The pathophysiology of recurrent isolated sleep paralysis (RISP) has yet to be fully clarified. Very little research has been performed on electroencephalographic (EEG) signatures outside RISP episodes. This study aimed to investigate whether sleep is disturbed even without the occurrence of a RISP episode and in a stage different than conventional REM sleep. 17 RISP patients and 17 control subjects underwent two consecutive full-night video-polysomnography recordings. Spectral analysis was performed on all sleep stages in the delta, theta, and alpha band. EEG microstate (MS) analysis was performed on the NREM 3 phase due to the overall high correlation of subject template maps with canonical templates. Spectral analysis showed a significantly higher power of theta band activity in REM and NREM 2 sleep stages in RISP patients. The observed rise was also apparent in other sleep stages. Conversely, alpha power showed a downward trend in RISP patients' deep sleep. MS maps similar to canonical topographies were obtained indicating the preservation of prototypical EEG generators in RISP patients. RISP patients showed significant differences in the temporal dynamics of MS, expressed by different transitions between MS C and D and between MS A and B. Both spectral analysis and MS characteristics showed abnormalities in the sleep of non-episodic RISP subjects. Our findings suggest that in order to understand the neurobiological background of RISP, there is a need to extend the analyzes beyond REM-related processes and highlight the value of EEG microstate dynamics as promising functional biomarkers of RISP.

3rd Faculty of Medicine Charles University Prague Czechia

Faculty of Biomedical Engineering Czech Technical University Prague Czechia

Sleep and Chronobiology Research Center National Institute of Mental Health Klecany Czechia

See more in PubMed

Al Zoubi O., Mayeli A., Tsuchiyagaito A., Misaki M., Zotev V., Refai H., et al. . (2019). EEG microstates temporal dynamics differentiate individuals with mood and anxiety disorders from healthy subjects. Front. Hum. Neurosci. 13:56. 10.3389/fnhum.2019.00056 PubMed DOI PMC

Anderson K. N., Pilsworth S., Sharples L. D., Smith I. E., Shneerson J. M. (2007). Idiopathic hypersomnia: a study of 77 cases. Sleep 30, 1274–1281. 10.1093/sleep/30.10.1274 PubMed DOI PMC

Antonova E., Holding M., Suen H. C., Sumich A., Maex R., Nehaniv C. (2022). EEG microstates: functional significance and short-term test-retest reliability. Neuroimage 2:100089. 10.1016/j.ynirp.2022.100089 DOI

Benham G. (2022). Sleep paralysis in college students. J. Am. Coll. Health 70, 1286–1291. 10.1080/07448481.2020.1799807 PubMed DOI

Bettica P., Squassante L., Groeger J., Gennery B., Winsky-Sommerer R., Dijk D.-J. (2012). Differential effects of a dual orexin receptor antagonist (SB-649868) and zolpidem on sleep initiation and consolidation, SWS, REM sleep, and EEG power spectra in a model of situational insomnia. Neuropsychopharmacology 37, 1224–33. 10.1038/npp.2011.310 PubMed DOI PMC

Blaskovich B., Reichardt R., Gombos F., Spoormaker V. I., Simor P. (2020). Cortical hyperarousal in NREM sleep normalizes from pre- to post- REM periods in individuals with frequent nightmares. Sleep 43:zsz201. 10.1093/sleep/zsz201 PubMed DOI

Brèchet L., Brunet D., Perogamvros L., Tononi G., Michel C. (2020). EEG microstates of dreams. Sci. Rep. 10:74075. 10.1038/s41598-020-74075-z PubMed DOI PMC

Britz J., Van De Ville D., Michel C. M. (2010). Bold correlates of EEG topography reveal rapid resting-state network dynamics. NeuroImage 52, 1162–1170. 10.1016/j.neuroimage.2010.02.052 PubMed DOI

Brodbeck V., Kuhn A., von Wegner F., Morzelewski A., Tagliazucchi E., Borisov S., et al. . (2012). EEG microstates of wakefulness and nrem sleep. NeuroImage 62, 2129–2139. 10.1016/j.neuroimage.2012.05.060 PubMed DOI

Buškovà J., Klikovà M. (2019). Recurrent isolated sleep paralysis. Neurologie Pro Praxi 20, 54–56. 10.36290/neu.2018.018 DOI

Çoğaltay N., Karadağ E. (2015). “Introduction to meta-analysis,” in Leadership and Organizational Outcomes, ed. E. Karadağ (Cham: Springer International Publishing; ), 19–28.

