The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug-Resistant Epilepsy.
Journal
Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449
Informations de publication
Date de publication:
15 Sep 2023
15 Sep 2023
Historique:
revised:
14
07
2023
received:
21
04
2023
accepted:
11
09
2023
pubmed:
15
9
2023
medline:
15
9
2023
entrez:
15
9
2023
Statut:
aheadofprint
Résumé
Sleep has important influences on focal interictal epileptiform discharges (IEDs), and the rates and spatial extent of IEDs are increased in non-rapid eye movement (NREM) sleep. In contrast, the influence of sleep on seizures is less clear, and its effects on seizure topography are poorly documented. We evaluated the influences of NREM sleep on ictal spatiotemporal dynamics and contrasted these with interictal network dynamics. We included patients with drug-resistant focal epilepsy who underwent continuous intracranial electroencephalography (iEEG) with depth electrodes. Patients were selected if they had 1 to 3 seizures from each vigilance state, wakefulness and NREM sleep, within a 48-hour window, and under the same antiseizure medication. A 10-minute epoch of the interictal iEEG was selected per state, and IEDs were detected automatically. A total of 25 patients (13 women; aged 32.5 ± 7.1 years) were included. The seizure onset pattern, duration, spatiotemporal propagation, and latency of ictal high-frequency activity did not differ significantly between wakefulness and NREM sleep (all p > 0.05). In contrast, IED rates and spatial distribution were increased in NREM compared with wakefulness (p < 0.001, Cliff's d = 0.48 and 0.49). The spatial overlap between vigilance states was higher for seizures (57.1 ± 40.1%) than IEDs (41.7 ± 46.2%; p = 0.001, Cliff's d = 0.51). In contrast to its effects on IEDs, NREM sleep does not affect ictal spatiotemporal dynamics. This suggests that once the brain surpasses the seizure threshold, it will follow the underlying epileptic network irrespective of the vigilance state. These findings offer valuable insights into neural network dynamics in epilepsy and have important clinical implications for localizing seizure foci. ANN NEUROL 2023.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : CIHR
ID : PJT-175056
Pays : Canada
Organisme : CIHR
ID : PJT-175056
Pays : Canada
Informations de copyright
© 2023 The Authors. Annals of Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.
Références
Chen Z, Brodie MJ, Liew D, Kwan P. Treatment outcomes in patients with newly diagnosed epilepsy treated with established and new antiepileptic drugs: a 30-year longitudinal cohort study. JAMA Neurol. 2018;75:279-286. https://doi.org/10.1001/jamaneurol.2017.3949.
Fiest KM, Sauro KM, Wiebe S, et al. Prevalence and incidence of epilepsy: a systematic review and meta-analysis of international studies. Neurology 2017;88:296-303. https://doi.org/10.1212/wnl.0000000000003509.
de Tisi J, Bell GS, Peacock JL, et al. The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet 2011;378:1388-1395. https://doi.org/10.1016/s0140-6736(11)60890-8.
Nowell M, Miserocchi A, McEvoy AW, Duncan JS. Advances in epilepsy surgery. J Neurol Neurosurg Psychiatry 2014;85:1273-1279. https://doi.org/10.1136/jnnp-2013-307069.
Frauscher B, von Ellenrieder N, Ferrari-Marinho T, et al. Facilitation of epileptic activity during sleep is mediated by high amplitude slow waves. Brain 2015;138:1629-1641. https://doi.org/10.1093/brain/awv073.
von Ellenrieder N, Frauscher B, Dubeau F, Gotman J. Interaction with slow waves during sleep improves discrimination of physiologic and pathologic high-frequency oscillations (80-500 Hz). Epilepsia 2016;57:869-878. https://doi.org/10.1111/epi.13380.
Nonoda Y, Miyakoshi M, Ojeda A, et al. Interictal high-frequency oscillations generated by seizure onset and eloquent areas may be differentially coupled with different slow waves. Clin Neurophysiol 2016;127:2489-2499. https://doi.org/10.1016/j.clinph.2016.03.022.
Frauscher B, von Ellenrieder N, Dubeau F, Gotman J. EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans. Epilepsia 2016;57:879-888. https://doi.org/10.1111/epi.13389.
Campana C, Zubler F, Gibbs S, et al. Suppression of interictal spikes during phasic rapid eye movement sleep: a quantitative stereo-electroencephalography study. J Sleep Res 2017;26:606-613. https://doi.org/10.1111/jsr.12533.
Motoi H, Miyakoshi M, Abel TJ, et al. Phase-amplitude coupling between interictal high-frequency activity and slow waves in epilepsy surgery. Epilepsia 2018;59:1954-1965. https://doi.org/10.1111/epi.14544.
Nobili L, Frauscher B, Eriksson S, et al. Sleep and epilepsy: a snapshot of knowledge and future research lines. J Sleep Res 2022;31:e13622. https://doi.org/10.1111/jsr.13622.
