Intracranial EEG in Temporal Lobe Epilepsy: Location of Seizure Onset Relates to Degree of Hippocampal Pathology

Abstract

Summary:Purpose: To determine whether the specific location of electrographic seizure onset in the temporal lobe is related to hippocampal pathology in temporal lobe epilepsy (TLE).Methods: Consecutive presurgical patients with scalp EEGvideo evidence of TLE and no or mild hippocampal atrophy (HA) on magnetic resonance imaging (MRI) were prospectively studied by using depth and subdural strip electrode recordings to identify the site of the initial ictal discharge (IID). Thirty-four patients had either no or mild HA (HA-group). Four additional patients with moderate or marked HA (HA+ group) who required depth and strip electrodes served as a comparison group. Hippocampal pathology was assessed by MRI volumetrics and histopathologic grade of sclerosis (HS).Results: Thirty-eight patients were investigated. In the HAgroup, 10 patients had lobar ictal EEG onsets in the hippocampus (HF), medial paleocortex (MPC), and lateral neocortex (LNC); eight cases had regional IIDs in both HF and MPC; 12 persons had IIDs completely outside the HF; three cases lacked depth electrodes, and only one case (3%) had an IID confined to the HF. By contrast, three (75%) of four HA+ cases had IIDs confined to the HF (p = 0.002). Similarly, in 12 patients with low-grade HS, IIDs confined to the HF area were seen significantly less often than in six cases with high-grade HS (p = 0.025).Conclusions: In this study of a large number of patients with no to mild and a smaller group with moderate to marked HA and HS, the location of seizure onset in the temporal lobe was related to the degree of hippocampal pathology. Absence of HA and low-grade HS was each associated with IIDs in both the hippocampus and medial (with or without lateral) temporal cortex, or only the MPC or LNC. Marked HA and high-grade HS both were associated with IIDs restricted to the HF. Key Words: EEG-Intracranial electrodes-Depth electrodes-Temporal lobe epilepsy-Pathology-Medial temporal sclerosis.Subtypes of temporal lobe epilepsy (TLE) have been proposed based on semiology, pathology, and neuroimaging findings (1-3). When hippocampal sclerosis (HS) is found in specimens from anteromesial temporal resections (AMTR), mesial TLE (MTLE) is often diagnosed (4). Occasionally, the hippocampus exhibits no or low-grade HS in AMTRs. In such instances, lateral or neocortical TLE (NTLE) may be suspected, particularly when seizures persist after resection of only MTL structures. Recent studies have begun to examine whether clinical neurophysiologic recordings can assist in differentiating MTLE from NTLE (5-10).Scalp EEG ictal discharges during temporal lobe complex partial seizures (CPSs) may consist of sequential spikes or sharp waves (11,12), but most commonly appear as rhythmic waves (13-17 (6) depth and subdural electrode recordings, Ebersole and Pacia found that scalp EEG temporal 5-to 9-Hz CPS discharges usually had ictal onset in the hippocampus, and that 2-to 5-Hz (lateralized or diffuse) extracranial ictal patterns often correlated with simultaneous ictal onset in hippocampu...

Grey and white matter abnormalities in temporal lobe epilepsy with and without mesial temporal sclerosis

“…Unfortunately, a number of patients had not undergone surgery to histologically confirm the presence or absence of MTS (10 out of 22), (2) Based on the findings of previous publications from our lab [2] and on electrophysiological findings [28] indicating a diffuse, medial–lateral temporal seizure onset zone in TLE with normal hippocampus, thickness of the inferior temporal lobe was selected as presumed seizure focus in TLE-no. However, only a subset of TLE-no had surgery, which in the case of postoperative seizure freedom is considered to be the ultimate confirmation of focus localization by EEG and; therefore, we cannot completely exclude that some of the TLE-no patients had mild hippocampal sclerosis not detected by MRI, (3) From this study we cannot conclude that TLE-mts and TLE-no are two distinctly different disorders given that we have not shown a significant difference between these two subgroups.…”

Epileptiform synchronization in the rat insular and perirhinal cortices in vitro

“…Furthermore, animais subjected to single episodes or a short series of seizures experience cell loss and synaptic rearrangement (Bengzon et al, 1997;Holmes and Ben-Ari, 1998;Haas et al, 2001). Combined MRI and EEG studies of TLE patients show that sites of epileptiform discharge onset tend to localize to the sa me brain regions exhibiting volumetric reductions (Cendes et al, 1996;Watson et al, 1997;Cendes et al, 2000;Bernasconi et al, 2003;Vossler et al, 2004). Many have therefore revised old theories to suggest instead that an initial insult causing subtle reactive changes can lead to recurrent temporal lobe seizures, which subsequently cause the global structural changes commonly associated with TLE (Ben-Ari, 1985;Holmes and Ben-Ari, 1998).…”

Widespread neocortical abnormalities in temporal lobe epilepsy with and without mesial sclerosis

“…To identify regions of cortical thinning in TLE-no. We expected extrafocal thinning in TLE-no to affect neocortical regions in the inferior medial temporal lobe (Carne et al, 2007; Vossler et al, 2004; Mueller et al 2007) and regions receiving projections from these regions, i.e., to show a different distribution than the one found in TLE-MTS.…”

“…atrophied hippocampus with MR signal abnormalities and severe neuronal loss in the histological examination, and TLE with normal appearing hippocampus on the MRI (TLE-no, about 30-40%) and no or only mild neuronal loss in the histological examination. Depth EEG exams show a relatively circumscribed epileptogenic zone in the hippocampus in TLE-MTS and more widespread, less well defined epileptogenic areas in the medial – lateral temporal lobe in TLE-no (Vossler et al 2004). In both types however, seizures are not restricted to the temporal lobe but can spread to other regions as well.…”

“…To identify regions of cortical gray matter thinning beyond the hippocampus in TLE-MTS and to confirm the typical pattern of cortical thinning in TLE-MTS described by previous studies. Based on EEG and structural findings in TLE-MTS (Vossler et al, 2004; Mueller et al, 2006), we expected to find neocortical thinning in regions receiving hippocampal projections . 2.…”