OBJECTIVE: Disturbed sleep is common in epilepsy. The direct influence of nocturnal epileptic activity on sleep fragmentation remains poorly understood. Stereo-electroencephalography paired with polysomnography is the ideal tool to study this relationship. We investigated whether sleep-related epileptic activity is associated with sleep disruption. METHODS: We visually marked sleep stages, arousals, seizures, and epileptic bursts in 36 patients with focal drug-resistant epilepsy who underwent combined stereo-electroencephalography/polysomnography during presurgical evaluation. Epileptic spikes were detected automatically. Spike and burst indices (n/sec/channel) were computed across four 3-second time windows (baseline sleep, pre-arousal, arousal, and post-arousal). Sleep stage and anatomic localization were tested as modulating factors. We assessed the intra-arousal dynamics of spikes and their relationship with the slow wave component of non-rapid eye-movement sleep (NR) arousals. RESULTS: The vast majority of sleep-related seizures (82.4%; 76.5% asymptomatic) were followed by awakenings or arousals. The epileptic burst index increased significantly before arousals as compared to baseline and postarousal, irrespective of sleep stage or brain area. A similar pre-arousal increase was observed for the spike index in NR stage 2 and rapid eye-movement sleep. In addition, the spike index increased during the arousal itself in neocortical channels, and was strongly correlated with the slow wave component of NR arousals (r = 0.99, p < 0.0001). INTERPRETATION: Sleep fragmentation in focal drug-resistant epilepsy is associated with ictal and interictal epileptic activity. The increase in interictal epileptic activity before arousals suggests its participation in sleep disruption. An additional increase in the spike rate during arousals may result from a sleep-wake boundary instability, suggesting a bidirectional relationship. ANN NEUROL 2020;88:907-920.

Analytical Neurophysiology Lab Montreal Neurological Institute and Hospital McGill University Montreal QC Canada

Center for Sleep Medicine and Respiratory Diseases Lyon University Hospital Lyon 1 University Lyon France

Institute of Scientific Instruments The Czech Academy of Sciences Brno Czech Republic

Lyon Neuroscience Research Center CNRS UMR5292 INSERM U1028 Lyon France

Montreal Neurological Institute and Hospital McGill University Montreal QC Canada

Komentář v

Epilepsy Curr. 2020 Nov 19;21(1):19-20. doi: 10.1177/1535759720973269. PubMed

Zobrazit více v PubMed

Latreille V, St Louis EK, Pavlova M. Co-morbid sleep disorders and epilepsy: a narrative review and case examples. Epilepsy Res 2018;145:185-197.

Khan S, Nobili L, Khatami R, et al. Circadian rhythm and epilepsy. Lancet Neurol 2018;17:1098-1108.

Frauscher B, Gotman J. Sleep, oscillations, interictal discharges, and seizures in human focal epilepsy. Neurobiol Dis 2019;127:545-553.

Ismayilova V, Demir AU, Tezer FI. Subjective sleep disturbance in epilepsy patients at an outpatient clinic: a questionnaire-based study on prevalence. Epilepsy Res 2015;115:119-125.

Sudbrack-Oliveira P, Lima Najar L, Foldvary-Schaefer N, da Mota Gomes M. Sleep architecture in adults with epilepsy: a systematic review. Sleep Med 2019;53:22-27.

Terzano MG, Parrino L, Anelli S, Halasz P. Modulation of generalized spike-and-wave discharges during sleep by cyclic alternating pattern. Epilepsia 1989;30:772-781.

Terzano MG, Parrino L, Garofalo PG, et al. Activation of partial seizures with motor signs during cyclic alternating pattern in human sleep. Epilepsy Res 1991;10:166-173.

Parrino L, Smerieri A, Spaggiari MC, Terzano MG. Cyclic alternating pattern (CAP) and epilepsy during sleep: how a physiological rhythm modulates a pathological event. Clin Neurophysiol 2000;111:S39-S46.

Terzano MG, Parrino L, Anelli S, et al. Effects of generalized interictal EEG discharges on sleep stability: assessment by means of cyclic alternating pattern. Epilepsia 1992;33:317-326.

Nobili L, Sartori I, Terzaghi M, et al. Intracerebral recordings of minor motor events, paroxysmal arousals and major seizures in nocturnal frontal lobe epilepsy. Neurol Sci 2005;26:s215-s219.

Malow A, Bowes RJ, Ross D. Relationship of temporal lobe seizures to sleep and arousal: a combined scalp-intracranial electrode study. Sleep 2000;23:231-234.

Nobili L, Sartori I, Terzaghi M, 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;29:701-704.

Sanchez Fernandez I, Loddenkemper T, Galanopoulou AS, Moshe SL. Should epileptiform discharges be treated? Epilepsia 2015;56:1492-1504.

Ives JR. New chronic EEG electrode for critical/intensive care unit monitoring. J Clin Neurophysiol 2005;22:119-123.

