human light sleep
Betta, M., Handjaras, G., Leo, A., Federici, A., Farinelli, V., Ricciardi, E., Siclari, F., Meletti, S., Ballotta, D., Benuzzi, F., et al. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118117 · Cited by 35
Topographical aspects in the dynamics of sleep homeostasis in young men: individual patterns
Rusterholz, T., & Achermann, P. (2011) · BMC Neuroscience · doi:10.1186/1471-2202-12-84 · Cited by 39
Brain white matter damage and its association with neuronal synchrony during sleep
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Spiess, M., Bernardi, G., Kurth, S., Ringli, M., Wehrle, F. M., Jenni, O. G., Huber, R., & Siclari, F. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.05.024 · Cited by 37
“The detection of individual slow waves was performed as previously described (Siclari et al., 2014; Riedner et al., 2007).”
Self-citationPiantoni, G., Cheung, B. L. P., Veen, B. D. V., Romeijn, N., Riedner, B. A., Tononi, G., van der Werf, Y. D., & Someren, E. J. W. V. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.04.103 · Cited by 35
Self-citationMechanistic insights into the interaction between epilepsy and sleep
Sheybani, L., Frauscher, B., Bernard, C., & Walker, M. C. (2025) · Nature Reviews Neurology · doi:10.1038/s41582-025-01064-z · Cited by 43
“3) and progressively increase during wakefulness 93,94 .”
Pathophysiology of sleep-dependent memory consolidation processes in children
Urbain, C. M., Galer, S., Bogaert, P. V., & Peigneux, P. (2013) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2013.06.022 · Cited by 35
“In line with previous studies (Kurth et al., 2010a; Riedner et al., 2007), healthy controls exhibited an overnight decrease in the slope of slow waves.”
ResultKang, X., Boly, M., Findlay, G., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-58612-4 · Cited by 35
Reduced Slow-Wave Rebound during Daytime Recovery Sleep in Middle-Aged Subjects
Lafortune, M., Gagnon, J., Latreille, V., Vandewalle, G., Martin, N. G., Filipini, D., Doyon, J., & Carrier, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043224 · Cited by 34
“As reported in previous studies in young subjects [9,10,34], compared to baseline sleep, SW slope was steeper, SW amplitude and density were higher and SW durations of positive and negative phases were shorter after sleep deprivation during recovery sleep in both age groups.”
ResultAdenotonsillectomy improves slow-wave activity in children with obstructive sleep apnoea
Ben-Israel, N. I., Zigel, Y., Tal, A., Segev, Y., & Tarasiuk, A. (2010) · European Respiratory Journal · doi:10.1183/09031936.00106710 · Cited by 34
Kim, B., Hwang, E., Strecker, R. E., Choi, J. H., & Kim, Y. (2020) · Scientific Reports · doi:10.1038/s41598-019-54790-y · Cited by 36
Closed-loop modulation of local slow oscillations in human NREM sleep
Ruch, S., Schmidig, F. J., Knüsel, L., & Henke, K. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119682 · Cited by 30
Abnormal timing of slow wave synchronization processes in non-rapid eye movement sleep parasomnias
Cataldi, J., Stephan, A. M., Marchi, N. A., Haba-Rubio, J., & Siclari, F. (2022) · Sleep · doi:10.1093/sleep/zsac111 · Cited by 33
Are age and sex effects on sleep slow waves only a matter of electroencephalogram amplitude?
