Origin and propagation of interictal discharges in the acute electrocorticogram. Implications for pathophysiology and surgical treatment of temporal lobe epilepsy

Abstract

Although acute electrocorticography (ECoG) is routinely performed during epilepsy surgery there is little evidence that the extent of the discharging regions is a useful guide to tailoring the resection or that the findings are predictive of outcome or pathology. Patterns of discharge propagation have, however, rarely been considered in assessing the ECoG. We hypothesize that regions where discharges show earliest peaks ('leading regions') are located in the epileptogenic zone, whereas sites in which late, secondary, propagated activity occurs have less epileptogenic potential and do not need to be excised. To allow intraoperative topographic ECoG analysis, a computer program has been developed to identify leading regions and the sites showing greatest rates or amplitudes of spikes. Their topography has been compared retrospectively with pathology and seizure control in 42 consecutive patients following temporal lobe surgery. Leading regions were most often found in the hippocampus, the subtemporal cortex and the superior temporal gyrus. The most common propagation patterns were from hippocampus to subtemporal cortex and vice versa. There was no association between seizure outcome and the location of regions with greatest incidence or amplitude of spikes or location of leading regions. There was, however, a strong and significant association between poor outcome and non-removal of leading regions other than those in the posterior subtemporal cortex. All leading regions (other than posterior subtemporal) were resected in 27 patients of whom 25 had a favourable outcome. Leading regions (other than posterior subtemporal) remained in 14 patients of whom only four had a good outcome. One patient had no epileptiform activity in the ECoG and good outcome. Persistent posterior subtemporal leading regions remained in nine subjects; all had favourable outcome (Grades I or II) but only three were seizure free. These results suggest that: (i) interictal epileptiform discharges may originate from a complex interaction between separate regions, resulting in propagation and recruitment of neuronal activity along specific neural pathways; (ii) removal of all discharging areas appears unnecessary to achieve seizure control provided that leading regions (other than posterior subtemporal) are removed; and (iii) identification of such leading regions could be used to tailor resections in order to improve seizure control and reduce neurological, neuropsychological and psychiatric post-surgical morbidity.

Selective amygdalohippocampectomy versus anterior temporal lobectomy in the management of mesial temporal lobe epilepsy: a meta-analysis of comparative studies

“…26,39 Moreover, some studies have indicated that SelAH has better neuropsychological outcomes 6,14 and a lower risk of visual field defects 22 than ATL. On the other hand, some investigators have recorded neocortical epileptiform spikes with cortical electrodes, 1,35 indicating that tailored resection of the temporal neocortex is Selective amygdalohippocampectomy versus anterior temporal lobectomy in the management of mesial temporal lobe epilepsy: a meta-analysis of comparative studies essential for MTLE. Other studies have suggested that better seizure outcomes were achieved in patients who underwent ATL than in those who underwent SelAH, 3,21 and that no significant differences in neuropsychological outcomes were found between the surgical strategies.…”

Surgical Implications of Neuromagnetic Spike Localization in Temporal Lobe Epilepsy

“…However, the non-AT dipoles were obviously reduced in the two patients with excellent seizure outcome; thus we believe that the non-AT localization was caused by remote activity propagated from the medial temporal epileptogenic area, and removal of the medial structures resulted in spike disappearance. Interictal cortical spikes can be propagated from the primary leading region near the epileptogenic area to remote secondary regions (4). Interictal spike propagations from deep to superficial temporal, anterior to posterior temporal, and temporal to frontal lobes were observed in spike-averaging studies (2,3).…”

“…Scalp-recorded EEG has been used to investigate interictal spike propagation (2,3). Intracranial EEG has revealed that leading spikes near the epileptogenic area may propagate over various neocortical areas (4,5). Therefore, the interictal spike area is usually more extensive than the epileptogenic area (1).…”

The pathology of magnetic-resonance-imaging-negative epilepsy

“…[1][2][3] The overall prevalence of nonlesional epilepsy in all surgical studies is B26%. 4 At present, surgical management of MRInegative pharmacoresistant focal epilepsy patients relies heavily on invasive intracranial electroencephalography, which is based on complimentary review of other noninvasive modalities including positron emission tomography, ictal single-photon emission computed tomography, and magnetoencephalography when available.…”