Flexible, high‐resolution cortical arrays with large coverage capture microscale high‐frequency oscillations in patients with epilepsy

Author:

Barth Katrina J.1ORCID,Sun James2,Chiang Chia‐Han1ORCID,Qiao Shaoyu2ORCID,Wang Charles1,Rahimpour Shervin34,Trumpis Michael1,Duraivel Suseendrakumar1ORCID,Dubey Agrita5,Wingel Katie E.5,Voinas Alex E.2ORCID,Ferrentino Breonna2,Doyle Werner6,Southwell Derek G.78,Haglund Michael M.8,Vestal Matthew89,Harward Stephen C.8,Solzbacher Florian41011,Devore Sasha12,Devinsky Orrin61213ORCID,Friedman Daniel12,Pesaran Bijan5,Sinha Saurabh R.14ORCID,Cogan Gregory B.815161718,Blanco Justin19ORCID,Viventi Jonathan1781516ORCID

Affiliation:

1. Department of Biomedical Engineering Duke University North Carolina Durham USA

2. Center for Neural Science New York University New York New York USA

3. Department of Neurosurgery, Clinical Neuroscience Center University of Utah Utah Salt Lake City USA

4. Department of Biomedical Engineering University of Utah Utah Salt Lake City USA

5. Department of Neurosurgery Perelman School of Medicine, University of Pennsylvania Pennsylvania Philadelphia USA

6. Department of Neurosurgery NYU Langone Health New York New York USA

7. Department of Neurobiology Duke University School of Medicine North Carolina Durham USA

8. Department of Neurosurgery Duke University School of Medicine North Carolina Durham USA

9. Department of Pediatrics Duke University School of Medicine North Carolina Durham USA

10. Department of Electrical and Computer Engineering University of Utah Utah Salt Lake City USA

11. Department of Materials Science and Engineering University of Utah Utah Salt Lake City USA

12. Department of Neurology NYU Grossman School of Medicine New York New York USA

13. Comprehensive Epilepsy Center NYU Langone Health New York New York USA

14. Department of Neurology, Perelman School of Medicine University of Pennsylvania Pennsylvania Philadelphia USA

15. Duke Comprehensive Epilepsy Center Duke University School of Medicine North Carolina Durham USA

16. Department of Neurology Duke University School of Medicine North Carolina Durham USA

17. Department of Psychology and Neuroscience Duke University North Carolina Durham USA

18. Center for Cognitive Neuroscience Duke University North Carolina Durham USA

19. Department of Electrical and Computer Engineering United States Naval Academy Maryland Annapolis USA

Abstract

AbstractObjectiveEffective surgical treatment of drug‐resistant epilepsy depends on accurate localization of the epileptogenic zone (EZ). High‐frequency oscillations (HFOs) are potential biomarkers of the EZ. Previous research has shown that HFOs often occur within submillimeter areas of brain tissue and that the coarse spatial sampling of clinical intracranial electrode arrays may limit the accurate capture of HFO activity. In this study, we sought to characterize microscale HFO activity captured on thin, flexible microelectrocorticographic (μECoG) arrays, which provide high spatial resolution over large cortical surface areas.MethodsWe used novel liquid crystal polymer thin‐film μECoG arrays (.76–1.72‐mm intercontact spacing) to capture HFOs in eight intraoperative recordings from seven patients with epilepsy. We identified ripple (80–250 Hz) and fast ripple (250–600 Hz) HFOs using a common energy thresholding detection algorithm along with two stages of artifact rejection. We visualized microscale subregions of HFO activity using spatial maps of HFO rate, signal‐to‐noise ratio, and mean peak frequency. We quantified the spatial extent of HFO events by measuring covariance between detected HFOs and surrounding activity. We also compared HFO detection rates on microcontacts to simulated macrocontacts by spatially averaging data.ResultsWe found visually delineable subregions of elevated HFO activity within each μECoG recording. Forty‐seven percent of HFOs occurred on single 200‐μm‐diameter recording contacts, with minimal high‐frequency activity on surrounding contacts. Other HFO events occurred across multiple contacts simultaneously, with covarying activity most often limited to a .95‐mm radius. Through spatial averaging, we estimated that macrocontacts with 2–3‐mm diameter would only capture 44% of the HFOs detected in our μECoG recordings.SignificanceThese results demonstrate that thin‐film microcontact surface arrays with both highresolution and large coverage accurately capture microscale HFO activity and may improve the utility of HFOs to localize the EZ for treatment of drug‐resistant epilepsy.

Funder

American Epilepsy Society

Centers for Disease Control and Prevention

Epilepsy Foundation

Finding A Cure for Epilepsy and Seizures

National Institutes of Health

National Science Foundation

U.S. Department of Defense

Vilcek Foundation

Tuberous Sclerosis Alliance

Office of Naval Research

Templeton World Charity Foundation

Army Research Office

Esther A. and Joseph Klingenstein Fund

Publisher

Wiley

Subject

Neurology (clinical),Neurology

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