Disconnection of the pathological connectome for multifocal epilepsy surgery

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OBJECTIVE

Recent neuroimaging studies suggest that intractable epilepsy involves pathological functional networks as well as strong epileptogenic foci. Combining cortico-cortical evoked potential (CCEP) recording and tractography is a useful strategy for mapping functional connectivity in normal and pathological networks. In this study, the authors sought to demonstrate the efficacy of preoperative combined CCEP recording, high gamma activity (HGA) mapping, and tractography for surgical planning, and of intraoperative CCEP measures for confirmation of selective pathological network disconnection.

METHODS

The authors treated 4 cases of intractable epilepsy. Diffusion tensor imaging–based tractography data were acquired before the first surgery for subdural grid implantation. HGA and CCEP investigations were done after the first surgery, before the second surgery was performed to resect epileptogenic foci, with continuous CCEP monitoring during resection.

RESULTS

All 4 patients in this report had measurable pathological CCEPs. The mean negative peak-1 latency of normal CCEPs related to language functions was 22.2 ± 3.5 msec, whereas pathological CCEP latencies varied between 18.1 and 22.4 msec. Pathological CCEPs diminished after complete disconnection in all cases. At last follow-up, all of the patients were in long-term postoperative seizure-free status, although 1 patient still suffered from visual aura every other month.

CONCLUSIONS

Combined CCEP measurement, HGA mapping, and tractography greatly facilitated targeted disconnection of pathological networks in this study. Although CCEP recording requires technical expertise, it allows for assessment of pathological network involvement in intractable epilepsy and may improve seizure outcome.

ABBREVIATIONS AED = antiepileptic drug; AF = arcuate fasciculus; CCEP = cortico-cortical evoked potential; CPS = complex partial seizure; DTI = diffusion tensor imaging; ECoG = electrocorticography; ECS = electrocortical stimulation; EEG = electroencephalography; FC = functional connectivity; fMRI = functional MRI; GCS = generalized convulsive seizure; HGA = high gamma activity.

Article Information

Correspondence Kyousuke Kamada, Department of Neurosurgery, Asahikawa Medical University, 2-1, Midorigaoka-Higashi, Asahikawa, Hokkaido, 078-8510, Japan. email: kamady-k@umin.ac.jp.

INCLUDE WHEN CITING Published online December 22, 2017; DOI: 10.3171/2017.6.JNS17452.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Case 1. A: Electrocorticogram showing 2 seizure-onset zones in anterior frontal (red circles) and middle temporal (blue circles) regions. In most seizure events, the frontal activity frequently spread to the lateral temporal cortex. B: Axial MR image demonstrating no pathological findings. C: Frontal (red) and temporal (blue) foci marked on the electrode templates. Figure is available in color online only.

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    Case 1. Normal and pathological CCEP results. A: Blue and red electrode pairs indicate stimulus points and blue and red squares show recording locations of pathological and normal CCEPs, respectively. Note that each first component (N1) waveform is approximately 24 msec after the stimuli. B: Pathological CCEPs peaking at 24 msec (arrow). C: Normal CCEPs appearing at 24 msec poststimulus (arrow). D: Tractography revealing fiber connections between the frontal and temporal regions via uncinate fascicles. Figure is available in color online only.

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    Case 1. A: Dissection of the sylvian fissure to expose the limen insulae while keeping the electrode position stable to monitor CCEPs. B: Removal of the anterior roof of the inferior temporal horn, preserving the ependymal layer (arrow). C: Operation sketch showing electrode grids, the shifted sylvian vein, and exposed ependymal layer (arrow). Copyright Kyousuke Kamada. Published with permission. D: Postoperative tractography showing complete disconnection of the uncinate fascicles. Figure is available in color online only.

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    Case 1. A: Intraoperative normal (blue squares) and pathological (red squares) CCEP results. B: Obvious pathological CCEP (red lines) before resection. C: CCEPs, which diminished after disconnection. D: Normal CCEPs appearing on the temporal regions. E: Normal CCEPs were preserved after disconnection of the pathological network. F and G: Postoperative MR images showing removal of the left frontal area (F, arrow) and a small incision in the left temporal tip (G, arrow). Figure is available in color online only.

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    Case 2. A: Axial MR image demonstrating no abnormal structures. B: Ictal EEG showing 3-Hz spikes and waves and multiple spikes. C: ECoG from the bifrontal region that did not indicate the lesional hemisphere of onset. Channels of right (blue) and left (red) hemispheres showed frequent spikes and waves. Figure is available in color online only.

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    Case 2. A: Pathological CCEPs recorded from the left frontal lobe (red square) in response to stimulation of the right epileptogenic foci (red channels 8, 9, 10, 13, 14, 15, 18, 19, and 20). B: CCEP deflections (red square) over the right frontal channels. The CCEPs in this case consisted of 2 obvious deflections. Figure is available in color online only.

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    Case 2. A: Dynamic changes in CCEP according to callosotomy. The resection procedure was performed from points 1 to 5 (arrows, left to right). Pathological CCEPs immediately diminished upon resection of point 3 and disappeared completely upon resection of point 5. B: Operation sketch showing the marked posterior border of the corpus callosum (blue dot and arrow) by neuronavigation. The callosotomy started from the posterior border to the anterior tip, exposing the cavity of the septum pellucidum (arrow). Copyright Kyousuke Kamada. Published with permission. C: Tractography between CCEP responsive areas in bilateral hemispheres. D and E: Postoperative MR images demonstrating anterior corpus callosotomy (D) and biopsy on the left frontal lobe (E). Figure is available in color online only.

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    Case 3. A: Electrocorticogram showing seizure-onset zones (channels 125–132) in the temporal base. B: Coronal MR image demonstrating no abnormality. C: Posterior 4-channel grid (green circle) detected strong face-recognition responses. Figure is available in color online only.

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    Case 3. A: Electrocorticogram showing electrode configurations. Electrical stimulation (red circle pair) evoked pathological CCEPs on the superior temporal region (channels 97 and 98). B: The stimulation (red circle pair) on the temporal lobe widely evoked pathological CCEPs (channels 128–132). C: Postoperative axial MR image showing the minimum resection of the temporal lobe on the basis of the mapping results. D: Postoperative coronal MR image showing complete resection of the mesial and lateral part of the right temporal region. Figure is available in color online only.

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    Case 4. A: Axial MR image demonstrating no pathological findings on any sequences. B: Pathological CCEPs recorded from the right temporal base (red circles) by stimulation to the lateral temporal lobe (channels 145, 148, 149, and 150, which are marked by filled red ovals). C: Evoked CCEPs on 4 channels of the temporal base. D and E: Postoperative MR images revealing complete and extensive resection of the temporal lobe on the basis of pathological CCEP locations. Figure is available in color online only.

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