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Slow oscillations open susceptible time windows for epileptic discharges

Bénar, Christian G.
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Published in Epilepsia. 2021
Abstract Objective: In patients with epilepsy, interictal epileptic discharges are a diag-nostic hallmark of epilepsy and represent abnormal, so- called “irritative” activity that disrupts normal cognitive functions. Despite their clinical relevance, their mechanisms of generation remain poorly understood. It is assumed that brain activity switches abruptly, unpredictably, and supposedly randomly to these epi-leptic transients. We aim to study the period preceding these epileptic discharges, to extract potential proepileptogenic mechanisms supporting their expression.Methods: We used multisite intracortical recordings from patients who under-went intracranial monitoring for refractory epilepsy, the majority of whom had a mesial temporal lobe seizure onset zone. Our objective was to evaluate the ex-istence of proepileptogenic windows before interictal epileptic discharges. We tested whether the amplitude and phase synchronization of slow oscillations (.5– 4Hz and 4– 7Hz) increase before epileptic discharges and whether the latter are phase- locked to slow oscillations. Then, we tested whether the phase- locking of neuronal activity (assessed by high- gamma activity, 60– 160Hz) to slow oscil-lations increases before epileptic discharges to provide a potential mechanism linking slow oscillations to interictal activities.Results: Changes in widespread slow oscillations anticipate upcoming epileptic discharges. The network extends beyond the irritative zone, but the increase in amplitude and phase synchronization is rather specific to the irritative zone. In contrast, epileptic discharges are phase- locked to widespread slow oscillations and the degree of phase- locking tends to be higher outside the irritative zone. Then, within the irritative zone only, we observe an increased coupling between slow oscillations and neuronal discharges before epileptic discharges.Significance: Our results show that epileptic discharges occur during vulnerable time windows set up by a specific phase of slow oscillations. The specificity of these permissive windows is further reinforced by the increased coupling of neu-ronal activity to slow oscillations. These findings contribute to our understanding of epilepsy as a distributed oscillopathy and open avenues for future neuromodu-lation strategies aiming at disrupting proepileptic mechanisms.
Keywords Human epilepsyInterictal epileptic dischargesIntracranial recordingPhase– amplitude couplingSlow oscillations
PMID: 34338315
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Research groups Epilepsie et Chirurgie (149)
Epilepsie et réseaux cérébraux (1002)
Human Neuron Lab (1034)
Swiss National Science Foundation: 167836; CRSII5 170873; 192749; CRS115-180365; 163398
(ISO format)
SHEYBANI, Laurent et al. Slow oscillations open susceptible time windows for epileptic discharges. In: Epilepsia, 2021. doi: 10.1111/epi.17020 https://archive-ouverte.unige.ch/unige:154510

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Deposited on : 2021-09-08

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