Custo A., Van De Ville D., Wells W., Tomescu M., Michel C. (2017). EEG resting-state networks: microstates' source localization. Brain Connect. 7:476. 10.1089/brain.2016.0476 PubMed DOI PMC

Darchia N., Oniani N., Sakhelashvili I., Supatashvili M., Basishvili T., Eliozishvili M., et al. . (2018). Relationship between sleep disorders and health related quality of life–results from the Georgia SOMNUS study. Int. J. Environ. Res. Publ. Health 15:1588. 10.3390/ijerph15081588 PubMed DOI PMC

De Gennaro L., Ferrara M., Bertini M. (2000). The relationship between frequency of rapid eye movements in REM sleep and SWS rebound. J. Sleep Res. 9, 155–159. 10.1046/j.1365-2869.2000.00193.x PubMed DOI

Denis D. (2018). Relationships between sleep paralysis and sleep quality: current insights. Nat. Sci. Sleep 10:355. 10.2147/NSS.S158600 PubMed DOI PMC

Denis D., French C. C., Gregory A. M. (2018). A systematic review of variables associated with sleep paralysis. Sleep Med. Rev. 38, 141–157. 10.1016/j.smrv.2017.05.005 PubMed DOI

Denis D., French C. C., Rowe R., Zavos H. M. S., Nolan P. M., Parsons M. J., et al. . (2015). A twin and molecular genetics study of sleep paralysis and associated factors. J. Sleep Res. 24, 438–446. 10.1111/jsr.12282 PubMed DOI PMC

Dongrui G., Long S., Yang H., Cheng Y., Guo S., Yu Y., et al. . (2020). SWS brain-wave music may improve the quality of sleep: an EEG study. Front. Neurosci. 14:67. 10.3389/fnins.2020.00067 PubMed DOI PMC

Drissi N. M., Szakàcs A., Witt S. T., Wretman A., Ulander M., Stàhlbrandt H., et al. . (2016). Altered brain microstate dynamics in adolescents with narcolepsy. Front. Hum. Neurosci. 10:369. 10.3389/fnhum.2016.00369 PubMed DOI PMC

Fèrat V., Seeber M., Michel C., Ros T. (2020). Beyond broadband: towards a spectral decomposition of EEG microstates. Hum. Brain Map. 16:342378. 10.1101/2020.10.16.342378 PubMed DOI PMC

Held K., Künzel H., Ising M., Schmid D., Zobel A., Murck H., et al. . (2004). Treatment with the CRH1-receptor-antagonist R121919 improves sleep-EEG in patients with depression. J. Psychiat. Res. 38, 129–136. 10.1016/S0022-3956(03)00076-1 PubMed DOI

Inouye T., Shinosaki K., Sakamoto H., Toi S., Ukai S., Iyama A., et al. . (1991). Quantification of EEG irregularity by use of the entropy of the power spectrum. Electroencephal. Clin. Neurophysiol. 79, 204–210. 10.1016/0013-4694(91)90138-T PubMed DOI

Kikuchi M., Koenig T., Munesue T., Hanaoka A., Strik W., Dierks T., et al. . (2011). EEG microstate analysis in drug-naive patients with panic disorder. PLoS ONE 6:22912. 10.1371/journal.pone.0022912 PubMed DOI PMC

Kindler J., Hubl D., Strik W., Dierks T., Koenig T. (2011). Resting-state eeg in schizophrenia: auditory verbal hallucinations are related to shortening of specific microstates. Clin. Neurophysiol. 122, 1179–1182. 10.1016/j.clinph.2010.10.042 PubMed DOI

Klikovà M., Pioreckỳ M., Miletìnovà E., Janku K., Dudysovà D., Buškovà J. (2021). Objective rapid eye movement sleep characteristics of recurrent isolated sleep paralysis: a case-control study. Sleep 44:zsab153. 10.1093/sleep/zsab153 PubMed DOI

Koenig T., Prichep L., Lehmann D., Sosa P. V., Braeker E., Kleinlogel H., et al. . (2002). Millisecond by millisecond, year by year: normative EEG microstates and developmental stages. NeuroImage 16, 41–48. 10.1006/nimg.2002.1070 PubMed DOI

