Quantitative visualization of ictal subdural EEG changes in children with neocortical focal seizures

Abstract

Objective: To quantify the ictal subdural electroencephalogram (EEG) changes using spectral analysis, and to delineate the quantitatively defined ictal onset zones on high-resolution 3D MR images in children with intractable neocortical epilepsy.

Methods: Fourteen children with intractable neocortical epilepsy (age: 1-16 years) who had subsequent resective surgery were retrospectively studied. The subjects underwent a high-resolution MRI and prolonged subdural EEG recording. Spectral analysis was applied to 3 habitual focal seizures. After fast Fourier transformation of the EEG epoch at ictal onset, an amplitude spectral curve (square root of the power spectral curve) was created for each electrode. The EEG magnitude of ictal rhythmic discharges was defined as the area under the amplitude spectral curve within a preset frequency band including the ictal discharge frequency, and calculated for each electrode. The topography mapping of ictal EEG magnitude was subsequently displayed on a surface-rendered MRI. Finally, receiver operating characteristic (ROC) analysis was performed to evaluate the consistency between quantitatively and visually defined ictal onset zones.

Results: The electrode showing the maximum of the averaged ictal EEG magnitude was part of the visually defined ictal onset zone in all cases. ROC analyses demonstrated that electrodes showing >30% of the maximum of the averaged ictal EEG magnitude had a specificity of 0.90 and a sensitivity of 0.74 for the concordance with visually defined ictal onset zones.

Significance: Quantitative ictal subdural EEG analysis using spectral analysis may supplement conventional visual inspection in children with neocortical epilepsy by providing an objective definition of the onset zone and its simple visualization on the patient's MRI.

Fig. 1

Ictal EEG of an 9-year-old boy with non-lesional neocortical epilepsy. (A) Prior to clinical onset (arrow), low-amplitude fast wave bursts emerge in channels A4, A3 and A5. The first epoch was placed at seizure onset, and the ictal discharge frequency was 26 Hz at the most-consistent onset electrode (A4). Each epoch length was 0.64 s. Note that EEG during epoch 3 was contaminated with diffuse movement artifacts (arrow). (B–D) Amplitude spectra at channels A4, A5 and A6 in the first epoch of the same ictal event are shown. A 5-point smoothing was applied. Ictal discharge frequency was 26 Hz at the first epoch. Note the various amplitudes of the peaks in the 24–32 Hz band at channels A4, A5 and A6, respectively (arrows) and that the lowest frequency part of the amplitude spectral curve is clipped off. (E) Topography of the ictal EEG magnitude within a 24–32 Hz band at the first epoch in the same ictal event. The highest ictal EEG magnitude was seen at electrode A4. White electrodes represent ‘visually defined onset’ electrodes. (F) The location of subdural grid electrodes are displayed onto the 3D-reconstructed MRI (von Stockhausen et al., 1997). The white line represents the central sulcus. (G) The topography of the ictal EEG magnitude at seizure onset is superimposed onto the 3D-reconstructed MRI.

Fig. 2

A 3D-reconstructed surface MRI and sequential topographic changes in the EEG magnitude during a seizure in a 1-year-old boy with uncontrolled focal seizures and a diagnosis of tuberous sclerosis complex. (A) A 7 s raw ictal subdural EEG showed a rhythmic theta activity at 5 Hz gradually building up in amplitude. Soon after the ictal EEG onset, brief rhythmic alpha wave activity emerged at electrode G4 and evolved into a continuous rhythmic alpha activity at the same area (arrows). This rhythmic alpha activity at electrode G4 may indicate ictal propagation. (B) The location of subdural electrodes is displayed onto the 3D MRI. Thereby, the visually defined ictal onset zones are shown by white circles. (C) The resection margin is delineated with a yellow line. The patient has been seizure-free for 12 months since surgery, where the primary hand motor cortex under electrode G4 was not resected. (D–F) Spectral analysis for 3 consecutive 2.56 s epochs demonstrates the topography of EEG magnitudes within a 4–8 Hz frequency band and shows the highest EEG magnitude in the primary sensory face area at seizure onset. The EEG magnitude at that region was further increased in the subsequent epochs. Adjacent electrodes also show gradually increasing EEG magnitude in the subsequent epochs. (G–I) Spectral analysis for 3 consecutive 2.56 s epochs demonstrates the topography of EEG magnitudes within an 8–12 Hz frequency band, of which spatial pattern is similar to that for a 4–8 Hz frequency band at the first epoch. The EEG magnitude within an 8–12 Hz frequency band gradually increased especially at electrode G4 (arrow), as the rhythmic alpha wave activity became visually continuous during ictal propagation. At the third epoch, the EEG magnitude within an 8–12 Hz frequency band was considerably large and cannot be neglected to delineate the ictal propagation.

Fig. 3

Concordance between quantitatively and visually defined onset electrodes. (A) The relationship between quantitatively and visually defined ictal onset zones in an 9-year-old boy with non-lesional neocortical epilepsy is shown (patient #7). It should be noted that subdural electrodes on the left inferior frontal or the temporal regions are not shown, and a total of 82 electrodes were included into statistical analysis. Electrodes encircled by bold, intermediate, thin, broken, and dotted lines represent the quantitatively defined ictal onset zones determined by various cutoff thresholds of 80, 60, 40, 30 and 20% of the maximal averaged ictal EEG magnitude. Cutoff thresholds of 80, 60, 40, 30 and 20% of the maximal averaged ictal EEG magnitude resulted in specificity of 1.00, 1.00, 0.96, 0.89, and 0.81 and sensitivity of 0.29, 0.29, 1.00, 1.00, and 1.00 for the concordance with ‘visually defined onset’ electrodes (white circles) in this individual. (B) The receiver operating characteristics curve (derived from mean specificity and sensitivity among all subjects) shows that cutoff thresholds of 80, 60, 40, 30 and 20% of the maximum of the averaged ictal EEG magnitude resulted in mean specificity of 1.00, 0.98, 0.95, 0.90 and 0.84 as well as mean sensitivity of 0.41, 0.56, 0.69, 0.74 and 0.74 for the concordance with ‘visually defined onset’ electrodes. Three patients showed multiple ictal onset foci; in these cases, we calculated sensitivity and specificity of the quantitatively defined seizure-onset zone for concordance with the dominant focus.