Lasting and extensive consequences of left mesial temporal lobe seizures on electrical cortical activity

Background and objectives: Focal epilepsies disrupt long-range networks with seizure recurrence driving both regional and global alterations in connectivity networks. While prior studies have focused on the interictal consequences, limited data exist on the direct aftermath of focal seizures. We hyp...

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Main Authors: Mathieu Dhoisne, Nacim Betrouni, Sophie Hennion, Lucie Plomhause, Arnaud Delval, Philippe Derambure
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811924004725
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author Mathieu Dhoisne
Nacim Betrouni
Sophie Hennion
Lucie Plomhause
Arnaud Delval
Philippe Derambure
author_facet Mathieu Dhoisne
Nacim Betrouni
Sophie Hennion
Lucie Plomhause
Arnaud Delval
Philippe Derambure
author_sort Mathieu Dhoisne
collection DOAJ
description Background and objectives: Focal epilepsies disrupt long-range networks with seizure recurrence driving both regional and global alterations in connectivity networks. While prior studies have focused on the interictal consequences, limited data exist on the direct aftermath of focal seizures. We hypothesize that mesial temporal lobe seizures lead to enduring cortical disorganization. The aim was to assess the effects of a mesial temporal lobe seizure on cortical activity and understand how the side of seizure onset influences these consequences. Methods: In this retrospective study, high-resolution EEG of patients with mesial temporal lobe epilepsy (mTLE) were analyzed. Groups of patients were identified based on the side of seizure onset. We compared relative powers in different frequency bands between interictal (prior to the seizure) and late postictal (one hour following the seizure) periods. Network-based statistics were employed to compare functional connectivity at source level between periods. Results: Twenty-three patients were included (13 left and 10 right mesial temporal lobe seizures). In patients with left mTLE, we observed a post-seizure increase in the relative spectral power in the delta band (p = 0.001) and a decrease in the relative spectral power in the alpha band (p = 0.013) over the left temporofrontal regions. We isolated a subnetwork that presented a decrease in connectivity strength in alpha band, primarily involving long-range left hemisphere connections (p = 0.042). We also identified a subnetwork that presented a decrease in connectivity strength in theta band, primarily involving interhemispheric connections (p = 0.039). No significant post-seizure changes were found in patients with right mTLE. Discussion: Left mesial temporal lobe seizures appear to be associated with lasting and widespread disorganization of cortical activity. We propose that the postictal state is associated with a prolonged functional deafferentation of the affected region in patients with left mTLE. This leads to a widespread disorganization of the functional networks, which may be associated with cognitive impairments and promote the progression of epilepsy. Further studies are required to fully understand the functional repercussions.
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spelling doaj-art-2bbd7d8885a0470e97c71c385a93fc792025-01-11T06:38:33ZengElsevierNeuroImage1095-95722025-01-01305120975Lasting and extensive consequences of left mesial temporal lobe seizures on electrical cortical activityMathieu Dhoisne0Nacim Betrouni1Sophie Hennion2Lucie Plomhause3Arnaud Delval4Philippe Derambure5Department of Clinical Neurophysiology, Lille University Hospital, Lille 59037, France; INSERM U1172, LilNCog – Lille Neuroscience & Cognition, Lille 59000, France; Corresponding author at: Department of Clinical Neurophysiology, Lille University Hospital, Avenue du professeur Émile Laine, Lille 59037, France.INSERM U1172, LilNCog – Lille Neuroscience & Cognition, Lille 59000, FranceDepartment of Clinical Neurophysiology, Lille University Hospital, Lille 59037, France; INSERM U1172, LilNCog – Lille Neuroscience & Cognition, Lille 59000, FranceDepartment of Clinical Neurophysiology, Lille University Hospital, Lille 59037, France; INSERM U1172, LilNCog – Lille Neuroscience & Cognition, Lille 59000, FranceDepartment of Clinical Neurophysiology, Lille University Hospital, Lille 59037, France; INSERM U1172, LilNCog – Lille Neuroscience & Cognition, Lille 59000, FranceDepartment of Clinical Neurophysiology, Lille University Hospital, Lille 59037, France; INSERM U1172, LilNCog – Lille Neuroscience & Cognition, Lille 59000, FranceBackground and objectives: Focal epilepsies disrupt long-range networks with seizure recurrence driving both regional and global alterations in connectivity networks. While prior studies have focused on the interictal consequences, limited data exist on the direct aftermath of focal seizures. We hypothesize that mesial temporal lobe seizures lead to enduring cortical disorganization. The aim was to assess the effects of a mesial temporal lobe seizure on cortical activity and understand how the side of seizure onset influences these consequences. Methods: In this retrospective study, high-resolution EEG of patients with mesial temporal lobe epilepsy (mTLE) were analyzed. Groups of patients were identified based on the side of seizure onset. We compared relative powers in different frequency bands between interictal (prior to the seizure) and late postictal (one hour following the seizure) periods. Network-based statistics were employed to compare functional connectivity at source level between periods. Results: Twenty-three patients were included (13 left and 10 right mesial temporal lobe seizures). In patients with left mTLE, we observed a post-seizure increase in the relative spectral power in the delta band (p = 0.001) and a decrease in the relative spectral power in the alpha band (p = 0.013) over the left temporofrontal regions. We isolated a subnetwork that presented a decrease in connectivity strength in alpha band, primarily involving long-range left hemisphere connections (p = 0.042). We also identified a subnetwork that presented a decrease in connectivity strength in theta band, primarily involving interhemispheric connections (p = 0.039). No significant post-seizure changes were found in patients with right mTLE. Discussion: Left mesial temporal lobe seizures appear to be associated with lasting and widespread disorganization of cortical activity. We propose that the postictal state is associated with a prolonged functional deafferentation of the affected region in patients with left mTLE. This leads to a widespread disorganization of the functional networks, which may be associated with cognitive impairments and promote the progression of epilepsy. Further studies are required to fully understand the functional repercussions.http://www.sciencedirect.com/science/article/pii/S1053811924004725Functional connectivityLate postictalMesial temporal lobe seizuresSide of seizure onset
spellingShingle Mathieu Dhoisne
Nacim Betrouni
Sophie Hennion
Lucie Plomhause
Arnaud Delval
Philippe Derambure
Lasting and extensive consequences of left mesial temporal lobe seizures on electrical cortical activity
NeuroImage
Functional connectivity
Late postictal
Mesial temporal lobe seizures
Side of seizure onset
title Lasting and extensive consequences of left mesial temporal lobe seizures on electrical cortical activity
title_full Lasting and extensive consequences of left mesial temporal lobe seizures on electrical cortical activity
title_fullStr Lasting and extensive consequences of left mesial temporal lobe seizures on electrical cortical activity
title_full_unstemmed Lasting and extensive consequences of left mesial temporal lobe seizures on electrical cortical activity
title_short Lasting and extensive consequences of left mesial temporal lobe seizures on electrical cortical activity
title_sort lasting and extensive consequences of left mesial temporal lobe seizures on electrical cortical activity
topic Functional connectivity
Late postictal
Mesial temporal lobe seizures
Side of seizure onset
url http://www.sciencedirect.com/science/article/pii/S1053811924004725
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