Clinical and anatomical analysis of the epileptogenic spread patterns in focal cortical dysplasia patients

Abstract

Background: Focal cortical dysplasia (FCD) is one of the main causes of intractable epilepsy, which is amendable by surgery. During the surgical management of FCD, the understanding of its epileptogenic foci, interconnections, and spreading pathways is crucial for attaining a good postoperative seizure free outcome.

Methods: We retrospectively evaluated 54 FCD patients operated in Federal Center of Neurosurgery, Tyumen, Russia. The electroencephalogram findings were correlated to the involved brain anatomical areas. Subsequently, we analyzed the main white matter tracts implicated during the epileptogenic spreading in some representative cases. We prepared 10 human hemispheres using Klinger's method and dissected them through the fiber dissection technique.

Results: The clinical results were displayed and the main white matter tracts implicated in the seizure spread were described in 10 patients. Respective FCD foci, interconnections, and ectopic epileptogenic areas in each patient were discussed.

Conclusion: A strong understanding of the main implicated tracts in epileptogenic spread in FCD patient remains cardinal for neurosurgeons dealing with epilepsy. To achieve meaningful seizure freedom, despite the focal lesion resection, the interconnections and tracts should be understood and somehow disconnected to stop the spreading.

Keywords: Epilepsy; Focal dysplasia; Seizure spreading; White matter tract.

Figure 1:

Correlation between electroencephalogram electrodes and cortical anatomy. Superior and lateral view of the brain surface (left side). Fp1: L Superior frontal gyrus, F3: L Middle frontal gyrus, F7: L Inferior frontal gyrus (TP), C3: L Precentral/Postcentral gyrus, T3: L Middle/Superior temporal gyrus*, T5: L Middle temporal gyrus, P3: L Angular gyrus, O1: L Middle occipital gyrus, Fz: Supplementary motor area, Cz: Paracentral lobe, Fp2: R Middle/ Superior frontal G, F4: R Middle Frontal gyrus, F8: R Inferior Frontal gyrus (TP), C4: R Precentral/Postcentral gyrus, T4: R Middle/superior temporal gyrus*, T6: R Middle temporal G **, P4: R Angular gyrus, O2: R Middle occipital gyrus, Pz: Superior parietal gyrus, L: Left, R: Right, *: Rostro-caudal location-posterior to rolandic fissure; **: Caudal to termination of sylvian fissure/posterior part. TP: Triangular part

Figure 2:

Exoscope-guided cadaveric dissection, with 3D camera.

Figure 3:

(a) Preoperative and postoperative maganetic resonance imaging (MRI) in a patient with focal cortical dysplasia (FCD) located in the left middle frontal gyrus (MFG). (b) Lateral view of the left frontal lobe, after dissecting of the U-fibers around the MFG. The epileptogenic zones (EZ) spread from the MFG to the inferior frontal gyrus and superior frontal gyrus through the U-fibers. Yellow: primary FCD EZ, Red: ectopic EZ, Discontinuous line: U-fibers. (c) Lateral view of the left frontal lobe, after dissecting the U-fibers around the MFG. u: U-fibers. (d) Lateral view of the left hemisphere, after removing the gray matter and U-fibers, exposing the ILF, which connects the EZ located in the occipital pole with the superior and medial temporal gyrus. Yellow: primary FCD EZ, Red: ectopic EZ. Discontinuous line: ILF. (e) Lateral view of the left hemisphere, after dissecting the ILF. ILF: Inferior Longitudinal Fascicle. (f) Tractography of the ILF.

