Localizing value of electrical source imaging: Frontal lobe, malformations of cortical development and negative MRI related epilepsies are the best candidates

Abstract

Objective: We aimed to prospectively assess the anatomical concordance of electric source localizations of interictal discharges with the epileptogenic zone (EZ) estimated by stereo-electroencephalography (SEEG) according to different subgroups: the type of epilepsy, the presence of a structural MRI lesion, the aetiology and the depth of the EZ.

Methods: In a prospective multicentric observational study, we enrolled 85 consecutive patients undergoing pre-surgical SEEG investigation for focal drug-resistant epilepsy. Electric source imaging (ESI) was performed before SEEG. Source localizations were obtained from dipolar and distributed source methods. Anatomical concordance between ESI and EZ was defined according to 36 predefined sublobar regions. ESI was interpreted blinded to- and subsequently compared with SEEG estimated EZ.

Results: 74 patients were finally analyzed. 38 patients had temporal and 36 extra-temporal lobe epilepsy. MRI was positive in 52. 41 patients had malformation of cortical development (MCD), 33 had another or an unknown aetiology. EZ was medial in 27, lateral in 13, and medio-lateral in 34. In the overall cohort, ESI completely or partly localized the EZ in 85%: full concordance in 13 cases and partial concordance in 50 cases. The rate of ESI full concordance with EZ was significantly higher in (i) frontal lobe epilepsy (46%; p = 0.05), (ii) cases of negative MRI (36%; p = 0.01) and (iii) MCD (27%; p = 0.03). The rate of ESI full concordance with EZ was not statistically different according to the depth of the EZ.

Significance: We prospectively demonstrated that ESI more accurately estimated the EZ in subgroups of patients who are often the most difficult cases in epilepsy surgery: frontal lobe epilepsy, negative MRI and the presence of MCD.

Keywords: Electrical source imaging; Epilepsy surgery; High resolution EEG; Malformations of cortical development; Stereo-EEG.

Fig. 1

Consecutive steps of electrical source imaging analysis. Two different interpreters analyzed the results prior to the SEEG results. Within each spike subgroup, only reproducible and concordant ESI results were selected and classified according to 36 predefined sublobar regions. ESL, electrical source localization; ROI, region of interest; RD, rotating dipole; MD, moving dipole; IIDs, interictal discharges.

Fig. 2

Illustration of a patient with a negative MRI and a full sublobar concordance between ESL and EZ. (A) Hypothesis derived from long-term video-EEG recordings and ECC pointing the right dorsolateral prefrontal, the ventrolateral prefrontal, the lateral premotor, and the operculo-insula areas. (B) Negative MRI for structural lesions. (C) 64-Channel EEG recordings showed IID in channels F6, FC6, F4, FC4, C4, F2, FC2, C2 (monopolar montage, common average reference), correlating with sources localized in the depth of the right IFS and in the right MFG (ECD and sLORETA). These anatomic localizations corresponded to a dorsolateral prefrontal sublobar classification. (D) SEEG recordings showed ictal discharges occurring first in the right inferior frontal sulcus (IFS) (pink square). CT-MRI coregistration shows the localization of the depth electrodes of interest. The yellow electrode recorded the ac-tivity of IFS. The sublobar classification of EZ was consequently dorsolateral prefrontal. (E) Considering the third column (sub-lobar classification), ESI was fully concordant with SEEG. ESI allowed a restriction of ECC that was validated by SEEG. ECC, electroclinical correlations; IID, interictal discharge; 64 chEEG, 64 channel EEG; ESI, electrical source imaging; ECD, equivalent current dipole; sLORETA, standardized low-resolution brain electromagnetic tomography; SEEG, stereo-electroencephalography; IFS, inferior frontal sulcus; MFG, middle frontal gyrus; IFG, inferior frontal gyrus; OF, orbito frontal gyrus; EZ, epileptogenic zone; DMPref, dorsal medial prefrontal; DLPref, dorsal lateral prefrontal;L Prem, lateral premotor; VLPref, ventrolateral prefron-tal; DLPref, dorsolateral prefrontal; OI, operculo-insula.

