Superior Frontal Sulcus Focal Cortical Dysplasia Type II: An MRI, PET, and Quantified SEEG Study

Abstract

Purpose: The superior frontal sulcus (SFS), located in the prefrontal and premotor cortex, is considered as one of the common locations of focal cortical dysplasia (FCD). However, the characteristics of seizures arising from this area are incompletely known. The primary purpose of this study was to investigate the clinical features and the epileptic networks of seizures originating from the SFS. Methods: We included seventeen patients with type II FCD within the SFS. SFS was identified both visually and automatically. Semiological features were evaluated and grouped. Interictal 18FDG-PET imaging in all patients was compared to controls using statistical parametric mapping (SPM-PET). In those subjects with stereoelectroencephalography (SEEG), two different quantitative intracranial electroencephalography analyses were applied. Finally, the locations of the SFS-related hypometabolic regions and epileptogenic zones (EZs) were transformed into standard space for group analysis. Results: We identified two semiological groups. Group 1 (9/17) showed elementary motor signs (head version and tonic posturing), while group 2 (8/17) exhibited complex motor behavior (fear, hypermotor, and ictal pouting). Based on SPM-PET, an SFS-supplementary motor area (SMA) epileptic propagation network was found in group 1, and an SFS-middle cingulate cortex (MCC)-pregenual anterior cingulate cortex (pACC) propagation network was discovered in group 2. Intracranial EEG analysis suggested similar affected structures with high epileptogenicity. The SFS-related hypometabolic regions and EZs in these groups showed a posterior-anterior spatial relationship. Conclusions: Even though originating from the spatially restricted cortex, SFS seizures can be divided into two groups based on semiological features. The SFS-SMA and SFS-MCC-pACC epileptic propagation networks may play pivotal roles in the generation of different semiologies. The posterior-anterior spatial relationship of both hypometabolic regions and EZs provides potentially useful information for distinguishing different types of SFS seizures and surgical evaluation.

Keywords: epileptic network; epileptogenic zone; focal cortical dysplasia; semiology; superior frontal sulcus.

Figure 1

Histologically proven FCD type II in the SFS of 17 patients. The upper and lower rows are group 1 (1–9) and group 2 (10–17), and the asterisks indicate cases with SEEG evaluation. For each patient, two coregistration images (MRI-PET and MRI-automatically identified sulci, Morphologist 2015, BrainVISA) with an identical axial position are displayed. The intersection of the red line demonstrates the location of the electrode contact, which is considered to be the seizure onset (1–4, 10–15) or the most apparent lesion (5–9, 16, 17). The green sulcus in the frontal lobe is the automatically recognized SFS.

Figure 2

The metabolism of SFS epilepsy patients compared to that of healthy controls. Brain areas with decreased glucose metabolism are superimposed on the MNI152 template (P < 0.001). (A–C) Significant hypometabolism in the SFS, SMA, precentral gyrus in group 1. (D–H) Significant hypometabolism in the SFS, MCC, pACC, caudate, and putamen in group 2. The color scale indicates T scores. Note that PET images in patients with right-sided lesions are all horizontally flipped to the left side.

Figure 3

High epileptogenic structures in 2 groups. (A) SEEG recording of one seizure of Case 3 in group 1. (B) EI values of the same seizure event presents an increased energy ratio at the ictal onset (from blue to yellow scale) and the detection parameters (circle, alarm time; cross, detection time) in each channel. This map showed that SFS, SMA, and MCC were highly epileptogenic. (C) SEEG recording of one seizure of Case 13 in group 2. (D) EI values map of the same seizure attack, in which SFS, MCC, and pACC were highly epileptogenic. (E) Mean EI value of the SFS, pACC, MCC, and SMA in each group. The arbitrary cut-off value used to identify the extended EZ was set at 0.3, as previously described (18). (G_Re, gyrus rectus; MFG, middle frontal gyrus; Pars_O, pars opercularis; PreCG, pre-central gyrus, rACC, rostral anterior cingulate cortex, SFG, superior frontal gyrus).

Figure 4

Electrodes position map and averaged epileptogenicity map. (A) Blue, green, red, and cyan dots show actual SEEG recording contacts from cases 1, 2, 3, and 4 in group 1. (B–D) EM averaged over the patients in group 1. (E) Blue, green, red, cyan, and pink dots indicate actual SEEG recording contacts from cases 10, 11, 12, 13, and 15 in group 2. (F–H) EM averaged over the patients in group 2. The significance map calculated based on the power of high frequencies at seizure onset was corrected by FWE (p < 0.05). The color scale indicates T scores. Electrodes and maps are drawn over the MNI152 atlas. Note that the epileptogenicity maps in patients with right-sided lesions are all horizontally flipped to the left side.

Figure 5

Glass brain rendering of the SFS-related hypometabolic areas (FDR-cor < 0.05) and highly epileptogenic regions (T-value > 25). (A) Significantly hypometabolic areas compared with the control and corresponding centroids. (B) Highly epileptogenic regions and corresponding centroids. Blue represents group 1, and orange represents group 2.