Spatial distribution of interictal spikes fluctuates over time and localizes seizure onset

Erin C. Conrad; Samuel B. Tomlinson; Jeremy N. Wong; Kelly F. Oechsel; Russell T. Shinohara; Brian Litt; Kathryn A. Davis; Eric D. Marsh

doi:10.1093/brain/awz386

Spatial distribution of interictal spikes fluctuates over time and localizes seizure onset

Erin C. Conrad, Samuel B. Tomlinson, Jeremy N. Wong, Kelly F. Oechsel, Russell T. Shinohara, Brian Litt, Kathryn A. Davis, Eric D. Marsh^*

^*Corresponding author for this work

Pediatrics

Research output: Contribution to journal › Article › peer-review

61 Scopus citations

Abstract

The location of interictal spikes is used to aid surgical planning in patients with medically refractory epilepsy; however, their spatial and temporal dynamics are poorly understood. In this study, we analysed the spatial distribution of interictal spikes over time in 20 adult and paediatric patients (12 females, mean age = 34.5 years, range = 5–58) who underwent intracranial EEG evaluation for epilepsy surgery. Interictal spikes were detected in the 24 h surrounding each seizure and spikes were clustered based on spatial location. The temporal dynamics of spike spatial distribution were calculated for each patient and the effects of sleep and seizures on these dynamics were evaluated. Finally, spike location was assessed in relation to seizure onset location. We found that spike spatial distribution fluctuated significantly over time in 14/20 patients (with a significant aggregate effect across patients, Fisher’s method: P 5 0.001). A median of 12 sequential hours were required to capture 80% of the variability in spike spatial distribution. Sleep and postictal state affected the spike spatial distribution in 8/20 and 4/20 patients, respectively, with a significant aggregate effect (Fisher’s method: P 5 0.001 for each). There was no evidence of pre-ictal change in the spike spatial distribution for any patient or in aggregate (Fisher’s method: P = 0.99). The electrode with the highest spike frequency and the electrode with the largest area of downstream spike propagation both localized the seizure onset zone better than predicted by chance (Wilcoxon signed-rank test: P = 0.005 and P = 0.002, respectively). In conclusion, spikes localize seizure onset. However, temporal fluctuations in spike spatial distribution, particularly in relation to sleep and post-ictal state, can confound localization. An adequate duration of intracranial recording—ideally at least 12 sequential hours—capturing both sleep and wakefulness should be obtained to sufficiently sample the interictal network.

Original language	English (US)
Pages (from-to)	554-569
Number of pages	16
Journal	Brain
Volume	143
Issue number	2
DOIs	https://doi.org/10.1093/brain/awz386
State	Published - Feb 1 2020

Funding

E.C. received funding from NIH/NINDS (R25 NS065745). S.T. was supported by the University of Rochester CTSA award number TL1 TR002000 from the National Center for Advancing Translational Sciences of the National Institutes of Health. K.O. and J.W. have no funding to report. B.L., E.M., and K.D. received funding from NIH/ NINDS (R01 NS099348). E.M. additionally received funding from NIH/NICHD IDDRC (U54 HD086984). K.D. additionally received funding from NIH/NINDS (K23 NS073801) and the Thornton Foundation. B.L. additionally received funding from The Mirowski Family Foundation, and Neil and Barbara Smit. R.S. received funding from the NIH (R01MH112845 and R01NS060910), the National Multiple Sclerosis Society, and the Race to Erase MS.

Keywords

EEG
Epilepsy
Epilepsy surgery
Interictal spikes
Intracranial EEG

ASJC Scopus subject areas

Clinical Neurology

Access to Document

10.1093/brain/awz386

Cite this

@article{d186b567d9ed47a68a14fce5a3641703,

title = "Spatial distribution of interictal spikes fluctuates over time and localizes seizure onset",

abstract = "The location of interictal spikes is used to aid surgical planning in patients with medically refractory epilepsy; however, their spatial and temporal dynamics are poorly understood. In this study, we analysed the spatial distribution of interictal spikes over time in 20 adult and paediatric patients (12 females, mean age = 34.5 years, range = 5–58) who underwent intracranial EEG evaluation for epilepsy surgery. Interictal spikes were detected in the 24 h surrounding each seizure and spikes were clustered based on spatial location. The temporal dynamics of spike spatial distribution were calculated for each patient and the effects of sleep and seizures on these dynamics were evaluated. Finally, spike location was assessed in relation to seizure onset location. We found that spike spatial distribution fluctuated significantly over time in 14/20 patients (with a significant aggregate effect across patients, Fisher{\textquoteright}s method: P 5 0.001). A median of 12 sequential hours were required to capture 80% of the variability in spike spatial distribution. Sleep and postictal state affected the spike spatial distribution in 8/20 and 4/20 patients, respectively, with a significant aggregate effect (Fisher{\textquoteright}s method: P 5 0.001 for each). There was no evidence of pre-ictal change in the spike spatial distribution for any patient or in aggregate (Fisher{\textquoteright}s method: P = 0.99). The electrode with the highest spike frequency and the electrode with the largest area of downstream spike propagation both localized the seizure onset zone better than predicted by chance (Wilcoxon signed-rank test: P = 0.005 and P = 0.002, respectively). In conclusion, spikes localize seizure onset. However, temporal fluctuations in spike spatial distribution, particularly in relation to sleep and post-ictal state, can confound localization. An adequate duration of intracranial recording—ideally at least 12 sequential hours—capturing both sleep and wakefulness should be obtained to sufficiently sample the interictal network.",

