The duration of slow-wave sleep (SWS) is related to the reported sleep quality and to the important variables of mental and physical health. The internal cues to end an episode of SWS are poorly understood. One such internal cue is the initiation of a body movement, which is detectable as electromyographic (EMG) activity in sleep-electroencephalography (EEG). In the present study, we characterized the termination of SWS episodes by movement to explore its potential as a biomarker. To this end, we characterized the relation between the occurrence of SWS termination by movement and individual characteristics (age, sex), SWS duration and spectral content, chronotype, depression, medication, overnight memory performance, and, as a potential neurological application, epilepsy. We analyzed 94 full-night EEG-EMG recordings (75/94 had confirmed epilepsy) in the video-EEG monitoring unit of the EpiCARE Centre Salzburg, Austria. Segments of SWS were counted and rated for their termination by movement or not through the visual inspection of continuous EEG and EMG recordings. Multiple linear regression was used to predict the number of SWS episodes that ended with movement by depression, chronotype, type of epilepsy (focal, generalized, no epilepsy, unclear), medication, gender, total duration of SWS, occurrence of seizures during the night, occurrence of tonic-clonic seizures during the night, and SWS frequency spectra. Furthermore, we assessed whether SWS movement termination was related to overnight memory retention. According to multiple linear regression, patients with overall longer SWS experienced more SWS episodes that ended with movement (t = 5.64; p = 0.001). No other variable was related to the proportion of SWS that ended with movement, including no epilepsy-related variable. A small sample (n = 4) of patients taking Sertraline experienced no SWS that ended with movement, which was significant compared to all other patients (t = 8.00; p < 0.001) and to n = 35 patients who did not take any medication (t = 4.22; p < 0.001). While this result was based on a small subsample and must be interpreted with caution, it warrants replication in a larger sample with and without seizures to further elucidate the role of the movement termination of SWS and its potential to serve as a biomarker for sleep continuity and for medication effects on sleep.

Department of Neurology Neurointensive Care and Neurorehabilitation Christian Doppler University Hospital Paracelsus Medical University Centre for Neuroscience Salzburg Member of the European Reference Network EpiCARE 5020 Salzburg Austria

Faculty of Pharmaceutical Sciences University of Iceland 102 Reykjavík Iceland

Faculty of Psychology University of Akureyri 600 Akureyri Iceland

Faculty of Social Studies Masaryk University 601 77 Brno Czech Republic

Neuroscience Institute Christian Doppler University Hospital Centre for Cognitive Neuroscience 5020 Salzburg Austria

Zobrazit více v PubMed

Dijk D. Regulation and Functional Correlates of Slow Wave Sleep. J. Clin. Sleep Med. 2009;5:6. doi: 10.5664/jcsm.5.2s.s6. PubMed DOI PMC

Rechtschaffen A., Kales A. A Manual of Standardized Terminology, Techniques and Scoring Systems for Sleep Stages of Human Subjects. Public Health Service, US Government Printing Office; Washington, DC, USA: 1968.

Iber C., Ancoli-Israel S., Chesson A., Quan S.F., American Academy of Sleep Medicine . The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. American Academy of Sleep Medicine; Westchester, NY, USA: 2007.

Ohayon M.M., Carskadon M.A., Guilleminault C., Vitiello M.V. Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: Developing normative sleep values across the human lifespan. Sleep. 2004;27:1255. doi: 10.1093/sleep/27.7.1255. PubMed DOI

Brunner D.P., Dijk D., Borbély A.A. A quantitative analysis of phasic and tonic submental EMG activity in human sleep. Physiol. Behav. 1990;48:741–748. doi: 10.1016/0031-9384(90)90219-T. PubMed DOI

Agnew H.W., Webb W.B., Williams R.L. The effects of stage four sleep deprivation. Electroencephalogr. Clin. Neurophysiol. 1964;17:68–70. doi: 10.1016/0013-4694(64)90011-2. PubMed DOI

Ferrara M., De Gennaro L., Bertini M. Selective slow-wave sleep (SWS) deprivation and SWS rebound: Do we need a fixed SWS amount per night? Sleep Res. Online. 1999;2:15–19. PubMed

