Slow Wave Synchronization and Sleep State Transitions

Overview

Journal Sci Rep

Specialty Science

Date 2022 May 6

PMID 35523989

Authors

Dan Guo

Robert J Thomas

Yanhui Liu

Steven A Shea

Jun Lu

Chung-Kang Peng

Affiliations

Soon will be listed here.

Abstract

Spontaneous synchronization over large networks is ubiquitous in nature, ranging from inanimate to biological systems. In the human brain, neuronal synchronization and de-synchronization occur during sleep, with the greatest degree of neuronal synchronization during slow wave sleep (SWS). The current sleep classification schema is based on electroencephalography and provides common criteria for clinicians and researchers to describe stages of non-rapid eye movement (NREM) sleep as well as rapid eye movement (REM) sleep. These sleep stage classifications have been based on convenient heuristic criteria, with little consideration of the accompanying normal physiological changes across those same sleep stages. To begin to resolve those inconsistencies, first focusing only on NREM sleep, we propose a simple cluster synchronization model to explain the emergence of SWS in healthy people without sleep disorders. We apply the empirical mode decomposition (EMD) analysis to quantify slow wave activity in electroencephalograms, and provide quantitative evidence to support our model. Based on this synchronization model, NREM sleep can be classified as SWS and non-SWS, such that NREM sleep can be considered as an intrinsically bistable process. Finally, we develop an automated algorithm for SWS classification. We show that this new approach can unify brain wave dynamics and their corresponding physiologic changes.

Citing Articles

Spontaneous Brain Activity Emerges from Pairwise Interactions in the Larval Zebrafish Brain.

Rosch R, Burrows D, Lynn C, Ashourvan A Phys Rev X. 2025; 14(3).

PMID: 39925410 PMC: 7617382. DOI: 10.1103/PhysRevX.14.031050.

Brainwave Patterns and Metabolic Adaptations in Rowers Crossing the Atlantic: A Case Series Pilot Study.

Chandanathil M, Longman D, Nowak T, Wells J, Muehlenbein M, Stock J Cureus. 2024; 16(11):e74731.

PMID: 39618766 PMC: 11605980. DOI: 10.7759/cureus.74731.

The Role of Epileptic Activity in Alzheimer's Disease.

Chen T, Lai M, Hong W, Huang C Am J Alzheimers Dis Other Demen. 2024; 39:15333175241303569.

PMID: 39576820 PMC: 11585063. DOI: 10.1177/15333175241303569.

[Wearable devices: Perspectives on assessing and monitoring human physiological status].

Peng C, Cui X, Zhang Z, Yu M Sheng Wu Yi Xue Gong Cheng Xue Za Zhi. 2023; 40(6):1045-1052.

PMID: 38151926 PMC: 10753302. DOI: 10.7507/1001-5515.202303043.

Disuse-driven plasticity in the human thalamus and putamen.

Chauvin R, Newbold D, Nielsen A, Miller R, Krimmel S, Metoki A bioRxiv. 2023; .

PMID: 37987000 PMC: 10659348. DOI: 10.1101/2023.11.07.566031.

References

Parrino L, Ferri R, Bruni O, Terzano M . Cyclic alternating pattern (CAP): the marker of sleep instability. Sleep Med Rev. 2011; 16(1):27-45. DOI: 10.1016/j.smrv.2011.02.003. View

Tasali E, Leproult R, Ehrmann D, Van Cauter E . Slow-wave sleep and the risk of type 2 diabetes in humans. Proc Natl Acad Sci U S A. 2008; 105(3):1044-9. PMC: 2242689. DOI: 10.1073/pnas.0706446105. View

Buzsaki G, Draguhn A . Neuronal oscillations in cortical networks. Science. 2004; 304(5679):1926-9. DOI: 10.1126/science.1099745. View

Marshall L, Helgadottir H, Molle M, Born J . Boosting slow oscillations during sleep potentiates memory. Nature. 2006; 444(7119):610-3. DOI: 10.1038/nature05278. View

