Detecting slow wave sleep and rapid eye movement stage using cortical effective connectivity

Detecting slow wave sleep and rapid eye movement stage using cortical effective connectivity

In recent neuroimaging research, there has been considerable interest in identifying neuromarkers of sleep. Automatic slow wave sleep (SWS) and rapid eye movement (REM) are two known phases of sleep. However, the level by which those changes contribute to brain interactions has not been well characterized. In recent years, it has been shown that brain connectivity measuring can be helpful in investigation of behavioral states of the brain. By considering the fact that brains have different states in different stages of sleep, the present work employs effective connectivity and machine-learning analysis to quantify and classify SWS and REM stages of sleep. We examine low-density 12-channel EEG data from 8 healthy participants during a full night of sleep. Data were epoched into 30-s windows and SWS and REM stages were labeled by a sleep consultant. Effective connectivity was quantified using a directed metric, generalized partial directed coherence, and measures were used as input features for a machine-learning system. A support vector machine classifier was used to solve 2 binary problems of REM vs. nREM and SWS vs. nSWS. Findings revealed an excellent balanced accuracy of 89.80% in REM detection and 87.32% in SWS detection. Overall, our work demonstrates a successful application of effective connectivity analysis and machine learning for sleep neuromarkers in EEG.

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  • [1] AASM. The AASM Manual for the Scoring of Sleep and Associated Events-Rules. Terminology and Technical Specifications. Chicago, IL, USA: American Academy of Sleep Medicine, 2007.
  • [2] Van Cauter E, Spiegel K, Tasali E, Leproult R. Metabolic consequences of sleep and sleep loss. Sleep Med 2008; 9: 23-28.
  • [3] Van Cauter E, Leproult R, Plat L. Age-related changes in slow wave sleep and REM sleep and relationship with growth hormone and cortisol levels in healthy men. J Am Med Assoc 2000; 84: 861-868.
  • [4] Majde JA, Krueger JM. Links between the innate immune system and sleep. J Allergy Clin Immunol 2005; 116: 1188-1198.
  • [5] Tasali E, Leproult R, Ehrmann DA, Van Cauter E. Slow-wave sleep and the risk of type 2 diabetes in humans. P Natl Acad Sci USA 2008; 105: 1044-1049.
  • [6] Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci 2010; 11: 114-126.
  • [7] Kyung Lee E, Douglass AB. Sleep in psychiatric disorders: where are we now? Can J Psychiatry 2010; 55: 403-412.
  • [8] Fung MM, Peters K, Redline S, Ziegler MG, Ancoli-Israel S, Barrett-Connor E, Stone KL. Decreased slow wave sleep increases risk of developing hypertension in elderly men. Hypertension 2011; 58: 596-603.
  • [9] Park HJ,Oh JS, Jeong DU, Park KS. Automated sleep stage scoring using hybrid rule-and case-based reasoning. Comput Biomed Res 2000; 33: 330-349.
  • [10] Agarwal R, Gotman J. Computer-assisted sleep staging. IEEE T Biomed 2001; 48: 1412-1423.
  • [11] Caffarel J, Gibson GJ, Harrison JP, Griffiths CJ, Drinnan MJ. Comparison of manual sleep staging with automated neural network-based analysis in clinical practice. Med Biol Eng Comput 2006; 44: 105-110.
  • [12] Poree F, Kachenoura A, Gauvrit H, Morvan C, Carrault G, Senhadji L. Blind source separation for ambulatory sleep recording. IEEE T Inf Technol Biomed 2006; 10: 293-301.
  • [13] Tagluk ME, Sezgin N, Akin M. Estimation of sleep stages by an artificial neural network employing EEG, EMG and EOG. J Med Syst 2010; 34: 717-725.
  • [14] Liang SF, Kuo CE, Hu YH, Cheng YS. A rule-based automatic sleep staging method. J Neurosci Methods 2012; 205: 169-176.
  • [15] Pan ST, Kuo CE, Zeng JH, Liang SF. A transition-constrained discrete hidden Markov model for automatic sleep staging. Biomed Eng Online 2012; 11: 52.
