Human interictal epileptiform discharges are bidirectional traveling waves echoing ictal discharges
- University of Utah, United States
- Weill Cornell Medicine, United States
- Columbia University Medical Center, United States
- Arizona State University, United States
- Neurosurgical Associates, LLC, United States
- Hospital for Special Surgery, United States
- Lenox Hill Hospital, United States
- Baylor College of Medicine, United States
- Columbia University, United States
Abstract
Interictal epileptiform discharges (IEDs), also known as interictal spikes, are large intermittent electrophysiological events observed between seizures in patients with epilepsy. Though they occur far more often than seizures, IEDs are less studied, and their relationship to seizures remains unclear. To better understand this relationship, we examined multi-day recordings of microelectrode arrays implanted in human epilepsy patients, allowing us to precisely observe the spatiotemporal propagation of IEDs, spontaneous seizures, and how they relate. These recordings showed that the majority of IEDs are traveling waves, traversing the same path as ictal discharges during seizures, and with a fixed direction relative to seizure propagation. Moreover, the majority of IEDs, like ictal discharges, were bidirectional, with one predominant and a second, less frequent antipodal direction. These results reveal a fundamental spatiotemporal similarity between IEDs and ictal discharges. These results also imply that most IEDs arise in brain tissue outside the site of seizure onset and propagate toward it, indicating that the propagation of IEDs provides useful information for localizing the seizure focus.
Data availability
Raw data is available upon establishment of a data use agreement with Columbia University Medical Center as required by their Institutional Review Board (IRB). Data from human subjects was analyzed, from which the dates of implants can potentially be reconstructed. This is especially true for a study like this one, in which chronic recordings were carried out for the full duration of the patients' hospital stays. Sharing these data widely could therefore expose private health information of participants, which is why a data use agreement is required by the IRB. Interested Researchers should contact Dr. Schevon to get the data use agreement process started with the Columbia University Medical Center IRB.Analysis code is upload to GitHub: https://github.com/elliothsmith/IEDs. We have included preprocessed data files for all IEDs, hosted online at OSF: https://osf.io/zhk24/. Data files include LFP, MUA event times, and traveling wave model coefficients for all detected IEDs.
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Human interictal epileptiform discharges are bidirectional traveling waves echoing ictal dischargesOSF, DOI: https://osf.io/zhk24/.
Article and author information
Author details
Funding
National Institutes of Health (NINDS R21 NS113031)
- Elliot H Smith
- Catherine Schevon
- John Rolston
National Institutes of Health (NINDS K23 NS114178)
- John Rolston
National Institutes of Health (S10 OD018211)
- Catherine Schevon
National Institutes of Health (R01 NS084142)
- Catherine Schevon
American Epilepsy Society (JIA)
- Elliot H Smith
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: The Institutional Review Boards at the University of Utah (IRB_00114691) and Columbia University Medical Center (IRB- AAAB6324) approved these studies. All participants provided informed consent prior to surgery for implantation of the clinical and research electrodes.
Reviewing Editor
- Matthew Shtrahman, University of California, San Diego, United States
Version history
- Preprint posted: April 29, 2021 (view preprint)
- Received: September 2, 2021
- Accepted: January 19, 2022
- Accepted Manuscript published: January 20, 2022 (version 1)
- Accepted Manuscript updated: January 24, 2022 (version 2)
- Version of Record published: February 3, 2022 (version 3)
Copyright
© 2022, Smith et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Human interictal epileptiform discharges are bidirectional traveling waves echoing ictal discharges
eLife 11:e73541.
https://doi.org/10.7554/eLife.73541
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