Rapid eye movement sleep affects interictal epileptic activity differently in mesiotemporal and neocortical areas.
epilepsy
interictal activity
rapid eye movement
sleep
stereo-electroencephalography
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
revised:
22
08
2023
received:
25
04
2023
accepted:
22
08
2023
medline:
7
11
2023
pubmed:
16
9
2023
entrez:
15
9
2023
Statut:
ppublish
Résumé
Rapid eye movement (REM) sleep reduces the rate and extent of interictal epileptiform discharges (IEDs). Breakthrough epileptic activity during REM sleep is therefore thought to best localize the seizure onset zone (SOZ). We utilized polysomnography combined with direct cortical recordings to investigate the influences of anatomical locations and the time of night on the suppressive effect of REM sleep on IEDs. Forty consecutive patients with drug-resistant focal epilepsy underwent combined polysomnography and stereo-electroencephalography during presurgical evaluation. Ten-minute interictal epochs were selected 2 h prior to sleep onset (wakefulness), and from the first and second half of the night during non-REM (NREM) sleep and REM sleep. IEDs were detected automatically across all channels. Anatomic localization, time of night, and channel type (within or outside the SOZ) were tested as modulating factors. Relative to wakefulness, there was a suppression of IEDs by REM sleep in neocortical regions (median = -27.6%), whereas mesiotemporal regions showed an increase in IEDs (19.1%, p = .01, d = .39). This effect was reversed when comparing the regional suppression of IEDs by REM sleep relative to NREM sleep (-35.1% in neocortical, -58.7% in mesiotemporal, p < .001, d = .39). Across all patients, no clinically relevant novel IED regions were observed in REM sleep versus NREM or wakefulness based on our predetermined thresholds (4 IEDs/min in REM, 0 IEDs/min in NREM and wakefulness). Finally, there was a reduction in IEDs in late (NREM: 1.08/min, REM: .61/min) compared to early sleep (NREM: 1.22/min, REM: .69/min) for both NREM (p < .001, d = .21) and REM (p = .04, d = .14). Our results demonstrate a spatiotemporal effect of IED suppression by REM sleep relative to wakefulness in neocortical but not mesiotemporal regions, and in late versus early sleep. This suggests the importance of considering sleep stage interactions and the potential influences of anatomical locations when using IEDs to define the epileptic focus.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3036-3048Subventions
Organisme : CIHR
ID : PJT-175056
Pays : Canada
Informations de copyright
© 2023 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.
Références
Gibbs EL, Gibbs FA. Diagnostic and localizing value of electroencephalographic studies in sleep | CiNii research. 1947 Accessed May 3, 2022. https://cir.nii.ac.jp/crid/1572261550119419904
Engel J Jr, Rausch R, Lieb JP, Kuhl DE, Crandall PH. Correlation of criteria used for localizing epileptic foci in patients considered for surgical therapy of epilepsy. Ann Neurol. 1981;9(3):215-224. https://doi.org/10.1002/ana.410090303
Aserinsky E, Kleitman N. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science. 1953;118(3062):273-274. https://doi.org/10.1126/science.118.3062.273
Ng M, Pavlova M. Why are seizures rare in rapid eye movement sleep? Review of the frequency of seizures in different sleep stages. Epilepsy Res Treat. 2013;2013:932790. https://doi.org/10.1155/2013/932790
Frauscher B, von Ellenrieder N, Dubeau F, Gotman J. EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans. Epilepsia. 2016;57(6):879-888. https://doi.org/10.1111/epi.13389
Giacomini T, Luria G, D'Amario V, et al. On the role of REM sleep microstructure in suppressing interictal spikes in electrical status epilepticus during sleep. Clin Neurophysiol. 2022;136:62-68. https://doi.org/10.1016/j.clinph.2022.01.008
Frauscher B, Gotman J. Sleep, oscillations, interictal discharges, and seizures in human focal epilepsy. Neurobiol Dis. 2019;127:545-553. https://doi.org/10.1016/j.nbd.2019.04.007
McLeod GA, Ghassemi A, Ng MC. Can REM sleep localize the epileptogenic zone? A systematic review and analysis. Front Neurol. 2020;11:584. https://doi.org/10.3389/fneur.2020.00584
Shouse MN, Siegel JM, Wu MF, Szymusiak R, Morrison AR. Mechanisms of seizure suppression during rapid-eye-movement (REM) sleep in cats. Brain Res. 1989;505(2):271-282. https://doi.org/10.1016/0006-8993(89)91453-4
Shouse MN, Farber PR, Staba RJ. Physiological basis: how NREM sleep components can promote and REM sleep components can suppress seizure discharge propagation. Clin Neurophysiol off J Int Fed Clin Neurophysiol. 2000;111:S9-S18. https://doi.org/10.1016/s1388-2457(00)00397-7
Steriade M, Contreras D, Curró Dossi R, Nuñez A. The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci off J Soc Neurosci. 1993;13(8):3284-3299.