Rosinvil, T., Bouvier, J., Dubé, J., Lafrenière, A., Bouchard, M., Cyr-Cronier, J., Gosselin, N., Carrier, J., & Lina, J. (2020) · SLEEP · doi:10.1093/sleep/zsaa186 · Cited by 34
Plante, D. T., Goldstein, M. R., Cook, J. D., Smith, R., Riedner, B. A., Rumble, M. E., Jelenchick, L. A., Roth, A., Tononi, G., Benca, R. M., et al. (2015) · Clinical Neurophysiology · doi:10.1016/j.clinph.2015.10.040 · Cited by 40
“Notably, changes in the amplitude and slope of low amplitude slow waves were observed in SR2 and SR4, regardless of the quantity of NREM sleep analyzed, suggesting these measures may be particularly sensitive to homeostatic changes that are occurring during partial sleep deprivation (Riedner et al., 2007; Vyazovskiy e…”
BackgroundMethodSelf-citationJaramillo, V., Schoch, S. F., Markovic, A., Kohler, M., Huber, R., Lustenberger, C., & Kurth, S. (2023) · NeuroImage · doi:10.1016/j.neuroimage.2023.119924 · Cited by 34
Self-citationRapid antidepressant effects: moving right along
Martinowich, K., Jimenez, D. V., Zarate, C. A., & Manji, H. K. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.55 · Cited by 34
In vitro Cortical Network Firing is Homeostatically Regulated: A Model for Sleep Regulation
Saberi-Moghadam, S., Simi, A., Setareh, H., Mikhail, C., & Tafti, M. (2018) · Scientific Reports · doi:10.1038/s41598-018-24339-6 · Cited by 30
Boosting Recovery During Sleep by Means of Auditory Stimulation
Krugliakova, E., Skoručak, J., Sousouri, G., Leach, S., Snipes, S., Ferster, M. L., Poian, G. D., Karlen, W., & Huber, R. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.755958 · Cited by 32
“Interestingly, the two types of waves seem to be unequally reflecting recovery during sleep: no homeostatic change across the night in slow waves of largest amplitudes was found (Riedner et al., 2007).”
BackgroundResultSelf-citationMethods in Pediatric Sleep Research and Sleep Medicine
Mouthon, A., & Huber, R. (2015) · Neuropediatrics · doi:10.1055/s-0035-1550232 · Cited by 32
Self-citationLevodopa‐induced dyskinesia in Parkinson disease: Sleep matters
Amato, N., Manconi, M., Möller, J. C., Sarasso, S., Stanzione, P., Staedler, C., Kaelin‐Lang, A., & Galati, S. (2018) · Annals of Neurology · doi:10.1002/ana.25360 · Cited by 38
A Protocol for Comparing Dry and Wet EEG Electrodes During Sleep
Leach, S., Chung, K.-Y., Tüshaus, L., Huber, R., & Karlen, W. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00586 · Cited by 34
Self-citationSolano, A., Riquelme, L. A., Pérez-Chada, D., & Della‐Maggiore, V. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab360 · Cited by 33
Synaptic refinement during development and its effect on slow-wave activity: a computational study
Hoel, E. P., Albantakis, L., Cirelli, C., & Tononi, G. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00812.2015 · Cited by 30
Self-citationBódizs, R., Schneider, B., Ujma, P. P., Horváth, C. G., Dresler, M., & Rosenblum, Y. (2024) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2024.102589 · Cited by 39
“…power of EEG slow wave activity (SWA: 0.75 – 4.5 Hz; Achermann et al., 1993; Borb ´ ely, 2001), the amplitude, the slope and the frequency of individual sleep slow waves/oscillatory cycles, as well as a lower number of multi-peak slow waves (Bersagliere and Acher-mann, 2010; Riedner et al., 2007).”
InfluentialSpontaneous slow oscillation—slow spindle features predict induced overnight memory retention
Dehnavi, F., Koo, P. C., Ghorbani, M., & Marshall, L. (2021) · SLEEP · doi:10.1093/sleep/zsab127 · Cited by 34
Effects of auditory sleep modulation approaches on brain oscillatory and cardiovascular dynamics
Huwiler, S., Carro‐Domínguez, M., Huwyler, S., Kiener, L., Stich, F. M., Sala, R., Aziri, F., Trippel, A., Schmied, C. M., Huber, R., et al. (2022) · SLEEP · doi:10.1093/sleep/zsac155 · Cited by 28
Self-citationA Dynamical Role for Acetylcholine in Synaptic Renormalization
Fink, C. G., Murphy, G. G., Żochowski, M., & Booth, V. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002939 · Cited by 30
“In addition, multiple lines of evidence suggest that slow waves involve the persistent synchronous bursting of cortical neuron populations [5,50–52].”
