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

doi:10.1016/j.nbd.2022.105928

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

Neurobiol Dis. 2022 Dec:175:105928. doi: 10.1016/j.nbd.2022.105928. Epub 2022 Nov 17.

Authors

Affiliations

¹ 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. Electronic address: [email protected].
² 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.
³ 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.
⁴ Dept. of Neurosurgery, David Geffen School of Medicine at UCLA, Los Angeles, California 90095, USA.
⁵ Dept. of Neuroradiology, Thomas Jefferson University, Philadelphia, PA, 19107, USA; Dept. of Neurosurgery, Thomas Jefferson University, Philadelphia, PA 19107, USA.
⁶ Dept. of Neurosurgery, Thomas Jefferson University, Philadelphia, PA 19107, USA.
⁷ 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.
⁸ Depts. of Neurology and Neuroscience, Thomas Jefferson University, Philadelphia, PA 19107, USA.
⁹ 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.
¹⁰ Dept. of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, California 90095, USA.

PMID: 36403895
DOI: 10.1016/j.nbd.2022.105928

Abstract

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.

Keywords: down state; epileptiform discharge; fast ripple; focal epilepsy; high-frequency oscillation; slow wave sleep.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Brain
Brain Waves*
Electrocorticography
Electroencephalography
Epilepsies, Partial* / diagnosis
Humans

Abstract

Publication types

MeSH terms

Grants and funding