Frauscher B, von Ellenrieder N, Ferrari-Marinho T, Avoli M, Dubeau F, Gotman J. Facilitation of epileptic activity during sleep is mediated by high amplitude slow waves. Brain. 2015;138(6):1629-1641. https://doi.org/10.1093/brain/awv073
Lambert I, Roehri N, Giusiano B, Carron R, Wendling F, Benar C, et al. Brain regions and epileptogenicity influence epileptic interictal spike production and propagation during NREM sleep in comparison with wakefulness. Epilepsia. 2018;59(1):235-243. https://doi.org/10.1111/epi.13958
Fouad A, Azizollahi H, Le Douget JE, et al. Interictal epileptiform discharges show distinct spatiotemporal and morphological patterns across wake and sleep. Brain Commun. 2022;4(5):fcac183. https://doi.org/10.1093/braincomms/fcac183
Genton P, Maton B, Ogihara M, Samoggia G, Guerrini R, Medina MT, et al. Continuous focal spikes during REM sleep in a case of acquired aphasia (Landau-Kleffner syndrome). Sleep. 1992;15(5):454-460. https://doi.org/10.1093/sleep/15.5.454
Watanabe Y, Ogihara M, Hoshika A. Cluster of epileptic spasms preceded by focal seizures observed in localization-related epilepsy. Brain Dev. 2007;29(9):571-576. https://doi.org/10.1016/j.braindev.2007.03.006
Kang X, Boly M, Findlay G, Jones B, Gjini K, Maganti R, et al. Quantitative spatio-temporal characterization of epileptic spikes using high density EEG: differences between NREM sleep and REM sleep. Sci Rep. 2020;10(1):1673. https://doi.org/10.1038/s41598-020-58612-4
McLeod GA, Abbasian P, Toutant D, et al. Sleep-wake states change the interictal localization of candidate epileptic source generators. Sleep. 2022;45:zsac062. https://doi.org/10.1093/sleep/zsac062
Krucoff MO, Chan AY, Harward SC, Rahimpour S, Rolston JD, Muh C, et al. Rates and predictors of success and failure in repeat epilepsy surgery: a meta-analysis and systematic review. Epilepsia. 2017;58(12):2133-2142. https://doi.org/10.1111/epi.13920
Malow BA, Aldrich MS. Localizing value of rapid eye movement sleep in temporal lobe epilepsy. Sleep Med. 2000;1(1):57-60. https://doi.org/10.1016/s1389-9457(99)00008-8
Nobili L, Sartori I, Terzaghi M, Stefano F, Mai R, Tassi L, et al. Relationship of epileptic discharges to arousal instability and periodic leg movements in a case of nocturnal frontal lobe epilepsy: a stereo-EEG study. Sleep. 2006;29(5):701-704. https://doi.org/10.1093/sleep/29.5.701
Ball T, Kern M, Mutschler I, Aertsen A, Schulze-Bonhage A. Signal quality of simultaneously recorded invasive and non-invasive EEG. Neuroimage. 2009;46(3):708-716. https://doi.org/10.1016/j.neuroimage.2009.02.028
Parvizi J, Kastner S. Promises and limitations of human intracranial electroencephalography. Nat Neurosci. 2018;21(4):474-483. https://doi.org/10.1038/s41593-018-0108-2
Peter-Derex L, Klimes P, Latreille V, Bouhadoun S, Dubeau F, Frauscher B. Sleep disruption in epilepsy: ictal and Interictal epileptic activity matter. Ann Neurol. 2020;88(5):907-920. https://doi.org/10.1002/ana.25884
Szymusiak R, McGinty D, David Fairchild M, Jenden DJ. Sleep-wake disturbances in an animal model of chronic cholinergic insufficiency. Brain Res. 1993;629(1):141-145. https://doi.org/10.1016/0006-8993(93)90492-6
Platt B, Riedel G. The cholinergic system, EEG and sleep. Behav Brain Res. 2011;221(2):499-504. https://doi.org/10.1016/j.bbr.2011.01.017
Simor P, Szalárdy O, Gombos F, Ujma PP, Jordán Z, Halász L, et al. REM sleep microstates in the human anterior thalamus. J Neurosci. 2021;41(26):5677-5686. https://doi.org/10.1523/JNEUROSCI.1899-20.2021
McKenzie MB, Jones ML, O'Carroll A, Serletis D, Shafer LA, Ng MC. Breakthrough spikes in rapid eye movement sleep from the epilepsy monitoring unit are associated with peak seizure frequency. Sleep. 2020;43(5):zsz281. https://doi.org/10.1093/sleep/zsz281
Frauscher B, von Ellenrieder N, Dubeau F, Gotman J. Scalp spindles are associated with widespread intracranial activity with unexpectedly low synchrony. Neuroimage. 2015;105:1-12. https://doi.org/10.1016/j.neuroimage.2014.10.048
Ives JR. New chronic EEG electrode for critical/intensive care unit monitoring. J Clin Neurophysiol. 2005;22(2):119-123. https://doi.org/10.1097/01.wnp.0000152659.30753.47
Drouin S, Kochanowska A, Kersten-Oertel M, Gerard IJ, Zelmann R, de Nigris D, et al. IBIS: an OR ready open-source platform for image-guided neurosurgery. Int J Comput Assist Radiol Surg. 2017;12(3):363-378. https://doi.org/10.1007/s11548-016-1478-0
Cuello Oderiz C, von Ellenrieder N, Dubeau F, Eisenberg A, Gotman J, Hall J, et al. Association of Cortical Stimulation-Induced Seizure with Surgical Outcome in patients with focal drug-resistant epilepsy. JAMA Neurol. 2019;76(9):1070-1078. https://doi.org/10.1001/jamaneurol.2019.1464
Frauscher B, von Ellenrieder N, Zelmann R, Doležalová I, Minotti L, Olivier A, et al. Atlas of the normal intracranial electroencephalogram: neurophysiological awake activity in different cortical areas. Brain J Neurol. 2018;141(4):1130-1144. https://doi.org/10.1093/brain/awy035
Frauscher B, von Ellenrieder N, Zelmann R, Rogers C, Nguyen DK, Kahane P, et al. High-frequency oscillations in the Normal human brain. Ann Neurol. 2018;84(3):374-385. https://doi.org/10.1002/ana.25304
Landman B, Warfield S. MICCAI 2012 workshop on multi-atlas labeling. Medical image computing and computer assisted intervention conference. Nice, France: CreateSpace Independent Publishing Platform; 2012.
