Spike patterns surrounding sleep and seizures localize the seizure-onset zone in focal epilepsy.


Journal

Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R

Informations de publication

Date de publication:
03 2023
Historique:
revised: 08 12 2022
received: 02 09 2022
accepted: 08 12 2022
pmc-release: 01 03 2024
pubmed: 10 12 2022
medline: 15 3 2023
entrez: 9 12 2022
Statut: ppublish

Résumé

Interictal spikes help localize seizure generators as part of surgical planning for drug-resistant epilepsy. However, there are often multiple spike populations whose frequencies change over time, influenced by brain state. Understanding state changes in spike rates will improve our ability to use spikes for surgical planning. Our goal was to determine the effect of sleep and seizures on interictal spikes, and to use sleep and seizure-related changes in spikes to localize the seizure-onset zone (SOZ). We performed a retrospective analysis of intracranial electroencephalography (EEG) data from patients with focal epilepsy. We automatically detected interictal spikes and we classified different time periods as awake or asleep based on the ratio of alpha to delta power, with a secondary analysis using the recently published SleepSEEG algorithm. We analyzed spike rates surrounding sleep and seizures. We developed a model to localize the SOZ using state-dependent spike rates. We analyzed data from 101 patients (54 women, age range 16-69). The normalized alpha-delta power ratio accurately classified wake from sleep periods (area under the curve = .90). Spikes were more frequent in sleep than wakefulness and in the post-ictal compared to the pre-ictal state. Patients with temporal lobe epilepsy had a greater wake-to-sleep and pre- to post-ictal spike rate increase compared to patients with extra-temporal epilepsy. A machine-learning classifier incorporating state-dependent spike rates accurately identified the SOZ (area under the curve = .83). Spike rates tended to be higher and better localize the seizure-onset zone in non-rapid eye movement (NREM) sleep than in wake or REM sleep. The change in spike rates surrounding sleep and seizures differs between temporal and extra-temporal lobe epilepsy. Spikes are more frequent and better localize the SOZ in sleep, particularly in NREM sleep. Quantitative analysis of spikes may provide useful ancillary data to localize the SOZ and improve surgical planning.

Identifiants

pubmed: 36484572
doi: 10.1111/epi.17482
pmc: PMC10045742
mid: NIHMS1876588
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

754-768

Subventions

Organisme : NINDS NIH HHS
ID : R25 NS065745
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS113366
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS116504
Pays : United States
Organisme : NINDS NIH HHS
ID : DP1 NS122038
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH117155
Pays : United States
Organisme : NINDS NIH HHS
ID : K23 NS121401
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS060910
Pays : United States
Organisme : NINDS NIH HHS
ID : R56 NS099348
Pays : United States
Organisme : NINDS NIH HHS
ID : T32 NS091006
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH112847
Pays : United States

Informations de copyright

© 2022 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.

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Auteurs

Erin C Conrad (EC)

Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Andrew Y Revell (AY)

Medical Scientist Training Program, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Adam S Greenblatt (AS)

Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Ryan S Gallagher (RS)

Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Akash R Pattnaik (AR)

Department of Bioengineering, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Nicole Hartmann (N)

Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

James J Gugger (JJ)

Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Russell T Shinohara (RT)

Department of Biostatistics, Epidemiology, & Informatics, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
Penn Statistics in Imaging and Visualization Center, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
Center for Biomedical Image Computing and Analytics, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Brian Litt (B)

Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Eric D Marsh (ED)

Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
Division of Child Neurology, Pediatric Epilepsy Program, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.

Kathryn A Davis (KA)

Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

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