Brain regions and epileptogenicity influence epileptic interictal spike production and propagation during NREM sleep in comparison with wakefulness

Abstract

SummaryObjective: Non-rapid eye movement (NREM) sleep is known to be a brain state associated with an activation of interictal epileptic activity. The goal of this work was to quantify topographic changes occurring during NREM sleep in comparison with wakefulness. Method: We studied intracerebral recordings of 20 patients who underwent stereo-electroencephalography (SEEG) during presurgical evaluation for pharmacoresistant focal epilepsy. We measured the number of interictal spikes (IS) and quantified the co-occurrence of IS between brain regions during 1 hour of NREM sleep and 1 hour of wakefulness. Co-occurrence is a method to estimate IS networks based on a temporal concordance between IS of different brain regions.Each studied region was labeled as "seizure-onset zone" (SOZ), "propagation zone" (PZ), or "not involved region" (NIR). Results: During NREM sleep, the number of interictal spikes significantly increased in all regions (mean of 68%). This increase was higher in medial temporal regions than in other regions, whether involved in the SOZ. Spike co-occurrence increased significantly in all regions during NREM sleep in comparison with wakefulness but was greater in neocortical regions. Spike co-occurrence in medial temporal regions was not higher than in other regions, suggesting that the increase of the number of spikes in this region was in great part a local effect. Significance: This study demonstrated that medial temporal regions show a greater propensity to spike production or propagation during NREM sleep compared to other brain regions, even when the medial temporal lobe is not involved in the SOZ. K E Y W O R D Sco-occurrence, focal epilepsy, interictal spikes, NREM sleep, stereo-electroencephalography

Reproducibility of interictal spike propagation in children with refractory epilepsy

“…Spike coactivation referred to the detection of spikes at distinct electrodes with brief interspike latencies ( Figure 1B). 28,29 Consistent with previous studies, coactivation was defined as peak times separated by <150 msec. 5,20,21 Spike coactivation rates were encoded in an electrode-byelectrode matrix (C).…”

The first-hour-of-the-day sleep EEG reliably identifies interictal epileptiform discharges during long-term video-EEG monitoring

“…Using intracranial EEG recording, IEDs were increased in all brain regions during NREM sleep compared with wakefulness. NREM sleep strongly activated interictal spikes in the seizure onset zone and promotes their propagation to other cortical areas [8]. Larger scalp voltage field potentials of IEDs were also detected in patients with temporal lobe epilepsy during sleep than wakefulness [10].…”

“…Therefore, a 3-day EMU admission might be a reasonable duration for the identification of IEDs during long-term video-EEG monitoring. Interictal epileptiform discharges are strongly activated during NREM sleep [7,8,21], although it has remained controversial whether IEDs are activated more significantly during NREM stage 1 and 2, or during slow-wave sleep [22]. IEDs are more effectively enhanced during sleep in patients with focal epilepsy than generalized epilepsy as compared with wakefulness [23,24].…”

“…Synchronous EEG oscillations including tonic background slow waves and phasic sleep EEG transients (i.e. sleep spindles, k-complexes, ripples) activate IEDs during drowsiness and NREM sleep [8][9][10][11], whereas asynchronous neuronal oscillations during wakefulness and REM sleep suppress IEDs [11,12]. Sleep is the most effective activation procedure as compared to other activation procedures such https://doi.org/10.1016/j.seizure.2018.10.015 Received 11 August 2018; Received in revised form 20 October 2018; Accepted 25 October 2018 as photic stimulation and hyperventilation and shows the highest yield of IEDs [13].…”

Can histologically normal epileptogenic zone share common electrophysiological phenotypes with focal cortical dysplasia? SEEG-based study in MRI-negative epileptic patients

“…Interictal activity (background, spikes, spike and wave complexes, slow activities, fast activities) was assessed on the electrodes that belonged to the EZ during a 10 min period of resting state in waking and during 10 min of NREM sleep. Sleep recordings were chosen because interictal epileptic activity and in particular, pseudoperiodic patterns pathognomonic of FCD type II are known to be activated in NREM sleep [24,36,37]. Interictal SEEG samples were selected at least 24 h after the SEEG implantation and The topographic organization of the EZ was defined as temporal, temporal plus (EI maximum within temporal lobe but also area with EI > 0.4 outside temporal lobe such as insula, frontal or occipital lobe), operculo-insular (opercular, insular or operculoinsular), frontal , frontal plus (EI maximum within frontal lobe but also area with EI > 0.4 outside frontal lobe such as temporal, insula or parietal), parietal, occipital.…”