Tasali E., Leproult R., Ehrmann D.A., Van Cauter E. Slow-wave sleep and the risk of type 2 diabetes in humans. Proc. Natl. Acad. Sci. USA. 2008;105:1044–1049. doi: 10.1073/pnas.0706446105. PubMed DOI PMC

Dijk D.J., Beersma D.G.M. Effects of SWS deprivation on subsequent EEG power density and spontaneous sleep duration. Electroencephalogr. Clin. Neurophysiol. 1989;72:312–320. doi: 10.1016/0013-4694(89)90067-9. PubMed DOI

Dijk D.J., Beersma D.G., Daan S., Bloem G.M., Van den Hoofdakker R.H. Quantitative analysis of the effects of slow wave sleep deprivation during the first 3 h of sleep on subsequent EEG power density. Eur. Arch. Psychiatry Neurol. Sci. 1987;236:323–328. doi: 10.1007/BF00377420. PubMed DOI

López-Gomáriz E., Hoyo-Rodrigo B., Rodríguez-Nieto I. The effects of epileptic seizures on sleep architecture. Rev. Neurol. 2004;38:176–180. doi: 10.33588/rn.3802.2003428. PubMed DOI

Eyjólfsdóttir S.G., Trinka E., Höller Y. Shorter duration of slow wave sleep is related to symptoms of depression in patients with epilepsy. Epilepsy Behav. 2023;149:109515. doi: 10.1016/j.yebeh.2023.109515. PubMed DOI

Edwards B.A., O’Driscoll D.M., Ali A., Jordan A.S., Trinder J., Malhotra A. Aging and Sleep: Physiology and Pathophysiology. Semin. Respir. Crit. Care Med. 2010;31:618–633. doi: 10.1055/s-0030-1265902. PubMed DOI PMC

Höller Y., Gudjónsdottir B.E., Valgeirsdóttir S.K., Heimisson G.T. The effect of age and chronotype on seasonality, sleep problems, and mood. Psychiatry Res. 2021;297:113722. doi: 10.1016/j.psychres.2021.113722. PubMed DOI

Colelli D.R., Dela Cruz G.R., Kendzerska T., Murray B.J., Boulos M.I. Impact of sleep chronotype on in-laboratory polysomnography parameters. J. Sleep Res. 2023;32:e13922. doi: 10.1111/jsr.13922. PubMed DOI

Krishnan V., Collop N. Gender differences in sleep disorders. Curr. Opin. Pulm. Med. 2006;12:383–389. doi: 10.1097/01.mcp.0000245705.69440.6a. PubMed DOI

Steiger A., Pawlowski M. Depression and Sleep. Int. J. Mol. Sci. 2019;20:607. doi: 10.3390/ijms20030607. PubMed DOI PMC

Carvalho B.M.S., Chaves J., Silva A.M.d. Effects of antiepileptic drugs on sleep architecture parameters in adults. Sleep Sci. 2022;15:224–244. doi: 10.5935/1984-0063.20220045. PubMed DOI PMC

Diekelmann S., Wilhelm I., Born J. The whats and whens of sleep-dependent memory consolidation. Sleep Med. Rev. 2009;13:309–321. doi: 10.1016/j.smrv.2008.08.002. PubMed DOI

Johnson L.C., Naitoh P., Moses J.M., Lubin A. Interaction of REM Deprivation and Stage 4 Deprivation With Total Sleep Loss: Experiment 2. Psychophysiology. 1974;11:147–159. doi: 10.1111/j.1469-8986.1974.tb00835.x. PubMed DOI

Aeschbach D., Cutler A.J., Ronda J.M. A Role for Non-Rapid-Eye-Movement Sleep Homeostasis in Perceptual Learning. J. Neurosci. 2008;28:2766–2772. doi: 10.1523/JNEUROSCI.5548-07.2008. PubMed DOI PMC

Tononi G., Huber R., Felice Ghilardi M., Massimini M. Local sleep and learning. Nature. 2004;430:78–81. doi: 10.1038/nature02663. PubMed DOI

