The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug‐Resistant Epilepsy

Author:

Hannan Sana12ORCID,Thomas John1ORCID,Jaber Kassem1,El Kosseifi Charbel1,Ho Alyssa1,Abdallah Chifaou1,Avigdor Tamir1ORCID,Gotman Jean3,Frauscher Birgit1456ORCID

Affiliation:

1. Analytical Neurophysiology Lab, Montreal Neurological Institute and Hospital McGill University Montréal Quebec Canada

2. Department of Biomedical and Life Sciences Lancaster University Lancaster United Kingdom

3. Montreal Neurological Institute and Hospital McGill University Montréal Quebec Canada

4. Department of Neurology Duke University Medical Center Durham North Carolina USA

5. Analytical Neurophysiology Lab Duke University Medical Center Durham North Carolina USA

6. Department of Biomedical Engineering Duke Pratt School of Engineering Durham North Carolina USA

Abstract

ObjectiveSleep 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.MethodsWe 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.ResultsThe 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).InterpretationIn 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 2024;95:42–56

Funder

Canadian Institutes of Health Research

FRQS

Hewitt Foundation

Savoy Foundation

Publisher

Wiley

Subject

Neurology (clinical),Neurology

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