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January 14, 2015

Gamma oscillations precede interictal epileptiform spikes in the seizure onset zone

Liankun Ren, MD, Michal T. Kucewicz, PhD, Jan Cimbalnik, MSc, Joseph Y. Matsumoto, MD, Benjamin H. Brinkmann, PhD, Wei Hu, MD, PhD, W. Richard Marsh, MD, Fredric B. Meyer, MD, S. Matthew Stead, MD, PhD, and Gregory A. Worrell, MD, PhDAuthors Info & Affiliations
February 10, 2015 issue
84 (6) 602-608
https://doi.org/10.1212/WNL.0000000000001234
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Abstract

Objective:

To investigate the generation, spectral characteristics, and potential clinical significance of brain activity preceding interictal epileptiform spike discharges (IEDs) recorded with intracranial EEG.

Methods:

Seventeen adult patients with drug-resistant temporal lobe epilepsy were implanted with intracranial electrodes as part of their evaluation for epilepsy surgery. IEDs detected on clinical macro- and research microelectrodes were analyzed using time-frequency spectral analysis.

Results:

Gamma frequency oscillations (30–100 Hz) often preceded IEDs in spatially confined brain areas. The gamma-IEDs were consistently observed 35 to 190 milliseconds before the epileptiform spike waveforms on individual macro- and microelectrodes. The gamma oscillations associated with IEDs had longer duration (p < 0.001) and slightly higher frequency (p = 0.045) when recorded on microelectrodes compared with clinical macroelectrodes. Although gamma-IEDs comprised only a subset of IEDs, they were strongly associated with electrodes in the seizure onset zone (SOZ) compared with the surrounding brain regions (p = 0.004), in sharp contrast to IEDs without preceding gamma oscillations that were often also detected outside of the SOZ. Similar to prior studies, isolated pathologic high-frequency oscillations in the gamma (30–100 Hz) and higher (100–600 Hz) frequency range, not associated with an IED, were also found to be associated with SOZ.

Conclusions:

The occurrence of locally generated gamma oscillations preceding IEDs suggests a mechanistic role for gamma in pathologic network activity generating IEDs. The results show a strong association between SOZ and gamma-IEDs. The potential clinical application of gamma-IEDs for mapping pathologic brain regions is intriguing, but will require future prospective studies.

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Information & Authors

Information

Published In

Neurology®
Volume 84 • Number 6 • February 10, 2015
Pages: 602-608
PubMed: 25589669

Copyright

© 2015 American Academy of Neurology.

Publication History

Received: May 29, 2014
Accepted: October 16, 2014
Published online: January 14, 2015
Published in print: February 10, 2015

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Disclosure

The authors report no disclosures relevant to the manuscript. Go to Neurology.org for full disclosures.

Study Funding

NIH R01-NS63039 and U24-63930; National Natural Science Foundation of China 81271447 and 81271448; European Regional Development Fund, Project FNUSA-ICRC CZ.1.05/1.1.00/02.0123.