Deak M.C., Stickgold R., Pietras A.C., Nelson A.P., Bubrick E.J. The role of sleep in forgetting in temporal lobe epilepsy: A pilot study. Epilepsy Behav. 2011;21:462–466. doi: 10.1016/j.yebeh.2011.04.061. PubMed DOI PMC

Malow B.A. The interaction between sleep and epilepsy. Epilepsia. 2007;48:36–38. doi: 10.1111/j.1528-1167.2007.01400.x. PubMed DOI

Galer S., Urbain C., De Tiège X., Emeriau M., Leproult R., Deliens G., Nonclerq A., Peigneux P., Van Bogaert P. Impaired sleep-related consolidation of declarative memories in idiopathic focal epilepsies of childhood. Epilepsy Behav. 2015;43:16–23. doi: 10.1016/j.yebeh.2014.11.032. PubMed DOI

Bjørnæs H., Bakke K.A., Larsson P.G., Heminghyt E., Rytter E., Brager-Larsen L.M., Eriksson A. Subclinical epileptiform activity in children with electrical status epilepticus during sleep: Effects on cognition and behavior before and after treatment with levetiracetam. Epilepsy Behav. 2013;27:40–48. doi: 10.1016/j.yebeh.2012.12.007. PubMed DOI

Urbain C., Di Vincenzo T., Peigneux P., Van Bogaert P. Is sleep-related consolidation impaired in focal idiopathic epilepsies of childhood? A pilot study. Epilepsy Behav. 2011;22:380–384. doi: 10.1016/j.yebeh.2011.07.023. PubMed DOI

Halász P., Ujma P.P., Fabó D., Bódizs R., Szűcs A. Epilepsy as a derailment of sleep plastic functions may cause chronic cognitive impairment—A theoretical review. Sleep Med. Rev. 2019;45:31–41. doi: 10.1016/j.smrv.2019.01.003. PubMed DOI

Latreille V., Schiller K., Peter-Derex L., Frauscher B. Does epileptic activity impair sleep-related memory consolidation in epilepsy? A critical and systematic review. J. Clin. Sleep Med. 2022;18:2481–2495. doi: 10.5664/jcsm.10166. PubMed DOI PMC

Benca R.M., Obermeyer W.H., Larson C.L., Yun B., Dolski I., Kleist K.D., Weber S.M., Davidson R.J. EEG alpha power and alpha power asymmetry in sleep and wakefulness. Psychophysiology. 1999;36:430–436. doi: 10.1111/1469-8986.3640430. PubMed DOI

Purcell S.M., Manoach D.S., Demanuele C., Cade B.E., Mariani S., Cox R., Panagiotaropoulou G., Saxena R., Pan J.Q., Smoller J.W., et al. Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nat. Commun. 2017;8:15930. doi: 10.1038/ncomms15930. PubMed DOI PMC

Driver H.S., Dijk D., Werth E., Biedermann K., Borbely A.A. Sleep and the sleep electroencephalogram across the menstrual cycle in young healthy women. J. Clin. Endocrinol. Metab. 1996;81:728–735. doi: 10.1210/jc.81.2.728. PubMed DOI

Fogel S., Smith C., Peigneux P. Principles and Practice of Sleep Medicine. 7th ed. Elsevier Inc.; Amsterdam, The Netherlands: 2022. Chapter 29—Memory Processing in Relation to Sleep; pp. 311–320.e6.

Dobesberger J., Höfler J., Leitinger M., Kuchukhidze G., Zimmermann G., Thomschewski A., Unterberger I., Walser G., Kalss G., Rohracher A., et al. Personalized safety measures reduce the adverse event rate of long-term video EEG. Epilepsia Open. 2017;2:400–414. doi: 10.1002/epi4.12078. PubMed DOI PMC

Egger-Rainer A., Trinka E., Höfler J., Dieplinger A.M. Epilepsy monitoring—The patients’ views: A qualitative study based on Kolcaba’s Comfort Theory. Epilepsy Behav. 2017;68:208–215. doi: 10.1016/j.yebeh.2016.11.005. PubMed DOI

Egger-Rainer A., Hettegger S.M., Feldner R., Arnold S., Bosselmann C., Hamer H., Hengsberger A., Lang J., Lorenzl S., Lerche H., et al. Do all patients in the epilepsy monitoring unit experience the same level of comfort? A quantitative exploratory secondary analysis. J. Adv. Nurs. 2022;78:2004–2014. doi: 10.1111/jan.15105. PubMed DOI PMC

Hautzinger M., Keller F., Kühner C., Beck A.T. Beck Depressions-Inventar. Harcourt Test Services; Frankfurt am Main, Germany: 2006.