Figure 4:

(a) Left frontal lobe after removal of the U-Fibers and part of SLF-II in the middle frontal gyrus, exposing the Aslant tract, which connects the supplementary motor area (SMA) and pre-SMA in the superior frontal gyrus to the pars opercularis and pars triangularis of the posterior inferior frontal gyrus. The inferior part of the SLF-II, which runs lateral to the aslant tract, is partially conserved. Yellow: primary focal cortical dysplasia epileptogenic zones (EZ), Red: ectopic EZ, Discontinuous black line: Aslant Tract, Discontinuous blue line: SLFII. (b) Left frontal lobe, exposing the Aslant tract. SFG: Superior frontal gyrus, IFG: Inferior frontal gyrus. (c) Tractography of the Aslant Tract. (d) Lateral view of the right hemisphere, after removal U-fibers of the middle and inferior frontal gyrus, inferior parietal lobe and the posterior part of the superior and middle temporal gyrus, exposing the SLF-II (originates in the angular gyrus and anterior intraparietal sulcus and terminates in the posterior regions of middle and superior frontal gyrus), SLF-III (joins the intraparietal sulcus and inferior parietal lobule to the inferior frontal gyrus), and the AF (connects Broca’s Area and Wernicke’s Area through frontal, parietal, and temporal Lobes). SLF-II: Superior longitudinal fascicle segment II, SLF-III: Superior longitudinal fascicle segment III, AF: Arcuate Fascicle. (e) Right frontal lobe, exposing the SLF-II, SLF-III, and the AF. (f) Tractography of the SLF-II and AF.

Figure 5:

(a) Lateral view of the right temporal and frontal poles, after exposing the uncinate fascicle, which connects the orbitofrontal cortex to the anterior temporal lobe. Yellow: primary focal cortical dysplasia epileptogenic zones (EZ), Red: ectopic EZ, Discontinuous line: Uncinate fascicle. (b) Lateral view of the right frontal and temporal lobes, after the dissection of the Uncinate Fascicle. tp: Temporal pole, unc: Uncinate Fascicle, f.orb: Orbitofrontal cortex. (c) Tractography of the uncinate fascicle. (d) Lateral view of the right hemisphere after dissection of U-fibers of the frontal, temporal, parietal, and occipital lobes, insula and part of the extreme capsule, exposing the inferior frontal occipital fasciculus (IFOF), which runs from the prefrontal area and orbitofrontal cortex directly to the parietal, occipital and postero-lateral temporal lobes. In the same picture, the right Uncinate Fascicle and Anterior Commissure can be appreciated. Yellow: primary focal cortical dysplasia EZ, Red: ectopic EZ, Discontinuous blue line: Anterior Commissure, Discontinuous black line: IFOF, Discontinuous white line: Uncinate fascicle. (e) Lateral view of the right hemisphere, exposing IFOF, uncinate fascicle, and anterior commissure. (f) Tractography of the IFOF.

Figure 6:

(a) Superior view of both hemispheres, after removal of the cingulum and the U-fibers of the medial surfaces, exposing the dorsal radiations of the corpus callosum (CC), the forceps major or posterior radiations and the forceps minor or anterior radiations. Yellow: Primary focal cortical dysplasia epileptogenic zones (EZ), Red: ectopic EZ, Discontinuous line: Commissural fibers of the CC, fm: Forceps Minor, fM: Forceps Major. (b) Superior view of both frontal lobes, after removal of the cingulum and the U-fibers of the medial surfaces, exposing the forceps minor or anterior radiations of the CC, which connects the medial surface and the basal region of both hemispheres. fm: Forceps minor, Superior frontal gyrus. (c) Superior view of both hemispheres, after removal of the cingulum and the U-fibers of the medial surfaces, exposing the dorsal radiations of the CC, the forceps major or posterior radiations and the forceps minor or anterior radiations. (d) Tractography of the CC. SFG: Superior frontal gyrus

Figure 7:

(a) Lateral view of the left hemisphere after the removal of the U-fibers, superior longitudinal fasciculus, and arcuate fascicle, exposing the mdLF. The mdLF connects the superior temporal gyrus with the parietal and occipital lobes. Yellow: primary focal cortical dysplasia EZ; Red: ectopic EZ; Discontinuous line: mdLF. (b) Tractography of the mdLF. (c) Lateral view of the left hemisphere, after dissection of the mdLF. mdLF: Middle Longitudinal Fasciculus, SPL: Superior Parietal Lobe, IFG: Inferior frontal gyrus, PreC: Precental gyrus, PostC: Postcentral gyrus, SMG: Supramarginal Gyrus, EZ: Epileptogenic zones, and SLF: Superior longitudinal fasciculus.