BackgroundBDNF-TrkB signaling orchestrates the buildup process of local sleep
ElGrawani, W., Sun, G., Kliem, F. P., Sennhauser, S., Pierre-Ferrer, S., Rosi‐Andersen, A., Boccalaro, I. L., Bethge, P., Heo, W. D., Helmchen, F., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114500 · Cited by 32
Besedovsky, L., Dang, R., Engert, L. C., Goldstein, M. R., Devine, J. K., Bertisch, S. M., Mullington, J. M., Simpson, N. S., & Haack, M. (2022) · PNAS Nexus · doi:10.1093/pnasnexus/pgac004 · Cited by 30
“Slow wave morphology including count and amplitude of slow waves was examined using previously described procedures (70, 72).”
Impaired slow wave sleep downscaling in patients with infantile spasms
Fattinger, S., Schmitt, B., Bölsterli, B. K., Critelli, H., Jenni, O. G., & Huber, R. (2014) · European Journal of Paediatric Neurology · doi:10.1016/j.ejpn.2014.11.002 · Cited by 30
Self-citationPavlidis, E., Møller, R. S., Nikanorova, M., Kölmel, M. S., Stendevad, P., Beniczky, S., Tassinari, C. A., Rubboli, G., & Gardella, E. (2019) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2019.05.030 · Cited by 28
Pisarenco, I., Caporro, M., Prosperetti, C., & Manconi, M. (2014) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2014.01.002 · Cited by 26
Visual imagery and visual perception induce similar changes in occipital slow waves of sleep
Bernardi, G., Betta, M., Cataldi, J., Leo, A., Haba‐Rubio, J., Heinzer, R. C., Cirelli, C., Tononi, G., Pietrini, P., Ricciardi, E., et al. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00085.2019 · Cited by 25
Self-citationMongrain, V., Carrier, J., Paquet, J., Bélanger-Nelson, E., & Dumont, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022679 · Cited by 26
“This is consistent with a previous report showing a strong association between SWA and SW slope [6], which lead the authors to propose that SW slope might therefore be regarded as an additional marker of sleep homeostasis.”
BackgroundResultSleep and Synaptic Homeostasis
Vyazovskiy, V. V., & Faraguna, U. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_301 · Cited by 35
“Notably, it has been found that sleep with high SWA, such as under high sleep pressure, is characterized by increased local and global synchronization of cortical neuronal activity (Destexhe et al. 1999; Nir et al. 2011; Riedner et al. 2007; Vyazovskiy et al. 2004a, 2009b, 2011a), suggesting that either functional and…”
BackgroundResultInfluentialSelf-citationThe effects of theta-burst stimulation on sleep and vigilance in humans
Mensen, A., Gorban, C., Niklaus, M., Kuske, E., & Khatami, R. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00420 · Cited by 24
“Research on the clinical benefits of TMS for patients with medication-resistant, major depressive disorder (George et al., 2013), as well as Parkinson’s Disease (Elahi et al., 2009; Benninger et al., 2011) may also provide links to the vigilance system.”
BackgroundThe occurrence of individual slow waves in sleep is predicted by heart rate
Mensen, A., Zhang, Z., Qi, M., & Khatami, R. (2016) · Scientific Reports · doi:10.1038/srep29671 · Cited by 25
Vyazovskiy, V. V., Palchykova, S., Achermann, P., Tobler, I., & Deboer, T. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx020 · Cited by 23
“Notably, the magnitude of the sleep-dependent change differs between specific slow-wave parameters, and their relative contribution to the overall signal accounts well for the observed changes in the EEG power spectra (Riedner et al. 2007; Vyazovskiy et al. 2007).”