keywords = "EEG, Epilepsy, Epilepsy surgery, Interictal spikes, Intracranial EEG",

author = "Conrad, {Erin C.} and Tomlinson, {Samuel B.} and Wong, {Jeremy N.} and Oechsel, {Kelly F.} and Shinohara, {Russell T.} and Brian Litt and Davis, {Kathryn A.} and Marsh, {Eric D.}",

year = "2020",

month = feb,

day = "1",

doi = "10.1093/brain/awz386",

language = "English (US)",

volume = "143",

pages = "554--569",

journal = "Brain",

issn = "0006-8950",

publisher = "Oxford University Press",

number = "2",

}

TY - JOUR

T1 - Spatial distribution of interictal spikes fluctuates over time and localizes seizure onset

AU - Conrad, Erin C.

AU - Tomlinson, Samuel B.

AU - Wong, Jeremy N.

AU - Oechsel, Kelly F.

AU - Shinohara, Russell T.

AU - Litt, Brian

AU - Davis, Kathryn A.

AU - Marsh, Eric D.

PY - 2020/2/1

Y1 - 2020/2/1

N2 - The location of interictal spikes is used to aid surgical planning in patients with medically refractory epilepsy; however, their spatial and temporal dynamics are poorly understood. In this study, we analysed the spatial distribution of interictal spikes over time in 20 adult and paediatric patients (12 females, mean age = 34.5 years, range = 5–58) who underwent intracranial EEG evaluation for epilepsy surgery. Interictal spikes were detected in the 24 h surrounding each seizure and spikes were clustered based on spatial location. The temporal dynamics of spike spatial distribution were calculated for each patient and the effects of sleep and seizures on these dynamics were evaluated. Finally, spike location was assessed in relation to seizure onset location. We found that spike spatial distribution fluctuated significantly over time in 14/20 patients (with a significant aggregate effect across patients, Fisher’s method: P 5 0.001). A median of 12 sequential hours were required to capture 80% of the variability in spike spatial distribution. Sleep and postictal state affected the spike spatial distribution in 8/20 and 4/20 patients, respectively, with a significant aggregate effect (Fisher’s method: P 5 0.001 for each). There was no evidence of pre-ictal change in the spike spatial distribution for any patient or in aggregate (Fisher’s method: P = 0.99). The electrode with the highest spike frequency and the electrode with the largest area of downstream spike propagation both localized the seizure onset zone better than predicted by chance (Wilcoxon signed-rank test: P = 0.005 and P = 0.002, respectively). In conclusion, spikes localize seizure onset. However, temporal fluctuations in spike spatial distribution, particularly in relation to sleep and post-ictal state, can confound localization. An adequate duration of intracranial recording—ideally at least 12 sequential hours—capturing both sleep and wakefulness should be obtained to sufficiently sample the interictal network.

AB - The location of interictal spikes is used to aid surgical planning in patients with medically refractory epilepsy; however, their spatial and temporal dynamics are poorly understood. In this study, we analysed the spatial distribution of interictal spikes over time in 20 adult and paediatric patients (12 females, mean age = 34.5 years, range = 5–58) who underwent intracranial EEG evaluation for epilepsy surgery. Interictal spikes were detected in the 24 h surrounding each seizure and spikes were clustered based on spatial location. The temporal dynamics of spike spatial distribution were calculated for each patient and the effects of sleep and seizures on these dynamics were evaluated. Finally, spike location was assessed in relation to seizure onset location. We found that spike spatial distribution fluctuated significantly over time in 14/20 patients (with a significant aggregate effect across patients, Fisher’s method: P 5 0.001). A median of 12 sequential hours were required to capture 80% of the variability in spike spatial distribution. Sleep and postictal state affected the spike spatial distribution in 8/20 and 4/20 patients, respectively, with a significant aggregate effect (Fisher’s method: P 5 0.001 for each). There was no evidence of pre-ictal change in the spike spatial distribution for any patient or in aggregate (Fisher’s method: P = 0.99). The electrode with the highest spike frequency and the electrode with the largest area of downstream spike propagation both localized the seizure onset zone better than predicted by chance (Wilcoxon signed-rank test: P = 0.005 and P = 0.002, respectively). In conclusion, spikes localize seizure onset. However, temporal fluctuations in spike spatial distribution, particularly in relation to sleep and post-ictal state, can confound localization. An adequate duration of intracranial recording—ideally at least 12 sequential hours—capturing both sleep and wakefulness should be obtained to sufficiently sample the interictal network.

KW - EEG

KW - Epilepsy

KW - Epilepsy surgery

KW - Interictal spikes

KW - Intracranial EEG

UR - http://www.scopus.com/inward/record.url?scp=85079250074&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85079250074&partnerID=8YFLogxK

U2 - 10.1093/brain/awz386

DO - 10.1093/brain/awz386

M3 - Article

C2 - 31860064

AN - SCOPUS:85079250074

SN - 0006-8950

VL - 143

SP - 554

EP - 569

JO - Brain

JF - Brain

IS - 2

ER -

Spatial distribution of interictal spikes fluctuates over time and localizes seizure onset

Abstract

Funding

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this