Grigg-Damberger M, Foldvary-Schaefer N. Bidirectional relationships of sleep and epilepsy in adults with epilepsy. Epilepsy Behav 2021;116:107735. https://doi.org/10.1016/j.yebeh.2020.107735.
Buzsáki G, Draguhn A. Neuronal oscillations in cortical networks. Science 2004;304:1926-1929. https://doi.org/10.1126/science.1099745.
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.
Sammaritano M, Gigli GL, Gotman J. Interictal spiking during wakefulness and sleep and the localization of foci in temporal lobe epilepsy. Neurology 1991;41:290-297. https://doi.org/10.1212/wnl.41.2_part_1.290.
Lambert I, Roehri N, Giusiano B, et al. Brain regions and epileptogenicity influence epileptic interictal spike production and propagation during NREM sleep in comparison with wakefulness. Epilepsia 2018;59:235-243. https://doi.org/10.1111/epi.13958.
Bazil CW, Walczak TS. Effects of sleep and sleep stage on epileptic and nonepileptic seizures. Epilepsia 1997;38:56-62. https://doi.org/10.1111/j.1528-1157.1997.tb01077.x.
Jobst BC, Williamson PD, Neuschwander TB, et al. Secondarily generalized seizures in mesial temporal epilepsy: clinical characteristics, lateralizing signs, and association with sleep-wake cycle. Epilepsia 2001;42:1279-1287. https://doi.org/10.1046/j.1528-1157.2001.09701.x.
Herman ST, Walczak TS, Bazil CW. Distribution of partial seizures during the sleep-wake cycle: differences by seizure onset site. Neurology 2001;56:1453-1459. https://doi.org/10.1212/wnl.56.11.1453.
Karoly PJ, Freestone DR, Boston R, et al. Interictal spikes and epileptic seizures: their relationship and underlying rhythmicity. Brain 2016;139:1066-1078. https://doi.org/10.1093/brain/aww019.
Galovic M, Ferreira-Atuesta C, Abraira L, et al. Seizures and epilepsy after stroke: epidemiology, biomarkers and management. Drugs Aging 2021;38:285-299. https://doi.org/10.1007/s40266-021-00837-7.
Pandis D, Scarmeas N. Seizures in Alzheimer disease: clinical and epidemiological data. Epilepsy Curr 2012;12:184-187. https://doi.org/10.5698/1535-7511-12.5.184.
Ives JR. New chronic EEG electrode for critical/intensive care unit monitoring. J Clin Neurophysiol 2005;22:119-123. https://doi.org/10.1097/01.wnp.0000152659.30753.47.
Berry R, Quan S, Abreu A, et al. The AASM manual for the scoring of sleep and associated events, version 2.6. Darien, IL: American Academy of Sleep Medicine, 2020.
Zweiphenning W, von Ellenrieder N, Dubeau F, et al. Correcting for physiological ripples improves epileptic focus identification and outcome prediction. Epilepsia 2022;63:483-496. https://doi.org/10.1111/epi.17145.
Spanedda F, Cendes F, Gotman J. Relations between EEG seizure morphology, interhemispheric spread, and mesial temporal atrophy in bitemporal epilepsy. Epilepsia 1997;38:1300-1314. https://doi.org/10.1111/j.1528-1157.1997.tb00068.x.
Perucca P, Dubeau F, Gotman J. Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology. Brain 2014;137:183-196. https://doi.org/10.1093/brain/awt299.
Bartolomei F, Chauvel P, Wendling F. Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain 2008;131:1818-1830. https://doi.org/10.1093/brain/awn111.
Colombet B, Woodman M, Badier JM, Bénar CG. AnyWave: a cross-platform and modular software for visualizing and processing electrophysiological signals. J Neurosci Methods 2015;242:118-126. https://doi.org/10.1016/j.jneumeth.2015.01.017.
Frauscher B, von Ellenrieder N, Zelmann R, et al. Atlas of the normal intracranial electroencephalogram: neurophysiological awake activity in different cortical areas. Brain 2018;141:1130-1144. https://doi.org/10.1093/brain/awy035.
Janca R, Jezdik P, Cmejla R, et al. Detection of interictal epileptiform discharges using signal envelope distribution modelling: application to epileptic and non-epileptic intracranial recordings. Brain Topogr 2015;28:172-183. https://doi.org/10.1007/s10548-014-0379-1.
Klimes P, Cimbalnik J, Brazdil M, et al. NREM sleep is the state of vigilance that best identifies the epileptogenic zone in the interictal electroencephalogram. Epilepsia 2019;60:2404-2415. https://doi.org/10.1111/epi.16377.
Azeem A, von Ellenrieder N, Hall J, et al. Interictal spike networks predict surgical outcome in patients with drug-resistant focal epilepsy. Ann Clin Transl Neurol 2021;8:1212-1223. https://doi.org/10.1002/acn3.51337.
Klimes P, Peter-Derex L, Hall J, et al. Spatio-temporal spike dynamics predict surgical outcome in adult focal epilepsy. Clin Neurophysiol 2022;134:88-99. https://doi.org/10.1016/j.clinph.2021.10.023.
