CoChat
Sign Up
Cited by 425Sleep and Wakefulness ResearchNeural dynamics and brain functionSleep and related disorders

The DOI matches its Crossref record.

Sleep Homeostasis and Cortical Synchronization: III. A High-Density EEG Study of Sleep Slow Waves in Humans

Open access
Riedner, Brady A., Vyazovskiy, Vladyslav V., Huber, Reto, Massimini, Marcello, Esser, Steve, Murphy, Michael, Tononi, Giulio·2007·Sleep
DOI 10.1093/sleep/30.12.1643PMC PMC2276133
Open this paper in CoChat — free account

Abstract

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.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1093/sleep/30.12.1643

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

The publisher hasn’t deposited this paper’s reference list.

Research works printed but not linked: 30

  1. [1]Tononi G, Cirelli C. Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull. 2003;62:143–50. doi: 10.1016/j.brainresbull.2003.09.004. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  2. [2]Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Med Rev. 2006;10:49–62. doi: 10.1016/j.smrv.2005.05.002. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  3. [3]Esser S, Hill S, Tononi G. Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. Sleep. 2007;30:1617–30. doi: 10.1093/sleep/30.12.1617. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  4. [4]Vyazovskiy VV, Riedner BA, Cirelli C, Tononi G. Sleep homeostasis and cortical synchronization: II. A local field potential study of sleep slow waves in the rat. Sleep. 2007;30:1631–42. doi: 10.1093/sleep/30.12.1631. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  5. [5]Blake H, Gerard RW. Brain potentials during sleep. Am J Physiol. 1937;119:692–703. [Google Scholar]
  6. [6]Daan S, Beersma DG, Borbély AA. Timing of human sleep: recovery process gated by a circadian pacemaker. Am J Physiol. 1984;246:R161–83. doi: 10.1152/ajpregu.1984.246.2.R161. [DOI] [PubMed] [Google Scholar] · DOI
  7. [7]Borbély AA. A two process model of sleep regulation. Hum Neurobiol. 1982;1:195–204. [PubMed] [Google Scholar]
  8. [8]Borbély AA, Achermann P. Sleep homeostasis and models of sleep regulation. In: Kryger MH, Roth T, Dement WC, editors. Principles and Practice of Sleep Medicine. Philadelphia: Elsevier; 2005. pp. 405–17. [Google Scholar]
  9. [9]Rechtschaffen A, Kales A Public Health Services-National Institutes of Health, National Institute of Neurological Diseases and Blindness, Neurological Information Network. A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Bethesda, Md: U.S. Dept. of Health, Education, and Welfare, Public Health Services-National Institutes of Health, National Institute of Neurological Diseases and Blindness, Neurological Information Network; 1968. [Google Scholar]
  10. [10]Huber R, Graf T, Cote KA, et al. Exposure to pulsed high-frequency electromagnetic field during waking affects human sleep EEG. Neuroreport. 2000;11:3321–5. doi: 10.1097/00001756-200010200-00012. [DOI] [PubMed] [Google Scholar] · DOI
  11. [11]Aeschbach D, Borbély AA. All-night dynamics of the human sleep EEG. J Sleep Res. 1993;2:70–81. doi: 10.1111/j.1365-2869.1993.tb00065.x. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  12. [12]Feinberg I, Floyd TC. Systematic trends across the night in human sleep cycles. Psychophysiology. 1979;16:283–91. doi: 10.1111/j.1469-8986.1979.tb02991.x. [DOI] [PubMed] [Google Scholar] · DOI
  13. [13]Molle M, Marshall L, Gais S, Born J. Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J Neurosci. 2002;22:10941–7. doi: 10.1523/JNEUROSCI.22-24-10941.2002. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  14. [14]Geering BA, Achermann P, Eggimann F, Borbély AA. Period-amplitude analysis and power spectral analysis: a comparison based on all-night sleep EEG recordings. J Sleep Res. 1993;2:121–129. doi: 10.1111/j.1365-2869.1993.tb00074.x. [DOI] [PubMed] [Google Scholar] · DOI
