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

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The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug‐Resistant Epilepsy. / Hannan, Sana; Thomas, John; Jaber, Kassem et al.
In: Annals of Neurology, 29.09.2023.

Research output: Contribution to Journal/MagazineJournal articlepeer-review

Harvard

Hannan, S, Thomas, J, Jaber, K, El Kosseifi, C, Ho, A, Abdallah, C, Avigdor, T, Gotman, J & Frauscher, B 2023, 'The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug‐Resistant Epilepsy', Annals of Neurology. https://doi.org/10.1002/ana.26796

APA

Hannan, S., Thomas, J., Jaber, K., El Kosseifi, C., Ho, A., Abdallah, C., Avigdor, T., Gotman, J., & Frauscher, B. (2023). The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug‐Resistant Epilepsy. Annals of Neurology. Advance online publication. https://doi.org/10.1002/ana.26796

Vancouver

Hannan S, Thomas J, Jaber K, El Kosseifi C, Ho A, Abdallah C et al. The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug‐Resistant Epilepsy. Annals of Neurology. 2023 Sept 29. Epub 2023 Sept 29. doi: 10.1002/ana.26796

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Bibtex

@article{aaa258365f9d476ea7bb1dfa6bbad2bb,
title = "The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug‐Resistant Epilepsy",
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.  ",
author = "Sana Hannan and John Thomas and Kassem Jaber and {El Kosseifi}, Charbel and Alyssa Ho and Chifaou Abdallah and Tamir Avigdor and Jean Gotman and Birgit Frauscher",
year = "2023",
month = sep,
day = "29",
doi = "10.1002/ana.26796",
language = "English",
journal = "Annals of Neurology",
issn = "0364-5134",
publisher = "John Wiley and Sons Inc.",

}

RIS

TY - JOUR

T1 - The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug‐Resistant Epilepsy

AU - Hannan, Sana

AU - Thomas, John

AU - Jaber, Kassem

AU - El Kosseifi, Charbel

AU - Ho, Alyssa

AU - Abdallah, Chifaou

AU - Avigdor, Tamir

AU - Gotman, Jean

AU - Frauscher, Birgit

PY - 2023/9/29

Y1 - 2023/9/29

N2 - 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.  

AB - 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.  

U2 - 10.1002/ana.26796

DO - 10.1002/ana.26796

M3 - Journal article

JO - Annals of Neurology

JF - Annals of Neurology

SN - 0364-5134

ER -