Connectivity Increases During Spikes and Spike-free Periods in Self-limited Epilepsy with Centrotemporal Spikes

Overview

Journal Clin Neurophysiol

Publisher Elsevier

Specialties Neurology
Psychiatry

Date 2022 Oct 28

PMID 36307364

Authors

Beatrice S Goad

Christopher Lee-Messer

Zihuai He

Brenda E Porter

Fiona M Baumer

Affiliations

Soon will be listed here.

Abstract

Objective: To understand the impact of interictal spikes on brain connectivity in patients with Self-Limited Epilepsy with Centrotemporal Spikes (SeLECTS).

Methods: Electroencephalograms from 56 consecutive SeLECTS patients were segmented into periods with and without spikes. Connectivity between electrodes was calculated using the weighted phase lag index. To determine if there are chronic alterations in connectivity in SeLECTS, we compared spike-free connectivity to connectivity in 65 matched controls. To understand the acute impact of spikes, we compared connectivity immediately before, during, and after spikes versus baseline, spike-free connectivity. We explored whether behavioral state, spike laterality, or antiseizure medications affected connectivity.

Results: Children with SeLECTS had markedly higher connectivity than controls during sleep but not wakefulness, with greatest difference in the right hemisphere. During spikes, connectivity increased globally; before and after spikes, left frontal and bicentral connectivity increased. Right hemisphere connectivity increased more during right-sided than left-sided spikes; left hemisphere connectivity was equally affected by right and left spikes.

Conclusions: SeLECTS patient have persistent increased connectivity during sleep; connectivity is further elevated during the spike and perispike periods.

Significance: Testing whether increased connectivity impacts cognition or seizure susceptibility in SeLECTS and more severe epilepsies could help determine if spikes should be treated.

Citing Articles

Interictal EEG source connectivity to localize the epileptogenic zone in patients with drug-resistant epilepsy: A machine learning approach.

Ntolkeras G, Makaram N, Bernabei M, De La Vega A, Bolton J, Madsen J Epilepsia. 2024; 65(4):944-960.

PMID: 38318986 PMC: 11018464. DOI: 10.1111/epi.17898.

References

Zeger S, Liang K . Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 1986; 42(1):121-30. View

Wickens S, Bowden S, DSouza W . Cognitive functioning in children with self-limited epilepsy with centrotemporal spikes: A systematic review and meta-analysis. Epilepsia. 2017; 58(10):1673-1685. DOI: 10.1111/epi.13865. View

Zeger S, Liang K, Albert P . Models for longitudinal data: a generalized estimating equation approach. Biometrics. 1988; 44(4):1049-60. View

Fisher R, Cross J, French J, Higurashi N, Hirsch E, Jansen F . Operational classification of seizure types by the International League Against Epilepsy: Position Paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017; 58(4):522-530. DOI: 10.1111/epi.13670. View

Clemens B, Puskas S, Besenyei M, Spisak T, Emri M, Fekete I . Remission of benign epilepsy with rolandic spikes: an EEG-based connectivity study at the onset of the disease and at remission. Epilepsy Res. 2013; 106(1-2):128-35. DOI: 10.1016/j.eplepsyres.2013.04.006. View

Specchio N, Wirrell E, Scheffer I, Nabbout R, Riney K, Samia P . International League Against Epilepsy classification and definition of epilepsy syndromes with onset in childhood: Position paper by the ILAE Task Force on Nosology and Definitions. Epilepsia. 2022; 63(6):1398-1442. DOI: 10.1111/epi.17241. View

Song D, Stoyell S, Ross E, Ostrowski L, Thorn E, Stufflebeam S . Beta oscillations in the sensorimotor cortex correlate with disease and remission in benign epilepsy with centrotemporal spikes. Brain Behav. 2019; 9(3):e01237. PMC: 6422718. DOI: 10.1002/brb3.1237. View

Adebimpe A, Aarabi A, Bourel-Ponchel E, Mahmoudzadeh M, Wallois F . Functional Brain Dysfunction in Patients with Benign Childhood Epilepsy as Revealed by Graph Theory. PLoS One. 2015; 10(10):e0139228. PMC: 4592214. DOI: 10.1371/journal.pone.0139228. View

Vannest J, Tenney J, Gelineau-Morel R, Maloney T, Glauser T . Cognitive and behavioral outcomes in benign childhood epilepsy with centrotemporal spikes. Epilepsy Behav. 2015; 45:85-91. DOI: 10.1016/j.yebeh.2015.01.041. View

10.

