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

Hannan, Sana and Thomas, John and Jaber, Kassem and El Kosseifi, Charbel and Ho, Alyssa and Abdallah, Chifaou and Avigdor, Tamir and Gotman, Jean and Frauscher, Birgit (2023) The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug‐Resistant Epilepsy. Annals of Neurology. ISSN 0364-5134

Abstract

Objective: 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. Methods: 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. Results: 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). Interpretation: 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.