Balatskaya A, Roehri N, Lagarde S, et al. The “connectivity Epileptogenicity index” (cEI), a method for mapping the different seizure onset patterns in StereoElectroEncephalography recorded seizures. Clin Neurophysiol 2020;131:1947-1955. https://doi.org/10.1016/j.clinph.2020.05.029.
Steriade M. Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci 2005;28:317-324. https://doi.org/10.1016/j.tins.2005.03.007.
Tseng HT, Hsiao YT, Yi PL, Chang FC. Deep brain stimulation increases seizure threshold by altering REM sleep and Delta powers during NREM sleep. Front Neurol 2020;11:752. https://doi.org/10.3389/fneur.2020.00752.
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.
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.
Peter-Derex L, Klimes P, Latreille V, et al. Sleep disruption in epilepsy: ictal and Interictal epileptic activity matter. Ann Neurol 2020;88:907-920. https://doi.org/10.1002/ana.25884.
Bernard C. Circadian/multidien molecular oscillations and rhythmicity of epilepsy (MORE). Epilepsia 2021;62:S49-s68. https://doi.org/10.1111/epi.16716.
Bernard C, Frauscher B, Gelinas J, Timofeev I. Sleep, oscillations, and epilepsy. Epilepsia 2023. https://doi.org/10.1111/epi.17664.
Kumar J, Solaiman A, Mahakkanukrauh P, et al. Sleep related epilepsy and pharmacotherapy: an insight. Front Pharmacol 2018;9:1088. https://doi.org/10.3389/fphar.2018.01088.
Vlachos I, Krishnan B, Treiman DM, et al. The concept of effective inflow: application to Interictal localization of the epileptogenic focus from iEEG. IEEE Trans Biomed Eng 2017;64:2241-2252. https://doi.org/10.1109/tbme.2016.2633200.
Gupta K, Grover P, Abel TJ. Current conceptual understanding of the epileptogenic network from Stereoelectroencephalography-based connectivity inferences. Front Neurol 2020;11:569699. https://doi.org/10.3389/fneur.2020.569699.
van Mierlo P, Carrette E, Hallez H, et al. Ictal-onset localization through connectivity analysis of intracranial EEG signals in patients with refractory epilepsy. Epilepsia 2013;54:1409-1418. https://doi.org/10.1111/epi.12206.
Wilke C, Worrell G, He B. Graph analysis of epileptogenic networks in human partial epilepsy. Epilepsia 2011;52:84-93. https://doi.org/10.1111/j.1528-1167.2010.02785.x.
de Curtis M, Avoli M. Initiation, propagation, and termination of partial (focal) seizures. Cold Spring Harb Perspect Med 2015;5:a022368. https://doi.org/10.1101/cshperspect.a022368.
O'Hara NB, Lee MH, Juhász C, et al. Diffusion tractography predicts propagated high-frequency activity during epileptic spasms. Epilepsia 2022;63:1787-1798. https://doi.org/10.1111/epi.17251.
Avoli M, D'Antuono M, Louvel J, et al. Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog Neurobiol 2002;68:167-207. https://doi.org/10.1016/s0301-0082(02)00077-1.
de Curtis M, Avanzini G. Interictal spikes in focal epileptogenesis. Prog Neurobiol 2001;63:541-567. https://doi.org/10.1016/s0301-0082(00)00026-5.
Jensen MS, Yaari Y. The relationship between interictal and ictal paroxysms in an in vitro model of focal hippocampal epilepsy. Ann Neurol 1988;24:591-598. https://doi.org/10.1002/ana.410240502.
Engel J Jr, Ackermann RF. Interictal EEG spikes correlate with decreased, rather than increased, epileptogenicity in amygdaloid kindled rats. Brain Res 1980;190:543-548. https://doi.org/10.1016/0006-8993(80)90296-6.
Gotman J, Marciani MG. Electroencephalographic spiking activity, drug levels, and seizure occurrence in epileptic patients. Ann Neurol 1985;17:597-603. https://doi.org/10.1002/ana.410170612.
Librizzi L, de Curtis M. Epileptiform ictal discharges are prevented by periodic interictal spiking in the olfactory cortex. Ann Neurol 2003;53:382-389. https://doi.org/10.1002/ana.10471.
Derry CP. Sleeping in fits and starts: a practical guide to distinguishing nocturnal epilepsy from sleep disorders. Pract Neurol 2014;14:391-398. https://doi.org/10.1136/practneurol-2014-000890.
Kaiboriboon K, Lüders HO, Hamaneh M, et al. EEG source imaging in epilepsy-practicalities and pitfalls. Nat Rev Neurol 2012;8:498-507. https://doi.org/10.1038/nrneurol.2012.150.
von Ellenrieder N, Peter-Derex L, Gotman J, Frauscher B. SleepSEEG: automatic sleep scoring using intracranial EEG recordings only. J Neural Eng 2022;19:026057. https://doi.org/10.1088/1741-2552/ac6829.