Delta oscillation coupled propagating fast ripples precede epileptiform discharges in patients with focal epilepsy

Shennan A. Weiss; Laurent Sheybani; Nitish Seenarine; Itzhak Fried; Chengyuan Wu; Ashwini Sharan; Jerome Engel, Jr; Michael R. Sperling; Yuval Nir; Richard J. Staba

Neurobiology of Disease (Dec 2022)

Delta oscillation coupled propagating fast ripples precede epileptiform discharges in patients with focal epilepsy

Shennan A. Weiss,
Laurent Sheybani,
Nitish Seenarine,
Itzhak Fried,
Chengyuan Wu,
Ashwini Sharan,
Jerome Engel, Jr,
Michael R. Sperling,
Yuval Nir,
Richard J. Staba

Affiliations

Shennan A. Weiss: Dept. of Neurology, State University of New York Downstate, Brooklyn, New York 11203, USA; Dept. of Physiology and Pharmacology, State University of New York Downstate, Brooklyn, New York 11203, USA; Dept. of Neurology, New York City Health + Hospitals/Kings County, Brooklyn, NY, USA; Corresponding author at: 450 Clarkson Avenue, MSC 1213, Brooklyn, NY 11203, USA.
Laurent Sheybani: EEG and Epilepsy Unit / Neurology, Department of Clinical Neuroscience, University Hospitals and Faculty of Medicine of University of Geneva, Geneva, Switzerland; Department of Clinical and Experimental Epilepsy, UCL Queen Square Institute of Neurology, University College London, London, UK
Nitish Seenarine: Dept. of Neurology, State University of New York Downstate, Brooklyn, New York 11203, USA; Dept. of Physiology and Pharmacology, State University of New York Downstate, Brooklyn, New York 11203, USA
Itzhak Fried: Dept. of Neurosurgery, David Geffen School of Medicine at UCLA, Los Angeles, California 90095, USA
Chengyuan Wu: Dept. of Neuroradiology, Thomas Jefferson University, Philadelphia, PA, 19107, USA; Dept. of Neurosurgery, Thomas Jefferson University, Philadelphia, PA 19107, USA
Ashwini Sharan: Dept. of Neurosurgery, Thomas Jefferson University, Philadelphia, PA 19107, USA
Jerome Engel, Jr: Dept. of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, California 90095, USA; Dept. of Neurosurgery, David Geffen School of Medicine at UCLA, Los Angeles, California 90095, USA; Dept. of Neurobiology, David Geffen School of Medicine at UCLA, Los Angeles, California 90095, USA; Dept. of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine at UCLA, Los Angeles, California 90095, USA; Brain Research Institute, David Geffen School of Medicine at UCLA, Los Angeles, California 90095, USA
Michael R. Sperling: Depts. of Neurology and Neuroscience, Thomas Jefferson University, Philadelphia, PA 19107, USA
Yuval Nir: Department of Physiology and Pharmacology, Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel; Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel; The Sieratzki-Sagol Center for Sleep Medicine, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel; Department of Biomedical Engineering, Faculty of Engineering, Tel Aviv University, Tel Aviv, Israel
Richard J. Staba: Dept. of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, California 90095, USA

Journal volume & issue: Vol. 175
p. 105928

Abstract

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Epileptiform spikes are used to localize epileptogenic brain tissue. The mechanisms that spontaneously trigger epileptiform discharges are not yet elucidated. Pathological fast ripple (FR, 200–600 Hz) are biomarkers of epileptogenic brain, and we postulated that FR network interactions are involved in generating epileptiform spikes. Using macroelectrode stereo intracranial EEG (iEEG) recordings from a cohort of 46 patients we found that, in the seizure onset zone (SOZ), propagating FR were more often followed by an epileptiform spike, as compared with non-propagating FR (p < 0.05). Propagating FR had a distinct frequency and larger power (p < 1e-10) and were more strongly phase coupled to the peak of iEEG delta oscillation, which likely correspond with the DOWN states during non-REM sleep (p < 1e-8), than non-propagating FR. While FR propagation was rare, all FR occurred with the highest probability within +/− 400 msec of epileptiform spikes with superimposed high-frequency oscillations (p < 0.05). Thus, a sub-population of epileptiform spikes in the SOZ, are preceded by propagating FR that are coordinated by the DOWN state during non-REM sleep.

Published in Neurobiology of Disease

ISSN: 0969-9961 (Print); 1095-953X (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry
Website: https://www.journals.elsevier.com/neurobiology-of-disease

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