TY - JOUR
T1 - Dynamic tractography-based localization of spike sources and animation of spike propagations
AU - Mitsuhashi, Takumi
AU - Sonoda, Masaki
AU - Sakakura, Kazuki
AU - Jeong, Jeong Won
AU - Luat, Aimee F.
AU - Sood, Sandeep
AU - Asano, Eishi
N1 - Funding Information:
We are grateful to Karin Halsey, BS, REEGT, and Jamie MacDougall, RN, BSN, CPN at Children's Hospital of Michigan for collaboration and assistance in performing the studies described above. This work was supported by the National Institutes of Health (NS064033 to E.A.; NS089659 to J.W.J.) and Japan Science and Technology Agency CREST (JPMJCR1784 to T.M.).
Funding Information:
We are grateful to Karin Halsey, BS, REEGT, and Jamie MacDougall, RN, BSN, CPN at Children's Hospital of Michigan for collaboration and assistance in performing the studies described above. This work was supported by the National Institutes of Health (NS064033 to E.A.; NS089659 to J.W.J.) and Japan Science and Technology Agency CREST (JPMJCR1784 to T.M.).
Publisher Copyright:
© 2021 International League Against Epilepsy
PY - 2021/10
Y1 - 2021/10
N2 - 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.
AB - 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.
KW - diffusion tensor imaging
KW - electrocorticography
KW - epileptic network
KW - interictal epileptiform activity
KW - irritative zone
KW - pediatric epilepsy surgery
UR - http://www.scopus.com/inward/record.url?scp=85111487957&partnerID=8YFLogxK
U2 - 10.1111/epi.17025
DO - 10.1111/epi.17025
M3 - Article
AN - SCOPUS:85111487957
SN - 0013-9580
VL - 62
SP - 2372
EP - 2384
JO - Epilepsia
JF - Epilepsia
IS - 10
ER -