Clemens B, Puskas S, Spisak T, Lajtos I, Opposits G, Besenyei M . Increased resting-state EEG functional connectivity in benign childhood epilepsy with centro-temporal spikes. Seizure. 2016; 35:50-5. DOI: 10.1016/j.seizure.2016.01.001. View

11.

Besseling R, Jansen J, Overvliet G, van der Kruijs S, Vles J, Ebus S . Reduced functional integration of the sensorimotor and language network in rolandic epilepsy. Neuroimage Clin. 2013; 2:239-46. PMC: 3777786. DOI: 10.1016/j.nicl.2013.01.004. View

12.

Smith A, Bajomo O, Pal D . A meta-analysis of literacy and language in children with rolandic epilepsy. Dev Med Child Neurol. 2015; 57(11):1019-26. DOI: 10.1111/dmcn.12856. View

13.

Zeng H, Ramos C, Nair V, Hu Y, Liao J, La C . Regional homogeneity (ReHo) changes in new onset versus chronic benign epilepsy of childhood with centrotemporal spikes (BECTS): A resting state fMRI study. Epilepsy Res. 2015; 116:79-85. PMC: 4567694. DOI: 10.1016/j.eplepsyres.2015.06.017. View

14.

Vannest J, Tenney J, Altaye M, Byars A, Spencer C, Maloney T . Impact of frequency and lateralization of interictal discharges on neuropsychological and fine motor status in children with benign epilepsy with centrotemporal spikes. Epilepsia. 2016; 57(8):e161-7. PMC: 4972650. DOI: 10.1111/epi.13445. View

15.

Besseling R, Overvliet G, Jansen J, van der Kruijs S, Vles J, Ebus S . Aberrant functional connectivity between motor and language networks in rolandic epilepsy. Epilepsy Res. 2013; 107(3):253-62. DOI: 10.1016/j.eplepsyres.2013.10.008. View

16.

Choi H, Chung Y, Choi S, Ahn S, Kim H, Yoon S . Electroencephalographic Resting-State Functional Connectivity of Benign Epilepsy with Centrotemporal Spikes. J Clin Neurol. 2019; 15(2):211-220. PMC: 6444134. DOI: 10.3988/jcn.2019.15.2.211. View

17.

Kavros P, Clarke T, Strug L, Halperin J, Dorta N, Pal D . Attention impairment in rolandic epilepsy: systematic review. Epilepsia. 2008; 49(9):1570-80. DOI: 10.1111/j.1528-1167.2008.01610.x. View

18.

Vinck M, Oostenveld R, van Wingerden M, Battaglia F, Pennartz C . An improved index of phase-synchronization for electrophysiological data in the presence of volume-conduction, noise and sample-size bias. Neuroimage. 2011; 55(4):1548-65. DOI: 10.1016/j.neuroimage.2011.01.055. View

19.

Stephen J, Weir C, Chin R . Temporal trends in incidence of Rolandic epilepsy, prevalence of comorbidities and prescribing trends: birth cohort study. Arch Dis Child. 2020; 105(6):569-574. PMC: 7285789. DOI: 10.1136/archdischild-2019-318212. View

20.

Oser N, Hubacher M, Specht K, Datta A, Weber P, Penner I . Default mode network alterations during language task performance in children with benign epilepsy with centrotemporal spikes (BECTS). Epilepsy Behav. 2014; 33:12-7. DOI: 10.1016/j.yebeh.2014.01.008. View