Value of electrical stimulation and high frequency oscillations (80-500 Hz) in identifying epileptogenic areas during intracranial EEG recordings

Abstract

Purpose: Electrical stimulation (ES) is used during intracranial electroencephalography (EEG) investigations to delineate epileptogenic areas and seizure-onset zones (SOZs) by provoking afterdischarges (ADs) or patients' typical seizure. High frequency oscillations (HFOs--ripples, 80-250 Hz; fast ripples, 250-500 Hz) are linked to seizure onset. This study investigates whether interictal HFOs are more frequent in areas with a low threshold to provoke ADs or seizures.

Methods: Intracranial EEG studies were filtered at 500 Hz and sampled at 2,000 Hz. HFOs were visually identified. Twenty patients underwent ES, with gradually increasing currents. Results were interpreted as agreeing or disagreeing with the intracranial study (clinical-EEG seizure onset defined the SOZ). Current thresholds provoking an AD or seizure were correlated with the rate of HFOs of each channel.

Results: ES provoked a seizure in 12 and ADs in 19 patients. Sixteen patients showed an ES response inside the SOZ, and 10 had additional areas with ADs. The response was more specific for mesiotemporal than for neocortical channels. HFO rates were negatively correlated with thresholds for ES responses; especially in neocortical regions; areas with low threshold and high HFO rate were colocalized even outside the SOZ.

Discussion: Areas showing epileptic HFOs colocalize with those reacting to ES. HFOs may represent a pathologic correlate of regions showing an ES response; both phenomena suggest a more widespread epileptogenicity.

Figure 1

This figure demonstrates the concept of the four different groups of channels used for statistical comparison. On the left, a situation that would have been rated as complete agreement; and on the right, one with partial disagreement. Epilepsia © ILAE

Figure 2

Current thresholds to evoke the different stimulation response types (AD, afterdischarge) in mesiotemporal (blue) and neo-cortical (red) channels. AD gives the results for all ADs together, AD + propagation and AD + clinic are included in this category. Some ADs may be shown in all three categories, as they showed propagation as well as clinical symptoms. In general, larger currents were needed to induce a response in neo-cortical areas. Epilepsia © ILAE

Figure 3

Percentage of channels showing a certain response type (AD, afterdischarge) within the seizure-onset zone (SOZ) (solid bars) and outside the SOZ (open bars). Mesiotemporal channels (left) showed higher percentages and, therefore, a larger overlap between SOZ and stimulation response than neocortical channels (right). Numbers on each bar give the actual number of responses that occurred for each response type. Epilepsia © ILAE

Figure 4

An example of channels showing both a stimulation response and interictal high frequency oscillations (HFOs). (A) Electroencephalography (EEG) section after electrical stimulation (ES) of channel LP1-2 (green), with an afterdischarge (AD) plus propagation (orange) to the left hippocampus (LH) and parahippocampus (LP) and to a lesser extend to the left amygdala (LA). (B) Interictal EEG of the same patient at normal time scale. (C) The gray section in B is extended to show the same EEG segment with no filter (left), 80-Hz high-pass filter (middle), and 250-Hz high-pass filter (right). Ripples and fast ripples are visible in the channels with stimulation response (orange). Epilepsia © ILAE