Stability of synchronization clusters and seizurability in temporal lobe epilepsy.

Agostina Palmigiano,Guillermo J Ortega,Rafael García De Sola,Jesús Pastor,Dante R Chialvo

doi:10.1371/journal.pone.0041799

Agostina Palmigiano, Guillermo J Ortega + Show 3 more

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https://doi.org/10.1371/journal.pone.0041799

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Abstract

PurposeIdentification of critical areas in presurgical evaluations of patients with temporal lobe epilepsy is the most important step prior to resection. According to the “epileptic focus model”, localization of seizure onset zones is the main task to be accomplished. Nevertheless, a significant minority of epileptic patients continue to experience seizures after surgery (even when the focus is correctly located), an observation that is difficult to explain under this approach. However, if attention is shifted from a specific cortical location toward the network properties themselves, then the epileptic network model does allow us to explain unsuccessful surgical outcomes.MethodsThe intraoperative electrocorticography records of 20 patients with temporal lobe epilepsy were analyzed in search of interictal synchronization clusters. Synchronization was analyzed, and the stability of highly synchronized areas was quantified. Surrogate data were constructed and used to statistically validate the results. Our results show the existence of highly localized and stable synchronization areas in both the lateral and the mesial areas of the temporal lobe ipsilateral to the clinical seizures. Synchronization areas seem to play a central role in the capacity of the epileptic network to generate clinical seizures. Resection of stable synchronization areas is associated with elimination of seizures; nonresection of synchronization clusters is associated with the persistence of seizures after surgery.DiscussionWe suggest that synchronization clusters and their stability play a central role in the epileptic network, favoring seizure onset and propagation. We further speculate that the stability distribution of these synchronization areas would differentiate normal from pathologic cases.

Highlights

Partial epileptic seizures were traditionally thought to originate in specific areas of the cortex known as seizure onset zones (SOZ), before spreading to other areas, known as epileptogenic zones (EZ), some of which overlap with the SOZ
We suggest that synchronization clusters and their stability play a central role in the epileptic network, favoring seizure onset and propagation
We demonstrate the existence of intense local synchronization (LS) areas in the lateral and mesial cortices of temporal lobe epilepsy (TLE) patients

Summary

Introduction

Partial epileptic seizures were traditionally thought to originate in specific areas of the cortex known as seizure onset zones (SOZ), before spreading to other areas, known as epileptogenic zones (EZ), some of which overlap with the SOZ. EZ are essential for seizures to propagate [1,2] Surgical approaches to this condition include resection or disconnection of these areas, principally the SOZ (usually identified as the epileptic focus), from the rest of the brain. This ‘‘single focus’’ model has been challenged [3,4,5] in favor of a network model in which the focus (or foci) would be distributed along the limbic structures. Even if the suspected epileptogenic area is correctly localized in presurgical studies and resected during surgery, a significant minority of patients continue to experience seizures after surgery, favoring the concept of an epileptic network

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