  15. [15]Uchida S, Feinberg I, March JD, et al. A comparison of period amplitude analysis and FFT power spectral analysis of all-night human sleep EEG. Physiol Behav. 1999;67:121–31. doi: 10.1016/s0031-9384(99)00049-9. [DOI] [PubMed] [Google Scholar] · DOI
  16. [16]Feinberg I, March JD, Fein G, et al. Period and amplitude analysis of 0.5–3 c/sec activity in NREM sleep of young adults. Electroencephalogr Clin Neurophysiol. 1978;44:202–13. doi: 10.1016/0013-4694(78)90266-3. [DOI] [PubMed] [Google Scholar] · DOI
  17. [17]Massimini M, Huber R, Ferrarelli F, et al. The sleep slow oscillation as a traveling wave. J Neurosci. 2004;24:6862–70. doi: 10.1523/JNEUROSCI.1318-04.2004. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  18. [18]Hamalainen MS, Ilmoniemi RJ. Interpreting magnetic fields of the brain: minimum norm estimates. Med Biol Eng Comput. 1994;32:35–42. doi: 10.1007/BF02512476. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  19. [19]Silva C, Maltez JC, Trindade E, et al. Evaluation of L1 and L2 minimum norm performances on EEG localizations. Clin Neurophysiol. 2004;115:1657–68. doi: 10.1016/j.clinph.2004.02.009. [DOI] [PubMed] [Google Scholar] · DOI
  20. [20]Siegel S, Castellan NJ. Nonparametric statistics for the behavioral sciences. 2nd ed. New York: McGraw-Hill; 1988. [Google Scholar]
  21. [21]Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp. 2002;15:1–25. doi: 10.1002/hbm.1058. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  22. [22]Landolt HP, Dijk DJ, Achermann P, Borbély AA. Effect of age on the sleep EEG: slow-wave activity and spindle frequency activity in young and middle-aged men. Brain Res. 1996;738:205–12. doi: 10.1016/s0006-8993(96)00770-6. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  23. [23]Glazewski S, Herman C, McKenna M, et al. Long-term potentiation in vivo in layers II/III of rat barrel cortex. Neuropharmacology. 1998;37:581–92. doi: 10.1016/s0028-3908(98)00039-2. [DOI] [PubMed] [Google Scholar] · DOI
  24. [24]O'Boyle MP, Do V, Derrick BE, Claiborne BJ. In vivo recordings of long-term potentiation and long-term depression in the dentate gyrus of the neonatal rat. J Neurophysiol. 2004;91:613–22. doi: 10.1152/jn.00307.2003. [DOI] [PubMed] [Google Scholar] · DOI
  25. [25]Whitlock JR, Heynen AJ, Shuler MG, Bear MF. Learning induces long-term potentiation in the hippocampus. Science. 2006;313:1093–7. doi: 10.1126/science.1128134. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  26. [26]Hill S, Tononi G. Modeling sleep and wakefulness in the thalamocortical system. J Neurophysiol. 2005;93:1671–98. doi: 10.1152/jn.00915.2004. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  27. [27]Timofeev I, Grenier F, Bazhenov M, et al. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex. 2000;10:1185–99. doi: 10.1093/cercor/10.12.1185. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  28. [28]Nunez PL, Srinivasan R. Electric Fields of the Brain: the Neurophysics of EEG. 2nd ed. New York: Oxford; 2006. [Google Scholar]
  29. [29]Colrain IM. The K-complex: a 7-decade history. Sleep. 2005;28:255–73. doi: 10.1093/sleep/28.2.255. [DOI] [PubMed] [Google Scholar] · DOI
  30. [30]Finelli LA, Borbély AA, Achermann P. Functional topography of the human nonREM sleep electroencephalogram. Eur J Neurosci. 2001;13:2282–90. doi: 10.1046/j.0953-816x.2001.01597.x. [DOI] [PubMed] [Google Scholar] · DOI

Cited by

Sorted by citations

See all 425

Related

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
DOI
10.1093/sleep/30.12.1643
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
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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review