BackgroundMethodInfluentialSelf-citationState-Dependent Modulation of Slow Wave Motifs towards Awakening
Shimaoka, D., Song, C., & Knöpfel, T. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00108 · Cited by 31
“…directions along major anatomical pathways (Massimini et al., 2004; Murphy et al., 2009; Botella-Soler et al., 2012) and individual waves may be driven by distinct cortical origins (Massimini et al., 2004; Volgushev et al., 2006; Riedner et al., 2007; Kurth et al., 2010; Nir et al., 2011).”
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“It is generally described as the best measure to assess the synaptic strength and sleep homeostasis compared to other classic parameters (Bersagliere and Achermann, 2010; Riedner et al., 2007).”
BackgroundBhagwandin, A., Gravett, N., Bennett, N. C., & Manger, P. R. (2013) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2013.06.002 · Cited by 25
Ontogeny of Sleep and Its Functions in Infancy, Childhood, and Adolescence
Grigg-Damberger, M. M. (2016) · Springer eBooks · doi:10.1007/978-3-319-28640-2_1 · Cited by 34
Computer Based Synchronization Analysis on Sleep EEG in Insomnia
Aydın, S. (2009) · Journal of Medical Systems · doi:10.1007/s10916-009-9387-1 · Cited by 24
Pinggal, E., Dockree, P. M., O’Connell, R. G., Bellgrove, M. A., & Andrillon, T. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0836-22.2022 · Cited by 25
Juan, E., Górska, U., Kozma, C. A., Papantonatos, C., Bugnon, T., Denis, C., Křemen, V., Worrell, G. A., Struck, A. F., Bateman, L. M., et al. (2022) · Brain · doi:10.1093/brain/awac291 · Cited by 23
Self-citationNiizeki, K., & Saitoh, T. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01338 · Cited by 23
Opposite effect of motivated forgetting on sleep spindles during stage 2 and slow wave sleep
Dehnavi, F., Moghimi, S., Haghighi, S. S., Safaie, M., & Ghorbani, M. (2019) · SLEEP · doi:10.1093/sleep/zsz085 · Cited by 24
Metadata
- Authors
- Riedner, B. A., Vyazovskiy, V. V., Huber, R., Massimini, M., Esser, S., Murphy, M., & Tononi, G.
- Affiliations
- University of Wisconsin–Madison (US)
- Corresponding author
- Tononi, Giulio
- ORCID
- Venue
- Sleep
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-12
- Volume
- 30
- Issue
- 12
- Pages
- 1643-1657
- ISSN
- 0161-8105 (ISSN-L)
- 1550-9109
- PMC
- PMC2276133
- OpenAlex
- W1577987636
- Cited by
- 424
- References
- 0
- Citations by year
- 2026: 25 · 2025: 27 · 2024: 28 · 2023: 24 · 2022: 31 · 2021: 31 · 2020: 24 · 2019: 28 · 2018: 20 · 2017: 28 · 2016: 16 · 2015: 20 · 2014: 28 · 2013: 24 · 2012: 19
- FWCI
- 5.00
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- SLEEP (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Open Research (University of Surrey) (submittedVersion)
- Surrey Research Insight Open Access (The University of Surrey) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (106264)
- National Institutes of Health
- National Institute of General Medical Sciences (T32GM007507)
- National Institute of Diabetes and Digestive and Kidney Diseases (T90DK070079)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Keywords
- sleep slow waves, slow-wave activity, sleep homeostasis, cortical synchronization, thalamocortical system, synaptic efficacy, NREM sleep, high-density EEG
- MeSH terms
- Adult, Brain Mapping, Cerebral Cortex, Circadian Rhythm, Computer Simulation, Cortical Synchronization, Electroencephalography, Evoked Potentials, Fourier Analysis, Homeostasis, Humans, Male, Nerve Net, Reference Values, Signal Processing, Computer-Assisted, Sleep, Sleep, REM, Synapses, Thalamus
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