Krylova M., Alizadeh S., Izyurov I., Teckentrup V., Chang C., van der Meer J., et al. . (2021). Evidence for modulation of EEG microstate sequence by vigilance level. NeuroImage 224:117393. 10.1016/j.neuroimage.2020.117393 PubMed DOI

Kuhn A., Brodbeck V., Tagliazucchi E., Morzelewski A., Wegner F., Laufs H. (2014). Narcoleptic patients show fragmented EEG-microstructure during early NREM sleep. Brain Topogr. 28:1. 10.1007/s10548-014-0387-1 PubMed DOI

Lehmann D., Faber P. L., Galderisi S., Herrmann W. M., Kinoshita T., Koukkou M., et al. . (2005). EEG microstate duration and syntax in acute, medication-naïve, first-episode Schizophrenia: a multi-center study. Psychiat. Res. 138, 141–156. 10.1016/j.pscychresns.2004.05.007 PubMed DOI

Lehmann D., Skrandies W. (1980). Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephal. Clin. Neurophysiol. 48, 609–621. PubMed

Li Y., Chen G., Lv J., Hou L., Dong Z., Wang R., et al. . (2022). Abnormalities in resting-state EEG microstates are a vulnerability marker of migraine. J. Headache Pain 23:1414. 10.1186/s10194-022-01414-y PubMed DOI PMC

Liškovà M., Janečkovà D., Kluzovà Kràčmarovà L., Mladà K., Buškovà J. (2016). The occurrence and predictive factors of sleep paralysis in university students. Neuropsychiat. Dis. Treat. 12, 2957–2962. 10.2147/NDT.S115629 PubMed DOI PMC

Mainieri G., Maranci J.-B., Champetier P., Leu-Semenescu S., Gales A., Dodet P., et al. . (2020). Are sleep paralysis and false awakenings different from REM sleep and from lucid REM sleep? A spectral EEG analysis. J. Clin. Sleep Med. 17:9056. 10.5664/jcsm.9056 PubMed DOI PMC

Mantua J., Gravel N., Spencer R. M. C. (2016). Reliability of sleep measures from four personal health monitoring devices compared to research-based actigraphy and polysomnography. Sensors 16:50646. 10.3390/s16050646 PubMed DOI PMC

Maris E., Oostenveld R. (2007). Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 164, 177–190. 10.1016/j.jneumeth.2007.03.024 PubMed DOI

Marquis L. P., Paquette T., Blanchette-Carrière C., Dumel G., Nielsen T. (2017). REM sleep theta changes in frequent nightmare recallers. Sleep 40:zsx110. 10.1093/sleep/zsx110 PubMed DOI PMC

Michel C. M., Koenig T. (2018). EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: a review. NeuroImage 180, 577–593. 10.1016/j.neuroimage.2017.11.062 PubMed DOI

Mokhlesi B., Punjabi N. M. (2012). “REM-related” obstructive sleep apnea: an epiphenomenon or a clinically important entity? Sleep 35, 5–7. 10.5665/sleep.1570 PubMed DOI PMC

Mukai J., Uchida S., Miyazaki S., Nishihara K., Honda Y. (2003). Spectral analysis of all-night human sleep EEG in narcoleptic patients and normal subjects. J. Sleep Res. 12, 63–71. 10.1046/j.1365-2869.2003.00331.x PubMed DOI

Nishida K., Morishima Y., Yoshimura M., Isotani T., Irisawa S., Jann K., et al. . (2013). EEG microstates associated with salience and frontoparietal networks in Frontotemporal dementia, Schizophrenia and Alzheimer's disease. Clin. Neurophysiol. 124, 1106–1114. 10.1016/j.clinph.2013.01.005 PubMed DOI

Oostenveld R., Fries P., Maris E., Schoffelen J. M. (2011). Fieldtrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011:156869. 10.1155/2011/156869 PubMed DOI PMC

Pascual-Marqui R., Lehmann D., Faber P., Milz P., Kochi K., Yoshimura M., et al. . (2014). The resting microstate networks (RMN): cortical distributions, dynamics, and frequency specific information flow. ArXiv 1411:1949. 10.48550/arXiv.1411.1949 DOI

