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February 16, 2021; 96 (7) Article

Spatiotemporal Patterns of High-Frequency Activity (80–170 Hz) in Long-Term Intracranial EEG

View ORCID ProfileZhuying Chen, View ORCID ProfileDavid B. Grayden, View ORCID ProfileAnthony N. Burkitt, Udaya Seneviratne, View ORCID ProfileWendyl J. D'Souza, Chris French, Philippa J. Karoly, Katrina Dell, Kent Leyde, Mark J. Cook, View ORCID ProfileMatias I. Maturana
First published December 22, 2020, DOI: https://doi.org/10.1212/WNL.0000000000011408
Zhuying Chen
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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David B. Grayden
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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Anthony N. Burkitt
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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Udaya Seneviratne
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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Wendyl J. D'Souza
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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Chris French
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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Philippa J. Karoly
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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Katrina Dell
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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Kent Leyde
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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Mark J. Cook
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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Matias I. Maturana
From the Department of Biomedical Engineering (Z.C., D.B.G., A.N.B., P.J.K, M.J.C.), and Department of Medicine (Z.C., D.B.G., U.S., W.J.D., K.D., M.J.C., M.I.M.), St Vincent's Hospital, Department of Medicine (C.F.), Royal Melbourne Hospital, and Graeme Clark Institute (P.J.K., M.J.C.), The University of Melbourne, VIC, Australia; Cadence Neuroscience (K.L.), Redmond, WA; and 6 Seer Medical (M.I.M.), Melbourne, VIC, Australia.
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Citation
Spatiotemporal Patterns of High-Frequency Activity (80–170 Hz) in Long-Term Intracranial EEG
Zhuying Chen, David B. Grayden, Anthony N. Burkitt, Udaya Seneviratne, Wendyl J. D'Souza, Chris French, Philippa J. Karoly, Katrina Dell, Kent Leyde, Mark J. Cook, Matias I. Maturana
Neurology Feb 2021, 96 (7) e1070-e1081; DOI: 10.1212/WNL.0000000000011408

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Abstract

Objective To determine the utility of high-frequency activity (HFA) and epileptiform spikes as biomarkers for epilepsy, we examined the variability in their rates and locations using long-term ambulatory intracranial EEG (iEEG) recordings.

Methods This study used continuous iEEG recordings obtained over an average of 1.4 years from 15 patients with drug-resistant focal epilepsy. HFA was defined as 80- to 170-Hz events with amplitudes clearly larger than the background, which was automatically detected with a custom algorithm. The automatically detected HFA was compared with visually annotated high-frequency oscillations (HFOs). The variations of HFA rates were compared with spikes and seizures on patient-specific and electrode-specific bases.

Results HFA included manually annotated HFOs and high-amplitude events occurring in the 80- to 170-Hz range without observable oscillatory behavior. HFA and spike rates had high amounts of intrapatient and interpatient variability. Rates of HFA and spikes had large variability after electrode implantation in most of the patients. Locations of HFA and spikes varied up to weeks in more than one-third of the patients. Both HFA and spike rates showed strong circadian rhythms in all patients, and some also showed multiday cycles. Furthermore, the circadian patterns of HFA and spike rates had patient-specific correlations with seizures, which tended to vary across electrodes.

Conclusion Analysis of HFA and epileptiform spikes should consider postimplantation variability. HFA and epileptiform spikes, like seizures, show circadian rhythms. However, the circadian profiles can vary spatially within patients, and their correlations to seizures are patient-specific.

Glossary

ACF=
autocorrelation function;
CV=
coefficient of variation;
EZ=
epileptogenic zone;
HFA=
high-frequency activity;
HFO=
high-frequency oscillation;
iEEG=
intracranial EEG;
SOZ=
seizure onset zone

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Received March 26, 2020.
  • Accepted in final form October 15, 2020.
  • © 2020 American Academy of Neurology
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