Spanedda F, Cendes F, Gotman J. Relations between EEG seizure morphology, interhemispheric spread, and mesial temporal atrophy in Bitemporal epilepsy. Epilepsia. 1997;38(12):1300-1314. https://doi.org/10.1111/j.1528-1157.1997.tb00068.x
Berry RB, Brooks R, Gamaldo C, Harding SM, Lloyd RM, Quan SF, et al. AASM scoring manual updates for 2017 (version 2.4). J Clin Sleep Med. 2017;13(5):665-666. https://doi.org/10.5664/jcsm.6576
Aserinsky E. Relationship of rapid eye movement density to the prior accumulation of sleep and wakefulness. Psychophysiology. 1973;10(6):545-558. https://doi.org/10.1111/j.1469-8986.1973.tb00804.x
Janca R, Jezdik P, Cmejla R, Tomasek M, Worrell GA, Stead M, et al. Detection of interictal epileptiform discharges using signal envelope distribution modelling: application to epileptic and non-epileptic intracranial recordings. Brain Topogr. 2015;28(1):172-183. https://doi.org/10.1007/s10548-014-0379-1
Jing J, Herlopian A, Karakis I, Ng M, Halford JJ, Lam A, et al. Interrater reliability of experts in identifying Interictal Epileptiform discharges in electroencephalograms. JAMA Neurol. 2020;77(1):49-57. https://doi.org/10.1001/jamaneurol.2019.3531
Tanaka N, Hämäläinen MS, Ahlfors SP, Liu H, Madsen JR, Bourgeois BF, et al. Propagation of epileptic spikes reconstructed from spatiotemporal magnetoencephalographic and electroencephalographic source analysis. Neuroimage. 2010;50(1):217-222. https://doi.org/10.1016/j.neuroimage.2009.12.033
Jones EG. Principles of thalamic organization. In: Jones EG, editor. The thalamus. Boston: Springer Science & Business Media; 2012. p. 85-149.
Menezes Cordeiro I, von Ellenrieder N, Zazubovits N, Dubeau F, Gotman J, Frauscher B. Sleep influences the intracerebral EEG pattern of focal cortical dysplasia. Epilepsy Res. 2015;113:132-139. https://doi.org/10.1016/j.eplepsyres.2015.03.014
Islam MK, Rastegarnia A, Yang Z. Methods for artifact detection and removal from scalp EEG: a review. Neurophysiol Clin Neurophysiol. 2016;46(4):287-305. https://doi.org/10.1016/j.neucli.2016.07.002
Schiller K, Avigdor T, Abdallah C, Sziklas V, Crane J, Stefani A, et al. Focal epilepsy disrupts spindle structure and function. Sci Rep. 2022;12(1):11137. https://doi.org/10.1038/s41598-022-15147-0
Dijk DJ. Regulation and functional correlates of slow wave sleep. J Clin Sleep Med. 2009;5(2 Suppl):S6-S15.
Dijk DJ. EEG slow waves and sleep spindles: windows on the sleeping brain. Behav Brain Res. 1995;69(1):109-116. https://doi.org/10.1016/0166-4328(95)00007-G
Campana C, Zubler F, Gibbs S, de Carli F, Proserpio P, Rubino A, et al. Suppression of interictal spikes during phasic rapid eye movement sleep: a quantitative stereo-electroencephalography study. J Sleep Res. 2017;26(5):606-613. https://doi.org/10.1111/jsr.12533
von Ellenrieder N, Dubeau F, Gotman J, Frauscher B. Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties. NeuroImage Clin. 2017;14:566-573. https://doi.org/10.1016/j.nicl.2017.02.018