  • [16] Diekelmann S, Wilhelm I, Born J. The whats and whens of sleep-dependent memory consolidation. Sleep Med Rev 2009; 13: 309-321.
  • [17] Bellesi M, Riedner BA, Garcia-Molina GN, Cirelli C, Tononi G. Enhancement of sleep slow waves: underlying mechanisms and practical consequences. Front Syst Neurosci 2014; 8: 208.
  • [18] Huber R, Ghilardi MF, Massimini M, Ferrarelli F, Riedner BA, Peterson MJ, Tononi G. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat Neurosci 2006; 9: 1169-1176.
  • [19] Ngo HV, Claussen JC, Born J, Molle M. Induction of slow oscillations by rhythmic acoustic stimulation. J Sleep Res 2013; 22: 22-31.
  • [20] Tononi G, Riedner BA, Hulse BK, Ferrarelli F, Sarasso S. Enhancing sleep slow waves with natural stimuli. Medicamundi 2010; 54: 82-88.
  • [21] Ngo HV, Miedema A, Faude I, Martinetz T, Molle M, Born J. Driving sleep slow oscillations by auditory closed-loop stimulation–a self-limiting process. J Neurosci 2015; 35: 6630-6638.
  • [22] van Poppel EAM. Predicting brainwaves: The influence of auditory closed-loop cueing during slow oscillation upstates on vocabulary memory. MSc, University of Amsterdam, Amsterdam, the Netherlands, 2016.
  • [23] Papalambros NA, Santostasi G, Malkani RG, Braun R, Weintraub S, Paller KA, Zee PC. Acoustic enhancement of sleep slow oscillations and concomitant memory improvement in older adults. Front Hum Neurosci 2017; 11: 1-14.
  • [24] Ong JL, Lo JC, Chee NI, Santostasi G, Paller KA, Zee PC, Chee MW. Effects of phase-locked acoustic stimulation during a nap on EEG spectra and declarative memory consolidation. Sleep Med 2016; 20: 88-97.
  • [25] Leminen MN, Virkkala J, Saure E, Paajanen T, Zee PC, Santostasi G, Hublin C, Muller K, Porkka-Heiskanen T, Huotilainen M et al. Enhanced memory consolidation via automatic sound stimulation during non-REM sleep. Sleep 2017; 40: zsx00.
  • [26] Schabus M, Dang-Vu T, Heib D, Boly M, Desseilles M, Vandewalle G, Schmidt C, Albouy G, Darsaud A, Gais S et al. The fate of incoming stimuli during NREM sleep is determined by spindles and the phase of the slow oscillation. Front Neurol 2012; 3: 40.
  • [27] Lustenberger C, Boyle MR, Alagapan S, Mellin JM, Vaughn BV, Frohlich F. Feedback-controlled transcranial alternating current stimulation reveals a functional role of sleep spindles in motor memory consolidation. Curr Biol 2016; 26: 2127-2136.
  • [28] Kim YK, Park E, Lee A, Im CH, Kim YH. Changes in network connectivity during motor imagery and execution. PLoS One 2018; 13: e0190715.
  • [29] Parker CS, Clayden JD, Cardoso MJ, Rodionov R, Duncan JS, Scott C, Diehl B, Ourselin S. Structural and effective connectivity in focal epilepsy. Neuroimage Clin 2018; 17: 943-952.
  • [30] Jobst BM, Hindriks R, Laufs H, Tagliazucchi E, Hahn G, Ponce-Alvarez A, Stevner ABA, Kringelbach ML, Deco G. Increased stability and breakdown of brain effective connectivity during slow-wave sleep: mechanistic insights from whole-brain computational modelling. Sci Rep-UK 2017; 7: 4634.
  • [31] Geweke J. Measurement of linear dependence and feedback between multiple time series. J Am Stat Assoc 1982; 77: 304-324.
  • [32] Kaminski M, Blinowska KJ. A new method of the description of the information flow in brain structures. Biol Cybern 1991; 65: 203-210.
  • [33] Baccala LA, Sameshima K. Partial directed coherence: a new conception in neural structure determination. Biol Cybern 2001; 84: 463-474.