Griefahn B., Künemund C., Bröde P., Mehnert P. Zur Validität der deutschen Übersetzung des Morningness-Eveningness-Questionnaires von Horne und Östberg. Somnologie. 2001;5:71–76. doi: 10.1046/j.1439-054X.2001.01149.x. DOI

Höller Y., Eyjólfsdóttir S., van Schalkwijk F.J., Trinka E. The effects of slow wave sleep characteristics on semantic, episodic, and procedural memory in people with epilepsy. Front. Pharmacol. 2024;15:1374760. doi: 10.5281/zenodo.10956609. PubMed DOI PMC

van Schalkwijk F.J., Gruber W.R., Miller L.A., Trinka E., Höller Y. Investigating the Effects of Seizures on Procedural Memory Performance in Patients with Epilepsy. Brain Sci. 2021;11:261. doi: 10.3390/brainsci11020261. PubMed DOI PMC

Jacobs A.M., Võ M.L., Briesemeister B.B., Conrad M., Hofmann M.J., Kuchinke L., Lüdtke J., Braun M. 10 years of BAWLing into affective and aesthetic processes in reading: What are the echoes? Front. Psychol. 2015;6:714. doi: 10.3389/fpsyg.2015.00714. PubMed DOI PMC

Võ M.L.H., Conrad M., Kuchinke L., Urton K., Hofmann M.J., Jacobs A.M. The Berlin Affective Word List Reloaded (BAWL-R) Behav. Res. Methods. 2009;41:534–538. doi: 10.3758/BRM.41.2.534. PubMed DOI

Höller Y., Höhn C., Schwimmbeck F., Plancher G., Trinka E. Effects of Antiepileptic Drug Tapering on Episodic Memory as Measured by Virtual Reality Tests. Front. Neurol. 2020;11:93. doi: 10.3389/fneur.2020.00093. PubMed DOI PMC

Höller Y., Höhn C., Schwimmbeck F., Plancher G., Trinka E. A virtual reality paradigm to assess episodic memory: Validation-dataset for six parallel versions and a structured behavioral assessment. Data Brief. 2020;29:105279. doi: 10.1016/j.dib.2020.105279. PubMed DOI PMC

Perucca E., French J.A., Aljandeel G., Balestrini S., Braga P., Burneo J.G., Felli A., Cross J.H., Galanopoulou A.S., Jain S., et al. Which terms should be used to describe medications used in the treatment of seizure disorders? An ILAE position paper. Epilepsia. 2024;65:533–541. doi: 10.1111/epi.17877. PubMed DOI PMC

Mayeli A., Janssen S.A., Sharma K., Ferrarelli F. Examining First Night Effect on Sleep Parameters with hd-EEG in Healthy Individuals. Brain Sci. 2022;12:233. doi: 10.3390/brainsci12020233. PubMed DOI PMC

Beniczky S., Neufeld M., Diehl B., Dobesberger J., Trinka E., Mameniskiene R., Rheims S., Gil-Nagel A., Craiu D., Pressler R., et al. Testing patients during seizures: A European consensus procedure developed by a joint taskforce of the ILAE—Commission on European Affairs and the European Epilepsy Monitoring Unit Association. Epilepsia. 2016;57:1363–1368. doi: 10.1111/epi.13472. PubMed DOI

Schulz H. Rethinking Sleep Analysis. J. Clin. Sleep Med. 2008;4:99–103. doi: 10.5664/jcsm.27124. PubMed DOI PMC

Hori T., Sugita Y., Koga E., Shirakawa S., Inoue K., Uchida S., Kuwahara H., Kousaka M., Kobayashi T., Tsuji Y., et al. 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;55:305–310. doi: 10.1046/j.1440-1819.2001.00810.x. PubMed DOI