Berry RB, Brooks R, Gamaldo CE, et al. The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications, version 2.4. www.aasmnet.org American Academy of Sleep Medicine: Darien, IL, 2017.

ASDA. EEG arousals: scoring rules and examples: a preliminary report from the Sleep Disorders Atlas Task Force of the American Sleep Disorders Association. Sleep 1992;15:173-184.

Perucca P, Dubeau F, Gotman J. Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology. Brain 2014;137:183-196.

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.

Jones EG. The thalamus. 2nd ed. Cambridge: University Press, 2007.

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.

Mitterling T, Hogl B, Schonwald SV, et al. Sleep and respiration in 100 healthy Caucasian sleepers-a Polysomnographic study according to American Academy of sleep medicine standards. Sleep 2015;38:867-875.

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.

Manni R, Galimberti CA, Sartori I, et al. Nocturnal partial seizures and arousals/awakenings from sleep: an ambulatory EEG study. Funct Neurol 1997;12:107-111.

Yildiz FG, Tezer FI, Saygi S. Temporal relationship between awakening and seizure onset in nocturnal partial seizures. J Neurol Sci 2012;315:33-38.

Gumusyayla S, Erdal A, Tezer FI, Saygi S. The temporal relation between seizure onset and arousal-awakening in temporal lobe seizures. Seizure 2016;39:24-27.

Dasheiff RM, Kofke WA. Primarily generalized seizures are more effective than partial seizures in arousing patients from sleep. Neurol Res 2003;25:63-67.

Roehrs T, Merlotti L, Petrucelli N, et al. Experimental sleep fragmentation. Sleep 1994;17:438-443.

Ermis U, Krakow K, Voss U. Arousal thresholds during human tonic and phasic REM sleep. J Sleep Res 2010;19:400-406.

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.

Zucconi M, Oldani A, Smirne S, Ferini-Strambi L. The macrostructure and microstructure of sleep in patients with autosomal dominant nocturnal frontal lobe epilepsy. J Clin Neurophysiol 2000;17:77-86.

Terzaghi M, Sartori I, Mai R, et al. Coupling of minor motor events and epileptiform discharges with arousal fluctuations in NFLE. Epilepsia 2008;49:670-676.

Saper CB, Fuller PM, Pedersen NP, et al. Sleep state switching. Neuron 2010;68:1023-1042.

Afifi A, Bergman R. Functional neuroanatomy. 2nd ed. New York: The McGraw Hill Companies Inc, 2005.

Devinsky O, Emoto S, Goldstein DS, et al. Cerebrospinal fluid and serum levels of dopa, catechols, and monoamine metabolites in patients with epilepsy. Epilepsia 1992;33:263-270.

During MJ, Spencer DD. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 1993;341:1607-1610.

Ujma PP, Simor P, Ferri R, et al. Increased interictal spike activity associated with transient slow wave trains during non-rapid eye movement sleep. Sleep Biol Rhythms 2015;13:155-162.

Halasz P, Ujszaszi J, Terzano MG, Declerck AC. Spectral features of evoked microarousals. New York: Raven Press, 1991.

Halasz P, Terzano M, Parrino L, Bodizs R. The nature of arousal in sleep. J Sleep Res 2004;13:1-23.

Steriade M, Amzica F. Slow sleep oscillation, rhythmic K-complexes, and their paroxysmal developments. J Sleep Res 1998;7:30-35.

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.

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.

Peter-Derex L, Magnin M, Bastuji H. Heterogeneity of arousals in human sleep: a stereo-electroencephalographic study. Neuroimage 2015;123:229-244.

Bonnet MH, Doghramji K, Roehrs T, et al. The scoring of arousal in sleep: reliability, validity, and alternatives. J Clin Sleep Med 2007;3:133-145.

Galer S, Urbain C, De Tiege X, et al. Impaired sleep-related consolidation of declarative memories in idiopathic focal epilepsies of childhood. Epilepsy Behav 2015;43:16-23.

Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci 2010;11:114-126.

Halasz P, Ujma PP, Fabo D, et al. Epilepsy as a derailment of sleep plastic functions may cause chronic cognitive impairment - a theoretical review. Sleep Med Rev 2019;45:31-41.

Mendes RAV, Zacharias LR, Ruggiero RN, et al. Hijacking of hippocampal-cortical oscillatory coupling during sleep in temporal lobe epilepsy. Epilepsy Behav 2019;15:106608.

Peled R, Lavie P. Paroxysmal awakenings from sleep associated with excessive daytime somnolence: a form of nocturnal epilepsy. Neurology 1986;36:95-98.

Serafini A, Kuate C, Gelisse P, et al. Sleep before and after temporal lobe epilepsy surgery. Seizure 2012;21:260-265.

Lin Z, Si Q, Xiaoyi Z. Obstructive sleep apnoea in patients with epilepsy: a meta-analysis. Sleep Breath 2017;21:263-270.

Invasive Electrophysiology for Circuit Discovery and Study of Comorbid Psychiatric Disorders in Patients With Epilepsy: Challenges, Opportunities, and Novel Technologies