Authors

Affiliations & Disclosures

Liankun Ren, MD*
From the Mayo Systems Electrophysiology Laboratory, Department of Neurology (L.R., M.T.K., J.C., J.Y.M., B.H.B., W.H., S.M.S., G.A.W.), and Department of Neurosurgery (W.R.M., F.B.M.), Mayo Clinic, Rochester, MN; Department of Neurology (L.R.), China-Japan Friendship Hospital, Beijing, China; and International Clinical Research Center (J.C.), St. Anne's University Hospital, Brno, Czech Republic.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NationalNatural Science Foundation of China: 81271447 and 81271448; Liankun Ren, 01/01/2013-12/31/2014
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
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Michal T. Kucewicz, PhD*
From the Mayo Systems Electrophysiology Laboratory, Department of Neurology (L.R., M.T.K., J.C., J.Y.M., B.H.B., W.H., S.M.S., G.A.W.), and Department of Neurosurgery (W.R.M., F.B.M.), Mayo Clinic, Rochester, MN; Department of Neurology (L.R.), China-Japan Friendship Hospital, Beijing, China; and International Clinical Research Center (J.C.), St. Anne's University Hospital, Brno, Czech Republic.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Jan Cimbalnik, MSc
From the Mayo Systems Electrophysiology Laboratory, Department of Neurology (L.R., M.T.K., J.C., J.Y.M., B.H.B., W.H., S.M.S., G.A.W.), and Department of Neurosurgery (W.R.M., F.B.M.), Mayo Clinic, Rochester, MN; Department of Neurology (L.R.), China-Japan Friendship Hospital, Beijing, China; and International Clinical Research Center (J.C.), St. Anne's University Hospital, Brno, Czech Republic.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Joseph Y. Matsumoto, MD
From the Mayo Systems Electrophysiology Laboratory, Department of Neurology (L.R., M.T.K., J.C., J.Y.M., B.H.B., W.H., S.M.S., G.A.W.), and Department of Neurosurgery (W.R.M., F.B.M.), Mayo Clinic, Rochester, MN; Department of Neurology (L.R.), China-Japan Friendship Hospital, Beijing, China; and International Clinical Research Center (J.C.), St. Anne's University Hospital, Brno, Czech Republic.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
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Benjamin H. Brinkmann, PhD
From the Mayo Systems Electrophysiology Laboratory, Department of Neurology (L.R., M.T.K., J.C., J.Y.M., B.H.B., W.H., S.M.S., G.A.W.), and Department of Neurosurgery (W.R.M., F.B.M.), Mayo Clinic, Rochester, MN; Department of Neurology (L.R.), China-Japan Friendship Hospital, Beijing, China; and International Clinical Research Center (J.C.), St. Anne's University Hospital, Brno, Czech Republic.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
(1) American Epilepsy Society, Travel subsidy for speaker 2011
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Wei Hu, MD, PhD
From the Mayo Systems Electrophysiology Laboratory, Department of Neurology (L.R., M.T.K., J.C., J.Y.M., B.H.B., W.H., S.M.S., G.A.W.), and Department of Neurosurgery (W.R.M., F.B.M.), Mayo Clinic, Rochester, MN; Department of Neurology (L.R.), China-Japan Friendship Hospital, Beijing, China; and International Clinical Research Center (J.C.), St. Anne's University Hospital, Brno, Czech Republic.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
W. Richard Marsh, MD
From the Mayo Systems Electrophysiology Laboratory, Department of Neurology (L.R., M.T.K., J.C., J.Y.M., B.H.B., W.H., S.M.S., G.A.W.), and Department of Neurosurgery (W.R.M., F.B.M.), Mayo Clinic, Rochester, MN; Department of Neurology (L.R.), China-Japan Friendship Hospital, Beijing, China; and International Clinical Research Center (J.C.), St. Anne's University Hospital, Brno, Czech Republic.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
Neurosurgery, ad hoc reviewer, 1990-present Mayo Clinic Proceedings, ad hoc reviewer, 1982-present
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Fredric B. Meyer, MD
From the Mayo Systems Electrophysiology Laboratory, Department of Neurology (L.R., M.T.K., J.C., J.Y.M., B.H.B., W.H., S.M.S., G.A.W.), and Department of Neurosurgery (W.R.M., F.B.M.), Mayo Clinic, Rochester, MN; Department of Neurology (L.R.), China-Japan Friendship Hospital, Beijing, China; and International Clinical Research Center (J.C.), St. Anne's University Hospital, Brno, Czech Republic.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
1. Journal of Neurosurgery, co-chairman, editorial board, 2002-present.
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
S. Matthew Stead, MD, PhD
From the Mayo Systems Electrophysiology Laboratory, Department of Neurology (L.R., M.T.K., J.C., J.Y.M., B.H.B., W.H., S.M.S., G.A.W.), and Department of Neurosurgery (W.R.M., F.B.M.), Mayo Clinic, Rochester, MN; Department of Neurology (L.R.), China-Japan Friendship Hospital, Beijing, China; and International Clinical Research Center (J.C.), St. Anne's University Hospital, Brno, Czech Republic.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
View all articles by this author
Gregory A. Worrell, MD, PhD
From the Mayo Systems Electrophysiology Laboratory, Department of Neurology (L.R., M.T.K., J.C., J.Y.M., B.H.B., W.H., S.M.S., G.A.W.), and Department of Neurosurgery (W.R.M., F.B.M.), Mayo Clinic, Rochester, MN; Department of Neurology (L.R.), China-Japan Friendship Hospital, Beijing, China; and International Clinical Research Center (J.C.), St. Anne's University Hospital, Brno, Czech Republic.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
Transactions in Biomedical Engineering 2013 -2014
Patents:
1.
Filed patent: Microscale Electrophysiology for mapping epileptogenic brain and predicting seizures
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NIH R01 NS 63039-1, PI: Worrell 04/01/2009 ? 03/31/2014 European Union Agreement FP 00066387 Co-I: Worrell 11/01/2011-12/31/2015 NeuroPace, Inc 15682PI: Worrell 11/01/2007 -?10/31/2014; National Natural Science Foundation of China 81271447 and 81271448: Liankun Ren 01/01/2013-12/31/2016
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
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Notes

Correspondence to Dr. Worrell: [email protected]
*
These authors contributed equally to this work.
Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

Author Contributions

Liankun Ren: drafting/revising the manuscript, study concept or design, analysis or interpretation of data, accepts responsibility for conduct of research and will give final approval. Michal Tomasz Kucewicz: drafting/revising the manuscript, study concept or design, analysis or interpretation of data, accepts responsibility for conduct of research and will give final approval, statistical analysis, study supervision. Jan Cimbalnik: analysis or interpretation of data, accepts responsibility for conduct of research and will give final approval, statistical analysis. Joseph Y. Matsumoto: drafting/revising the manuscript, study concept or design, analysis or interpretation of data, accepts responsibility for conduct of research and will give final approval, study supervision. Benjamin H. Brinkmann: drafting/revising the manuscript, study concept or design, analysis or interpretation of data, accepts responsibility for conduct of research and will give final approval, study supervision. Wei Hu: analysis or interpretation of data, accepts responsibility for conduct of research and will give final approval, acquisition of data. W. Richard Marsh: drafting/revising the manuscript, accepts responsibility for conduct of research and will give final approval, acquisition of data. Fredric B. Meyer: study concept or design, accepts responsibility for conduct of research and will give final approval, acquisition of data. S. Matthew Stead: analysis or interpretation of data, accepts responsibility for conduct of research and will give final approval, acquisition of data. Gregory A. Worrell: drafting/revising the manuscript, study concept or design, analysis or interpretation of data, accepts responsibility for conduct of research and will give final approval.

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