Wu Z, Huang N, Long S, Peng C . On the trend, detrending, and variability of nonlinear and nonstationary time series. Proc Natl Acad Sci U S A. 2007; 104(38):14889-94. PMC: 1986583. DOI: 10.1073/pnas.0701020104. View

Newell J, Mairesse O, Verbanck P, Neu D . Is a one-night stay in the lab really enough to conclude? First-night effect and night-to-night variability in polysomnographic recordings among different clinical population samples. Psychiatry Res. 2012; 200(2-3):795-801. DOI: 10.1016/j.psychres.2012.07.045. View

Dimitrov T, He M, Stickgold R, Prerau M . Sleep spindles comprise a subset of a broader class of electroencephalogram events. Sleep. 2021; 44(9). PMC: 8436142. DOI: 10.1093/sleep/zsab099. View

Danker-Hopfe H, Anderer P, Zeitlhofer J, Boeck M, Dorn H, Gruber G . Interrater reliability for sleep scoring according to the Rechtschaffen & Kales and the new AASM standard. J Sleep Res. 2009; 18(1):74-84. DOI: 10.1111/j.1365-2869.2008.00700.x. View

Ohayon M, Carskadon M, Guilleminault C, Vitiello M . Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: developing normative sleep values across the human lifespan. Sleep. 2004; 27(7):1255-73. DOI: 10.1093/sleep/27.7.1255. View

10.

Thomas R, Mietus J, Peng C, Goldberger A . An electrocardiogram-based technique to assess cardiopulmonary coupling during sleep. Sleep. 2005; 28(9):1151-61. DOI: 10.1093/sleep/28.9.1151. View

11.

Niizeki K, Saitoh T . Association Between Phase Coupling of Respiratory Sinus Arrhythmia and Slow Wave Brain Activity During Sleep. Front Physiol. 2018; 9:1338. PMC: 6167474. DOI: 10.3389/fphys.2018.01338. View

12.

Hori T, Sugita Y, Koga E, Shirakawa S, Inoue K, Uchida S . Proposed supplements and amendments to 'A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects', the Rechtschaffen & Kales (1968) standard. Psychiatry Clin Neurosci. 2001; 55(3):305-10. DOI: 10.1046/j.1440-1819.2001.00810.x. View

13.

Huber R, Ghilardi M, Massimini M, Tononi G . Local sleep and learning. Nature. 2004; 430(6995):78-81. DOI: 10.1038/nature02663. View

14.

Vanhatalo S, Palva J, Holmes M, Miller J, Voipio J, Kaila K . Infraslow oscillations modulate excitability and interictal epileptic activity in the human cortex during sleep. Proc Natl Acad Sci U S A. 2004; 101(14):5053-7. PMC: 387372. DOI: 10.1073/pnas.0305375101. View

15.

Mietus J, Peng C, Henry I, Goldsmith R, Goldberger A . The pNNx files: re-examining a widely used heart rate variability measure. Heart. 2002; 88(4):378-80. PMC: 1767394. DOI: 10.1136/heart.88.4.378. View

16.

Silber M, Ancoli-Israel S, Bonnet M, Chokroverty S, Grigg-Damberger M, Hirshkowitz M . The visual scoring of sleep in adults. J Clin Sleep Med. 2007; 3(2):121-31. View

17.

Diekelmann S, Born J . The memory function of sleep. Nat Rev Neurosci. 2010; 11(2):114-26. DOI: 10.1038/nrn2762. View

18.

Tononi G, Cirelli C . Sleep function and synaptic homeostasis. Sleep Med Rev. 2005; 10(1):49-62. DOI: 10.1016/j.smrv.2005.05.002. View

19.

Power A . Slow-wave sleep, acetylcholine, and memory consolidation. Proc Natl Acad Sci U S A. 2004; 101(7):1795-6. PMC: 357005. DOI: 10.1073/pnas.0400237101. View

20.

Ujma P, Simor P, Steiger A, Dresler M, Bodizs R . Individual slow-wave morphology is a marker of aging. Neurobiol Aging. 2019; 80:71-82. DOI: 10.1016/j.neurobiolaging.2019.04.002. View