Dynamic tractography‐based localization of spike sources and animation of spike propagations

• Published in: Epilepsia (Copenhagen) Vol. 62; no. 10; pp. 2372 - 2384
• Main Authors: Mitsuhashi, Takumi, Sonoda, Masaki, Sakakura, Kazuki, Jeong, Jeong‐Won, Luat, Aimee F., Sood, Sandeep, Asano, Eishi
• Format: Journal Article
• Language: English
• Published: United States Wiley Subscription Services, Inc 01-10-2021
• Subjects: Cross-Sectional Studies; diffusion tensor imaging; Drug Resistant Epilepsy - diagnostic imaging; Drug Resistant Epilepsy - surgery; EEG; electrocorticography; Electrocorticography - methods; Electroencephalography - methods; Epilepsy; Epilepsy - diagnostic imaging; Epilepsy - surgery; Epilepsy, Temporal Lobe - diagnostic imaging; Epilepsy, Temporal Lobe - surgery; epileptic network; Humans; interictal epileptiform activity; irritative zone; Latency; Localization; Magnetic resonance imaging; Neocortex; Patients; pediatric epilepsy surgery; Seizures; Substantia alba; Temporal lobe; Velocity; diffusion tensor imaging; electrocorticography; pediatric epilepsy surgery; irritative zone; interictal epileptiform activity; epileptic network
• ISSN: 0013-9580; 1528-1167
• DOI: 10.1111/epi.17025

Objective
This study was undertaken to build and validate a novel dynamic tractography‐based model for localizing interictal spike sources and visualizing monosynaptic spike propagations through the white matter.
Methods
This cross‐sectional study investigated 1900 spike events recorded in 19 patients with drug‐resistant temporal lobe epilepsy (TLE) who underwent extraoperative intracranial electroencephalography (iEEG) and resective surgery. Twelve patients had mesial TLE (mTLE) without a magnetic resonance imaging‐visible mass lesion. The remaining seven had a mass lesion in the temporal lobe neocortex. We identified the leading and lagging sites, defined as those initially and subsequently (but within ≤50 ms) showing spike‐related augmentation of broadband iEEG activity. In each patient, we estimated the sources of 100 spike discharges using the latencies at given electrode sites and diffusion‐weighted imaging‐based streamline length measures. We determined whether the spatial relationship between the estimated spike sources and resection was associated with postoperative seizure outcomes. We generated videos presenting the spatiotemporal change of spike‐related fiber activation sites by estimating the propagation velocity using the streamline length and spike latency measures.
Results
The spike propagation velocity from the source was 1.03 mm/ms on average (95% confidence interval = .91–1.15) across 133 tracts noted in the 19 patients. The estimated spike sources in mTLE patients with International League Against Epilepsy Class 1 outcome were more likely to be in the resected area (83.9% vs. 72.3%, φ = .137, p < .001) and in the medial temporal lobe region (80.5% vs. 72.5%, φ = .090, p = .002) than those associated with the Class ≥2 outcomes. The resulting video successfully animated spike propagations, which were confined within the temporal lobe in mTLE but involved extratemporal lobe areas in lesional TLE.
Significance
We have, for the first time, provided dynamic tractography visualizing the spatiotemporal profiles of rapid propagations of interictal spikes through the white matter. Dynamic tractography has the potential to serve as a unique epilepsy biomarker.