R Core Team R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. 2022. [(accessed on 1 May 2024)]. Available online: https://www.r-project.org/

Bonnet M.H. Sleep Restoration as a Function of Periodic Awakening, Movement, or Electroencephalographic Change. Sleep. 1987;10:364–373. doi: 10.1093/sleep/10.4.364. PubMed DOI

Huijben I.A.M., van Sloun R.J.G., Hoondert B., Dujardin S., Pijpers A., Overeem S., van Gilst M.M. Temporal dynamics of awakenings from slow-wave sleep in non-rapid eye movement parasomnia. J. Sleep Res. 2023:e14096. doi: 10.1111/jsr.14096. PubMed DOI

Gonzalez C., Jiang X., Gonzalez-Martinez J., Halgren E. Human Spindle Variability. J. Neurosci. 2022;42:4517–4537. doi: 10.1523/JNEUROSCI.1786-21.2022. PubMed DOI PMC

Knoblauch V., Kräuchi K., Renz C., Wirz-Justice A., Cajochen C. Homeostatic Control of Slow-wave and Spindle Frequency Activity during Human Sleep: Effect of Differential Sleep Pressure and Brain Topography. Cerebral Cortex. 2002;12:1092–1100. doi: 10.1093/cercor/12.10.1092. PubMed DOI

Irfan M., Schenck C.H., Howell M.J. NonREM Disorders of Arousal and Related Parasomnias: An Updated Review. Neurotherapeutics. 2021;18:124–139. doi: 10.1007/s13311-021-01011-y. PubMed DOI PMC

Sohi M., Jain L., Ang-Rabanes M., Mogallapu R. Sertraline-Induced Sleep Paralysis: A Case Report. Curēus. 2023;15:e49014. doi: 10.7759/cureus.49014. PubMed DOI PMC

Rush A.J., Armitage R., Gillin J.C., Yonkers K.A., Winokur A., Moldofsky H., Vogel G.W., Kaplita S.B., Fleming J.B., Montplaisir J., et al. Comparative effects of nefazodone and fluoxetine on sleep in outpatients with major depressive disorder. Biol. Psychiatry. 1998;44:3–14. doi: 10.1016/S0006-3223(98)00092-4. PubMed DOI

Jindal R.D., Friedman E.S., Berman S.R., Fasiczka A.L., Howland R.H., Thase M.E. Effects of Sertraline on Sleep Architecture in Patients With Depression. J. Clin. Psychopharmacol. 2003;23:540–548. doi: 10.1097/01.jcp.0000095345.32154.9a. PubMed DOI

van der Veen S., Caviness J.N., Dreissen Y.E.M., Ganos C., Ibrahim A., Koelman J.H.T.M., Stefani A., Tijssen M.A.J. Myoclonus and other jerky movement disorders. Clin. Neurophysiol. Pract. 2022;7:285–316. doi: 10.1016/j.cnp.2022.09.003. PubMed DOI PMC

Werth E., Dijk D., Achermann P., Borbely A.A. Dynamics of the sleep EEG after an early evening nap: Experimental data and simulations. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1996;40:R501–R510. doi: 10.1152/ajpregu.1996.271.3.R501. PubMed DOI

Nguyen-Michel V., Herlin B., Gales A., Vaz S., Levy P., Dupont S., Adam C., Navarro V., Frazzini V. Sleep scoring based on video-electroencephalography monitoring in an Epileptology Unit: Comparison with polysomnography. J. Sleep Res. 2021;30:e13332. doi: 10.1111/jsr.13332. PubMed DOI

Kobulashvili T., Höfler J., Dobesberger J., Ernst F., Ryvlin P., Cross J.H., Braun K., Dimova P., Francione S., Hecimovic H., et al. Current practices in long-term video-EEG monitoring services: A survey among partners of the E-PILEPSY pilot network of reference for refractory epilepsy and epilepsy surgery. Seizure. 2016;38:38–45. doi: 10.1016/j.seizure.2016.03.009. PubMed DOI