Fig. 3

Rates of full concordance between the electrical source localizations and the epileptogenic zones according to the different subgroups in our population (n = 74): epilepsy type, MRI structural lesion and aetiology. The higher rates of full concordance was for frontal lobe epilepsy, negative MRI (non lesional epilepsy) and malformation cortical development. TLE, temporal lobe epilepsy; FLE, frontal lobe epilepsy; PE, posterior epilepsy; MFE, multifocal epilepsy; MCD, malformation cortical development.

Fig. 4

Illustration of a patient with a positive MRI and a partial sublobar concordance between ESL and EZ (IZ > EZ). (A) Hypothesis derived from long-term video-EEG recordings and ECC pointing the right mesial anterior and posterior temporal areas, the right lateral posterior temporal area and the mesial occipital area. (B) MRI showed a closed-lip schizencephaly (classified in MCD etiology) in T3, T4, T5 and O3, O4 and O5 gyri (lateral temporal area and the mesial and lateral occipital areas). (C) 64-Channel EEG recordings showed IID in channels FT10, P10, AF8, F8, FT8, T8 (monopolar montage, common average reference), correlating with sources localized in mesial and basal temporal areas (ECD) and lateral temporal area (sLORETA). These anatomic localizations corresponded to a mesial and lateral anterior temporal sublobar classification. (D) SEEG recordings showed ictal discharges occurring first in the right amygdala (amy) (pink doted-square). CT-MRI coregistration showed the localization of the depth electrodes of interest. The green electrode recorded the activity of amygdala. The sublobar classification of EZ was consequently mesial anterior temporal. (E) Considering the third column (sub-lobar classification), ESI was partially concordant with SEEG (IZ > EZ). This result could be explained by the common lateral anatomical diffusion of IIDs in temporal lobe epilepsy. ECC, electroclinical correlations; IID, interictal discharge; 64 chEEG, 64 channel EEG; ESI, electrical source imaging; ECD, equivalent current dipole; sLORETA, standardized low-resolution brain electromagnetic tomography; SEEG, stereo-electroencephalography; Amy, amydgala; Ant hipp, anterior hippocampus; Post hipp, posterior hippocampus; Fusi, fusiform gyrus; MAT, mesial anterior temporal; LAT, lateral anterior temporal; MPT, mesial posterior temporal; LPT, lateral posterior temporal; MO, mesial occipital; LO, lateral occipital.

Fig. 5

Illustration of a patient with a positive MRI and a sublobar disconcordance between ESL and EZ (IZ ≠ EZ). (A) Hypothesis derived from long-term video-EEG recordings and ECC pointing the right mesial anterior and posterior temporal areas. (B) MRI showed a right hippocampal sclerosis (classified in other etiologies) (mesial anterior temporal area). (C) 64-Channel EEG recordings showed IID in channels P8, PO8, PO4, O2 (monopolar montage, common average reference), correlating with sources localized in lateral posterior temporal area (ECD, sLORETA). (D) SEEG recordings showed ictal discharges occurring first in the right anterior hippocampus (ant hipp) (pink doted-square). CT-MRI coregistration showed the localization of the depth electrodes of interest. The orange electrode recorded the activity of anterior hippocampus. The sublobar classification of EZ was consequently mesial anterior temporal. (E) Considering the third column (sub-lobar classification), ESI was disconcordant with SEEG (IZ ≠ EZ). This result could be explained by non-visible IIDs in scalp EEG originating from the purely mesial part of the temporal lobe. ECC, electroclinical correlations; IID, interictal discharge; 64 chEEG, 64 channel EEG; ESI, electrical source imaging; ECD, equivalent current dipole; sLORETA, standardized low-resolution brain electromagnetic tomography; SEEG, stereo-electroencephalography; Amy, amydgala; Ant hipp, anterior hippocampus; Post hipp, posterior hippocampus; MAT, mesial anterior temporal; LAT, lateral anterior temporal; MPT, mesial posterior temporal; LPT, lateral posterior temporal.