Pascual-Marqui R., Michel C., Lehmann D. (1995). Segmentation of brain electrical activity into microstates: model estimation and validation. IEEE Trans. Biomed. Eng. 42, 658–665. PubMed

Piorecky M., Koudelka V., Strobl J., Brunovsky M., Krajca V. (2019). Artifacts in simultaneous HDEEG/FMRI imaging: a nonlinear dimensionality reduction approach. Sensors 19:970. 10.3390/s19204454 PubMed DOI PMC

Sateia M. J. (2014). International classification of sleep disorders-third edition. Chest 146, 1387–1394. 10.1378/chest.14-0970 PubMed DOI

Sharpless B. (2016). A clinician's guide to recurrent isolated sleep paralysis. Neuropsychiat. Dis. Treat. 12:S100307. 10.2147/NDT.S100307 PubMed DOI PMC

Sharpless B. A., Barber J. P. (2011). Lifetime prevalence rates of sleep paralysis: a systematic review. Sleep Med. Rev. 15, 311–315. 10.1016/j.smrv.2011.01.007 PubMed DOI PMC

Simor P., Blaskovich B. (2019). The pathophysiology of nightmare disorder: signs of impaired sleep regulation and hyperarousal. J. Sleep Res. 28:e12867. 10.1111/jsr.12867 PubMed DOI

Simor P., Horvàth K., Ujma P. P., Gombos F., Bòdizs R. (2013). Fluctuations between sleep and wakefulness: wake-like features indicated by increased EEG alpha power during different sleep stages in nightmare disorder. Biol. Psychol. 94, 592–600. 10.1016/j.biopsycho.2013.05.022 PubMed DOI

Simor P., Körmendi J., Horvàth K., Gombos F., Ujma P. P., Bòdizs R. (2014). Electroencephalographic and autonomic alterations in subjects with frequent nightmares during pre-and post-REM periods. Brain Cogn. 91, 62–70. 10.1016/j.bandc.2014.08.004 PubMed DOI

Slepian D. (1978). Prolate spheroidal wave functions, fourier analysis, and uncertainty—v: the discrete case. Bell Syst. Tech. J. 57, 1371–1430.

Stefani A., Högl B. (2021). Nightmare disorder and isolated sleep paralysis. Neurotherapeutics 18, 100–106. 10.1007/s13311-020-00966-8 PubMed DOI PMC

Takeuchi T., Miyasita A., Sasaki Y., Inugami M., Fukuda K. (1992). Isolated sleep paralysis elicited by sleep interruption. Sleep 15, 217–225. PubMed

Tarailis P., Šimkutė D., Koenig T., Griškova-Bulanova I. (2021). Relationship between spatiotemporal dynamics of the brain at rest and self-reported spontaneous thoughts: an EEG microstate approach. J. Personal. Med. 11:111216. 10.3390/jpm11111216 PubMed DOI PMC

Terzaghi M., Ratti P. L., Manni F., Manni R. (2011). Sleep paralysis in narcolepsy: more than just a motor dissociative phenomenon? Neurol. Sci. 33, 169–172. 10.1007/s10072-011-0644-y PubMed DOI

van der Wijk G., Blaskovich B., Farahzadi Y., Simor P. (2020). Unaltered EEG spectral power and functional connectivity in REM microstates in frequent nightmare recallers: are nightmares really a REM parasomnia? Sleep Med. 75, 192–200. 10.1016/j.sleep.2020.07.014 PubMed DOI

Walther B. W., Schulz H. (2004). Recurrent isolated sleep paralysis: polysomnographic and clinical findings. Somnologie 8, 53–60. 10.1111/j.1439-054X.2004.00017.x DOI

Wròbel-Knybel P., Flis M., Rog J., Jalal B., Wołkowski L., Karakuła-Juchnowicz H. (2022). Characteristics of sleep paralysis and its association with anxiety symptoms, perceived stress, ptsd, and other variables related to lifestyle in selected high stress exposed professions. Int. J. Environ. Res. Publ. Health 19:7821. 10.3390/ijerph19137821 PubMed DOI PMC

Zhao W., Van Someren E. J., Li C., Chen X., Gui W., Tian Y., et al. . (2021). EEG spectral analysis in insomnia disorder: a systematic review and meta-analysis. Sleep Med. Rev. 59:101457. 10.1016/j.smrv.2021.101457 PubMed DOI