Rapid eye movement sleep affects interictal epileptic activity differently in mesiotemporal and neocortical areas

Ho, Alyssa and Hannan, Sana and Thomas, John and Avigdor, Tamir and Abdallah, Chifaou and Dubeau, François and Gotman, Jean and Frauscher, Birgit (2023) Rapid eye movement sleep affects interictal epileptic activity differently in mesiotemporal and neocortical areas. Epilepsia, 64 (11). pp. 3036-3048. ISSN 0013-9580

Abstract

Objective: 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. Methods: 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. Results: 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). Significance: 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.