  • [34] Baccala LA, Sameshima K, Takahashi DY. Generalized partial directed coherence. In: IEEE 2007 15th International Conference on Digital Signal Processing. New York, NY, USA: IEEE. pp. 163-166.
  • [35] Berthomier C, Drouot X, Herman-Stoica M, Berthomier P, Prado J, Bokar-Thire D, Benoit O, Mattout J, D’Ortho MP. Automatic analysis of single-channel sleep EEGg: validation in healthy individuals. Sleep 2007; 30: 1587-1595.
  • [36] Seifpour S, Niknazar H, Mikaeili M, Nasrabadi AM. A new automatic sleep staging system based on statistical behavior of local extrema using single channel EEG signal. Expert Syst Appl 2018; 104: 277-293.
  • [37] Akaike H. Information theory and an extension of the maximum likelihood principle. In: 2nd International Symposium on Information Theory; 2–8 September 1971; Tsahkadsor, Armenia. Budapest, Hungary: Akademiai Kiad. pp. 267-281.
  • [38] Delorme A, Mullen T, Kothe C, Acar ZA, Bigdely-Shamlo N, Vankov A, Makeig S. EEGLAB, SIFT, NFT, BCILAB, and ERICA: New tools for advanced EEG processing. Comput Intell Neurosci 2011; 2011: 130714.
  • [39] Dietterich TG, Bakiri G. Solving multiclass learning problems via error-correcting output codes. arXiv 1994: Cs/9501101.
  • [40] Cohen JA. Coefficient of agreement for nominal scales. Educ Psyhol Meas 1960; 20: 37-46.
  • [41] Kreyszig E. Advanced Engineering Mathematics. 4th ed. New York, NY, USA: Wiley, 1979.
  • [42] Kubicki S, Holler L, Berg I, Pastelak-Price C, Dorow R. Sleep EEG evaluation: a comparison of results obtained by visual scoring and automatic analysis with the Oxford sleep stager. Sleep 1989; 12: 140-149.
  • [43] Durka PJ, Malinowska U, Szelenberger W, Wakarow A, Blinowska KJ. High resolution parametric description of slow wave sleep. J Neurosci Meth 2005; 147: 15-21.
  • [44] Virkkala J, Hasan J, Varri A, Himanen S, Muller K. Automatic detection of slow wave sleep using two channel electro-oculography. J Neurosci Methods 2007; 160: 171-177.
  • [45] Su B, Luo Y, Hong C, Nagurka ML, Yen C. Detecting slow wave sleep using a single EEG signal channel. J Neurosci Methods 2015; 243: 47-52.
  • [46] Imtiaz SA, Rodriguez-Villegas E. A low computational cost algorithm for REM sleep detection using single channel EEG. Ann Biomed Eng 2014; 42: 2344-2359.
  • [47] Liang S, Kuo C, Hu Y, Pan Y, Wang Y. Automatic stage scoring of single-channel sleep EEG by using multiscale entropy and autoregressive models. IEEE T Instrum Meas 2012; 61: 1649-1657.
  • [48] Ronzhina M, Janousek O, Kolarova J, Novakova M, Honzik P, Provaznik I. Sleep scoring using artificial neural networks. Sleep Med Rev 2012; 16: 251-263.
  • [49] Hsu YL, Yang YT, Wang JS, Hsu CY. Automatic sleep stage recurrent neural classifier using energy features of EEG signals. Neurocomputing 2013; 104: 105-114.
  • [50] Bajaj V, Pachori RB. Automatic classification of sleep stages based on the time-frequency image of EEG signals. Comput Methods Programs Biomed 2013; 112: 320-328.
  • [51] Zhu G, Li Y, Wen P. Analysis and classification of sleep stages based on difference visibility graphs from a singlechannel EEG signal. IEEE J Biomed Health Inform 2014; 18: 1813-1821.
  • [52] Hassan AR, Bhuiyan MI. Automated identification of sleep states from EEG signals by means of ensemble empirical mode decomposition and random under sampling boosting. Comput Methods Programs Biomed 2017; 140: 201-210.
Turkish Journal of Electrical Engineering and Computer Sciences-Cover
  • ISSN: 1300-0632
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK