The influence of wakefulness fluctuations on brain networks involved in centrotemporal spike occurrence

Clin Neurophysiol. 2024 Aug:164:47-56. doi: 10.1016/j.clinph.2024.05.005. Epub 2024 May 24.

Abstract

Objective: Drowsiness has been implicated in the modulation of centro-temporal spikes (CTS) in Self-limited epilepsy with Centro-Temporal Spikes (SeLECTS). Here, we explore this relationship and whether fluctuations in wakefulness influence the brain networks involved in CTS generation.

Methods: Functional MRI (fMRI) and electroencephalography (EEG) was simultaneously acquired in 25 SeLECTS. A multispectral EEG index quantified drowsiness ('EWI': EEG Wakefulness Index). EEG (Pearson Correlation, Cross Correlation, Trend Estimation, Granger Causality) and fMRI (PPI: psychophysiological interactions) analytic approaches were adopted to explore respectively: (a) the relationship between EWI and changes in CTS frequency and (b) the functional connectivity of the networks involved in CTS generation and wakefulness oscillations. EEG analyses were repeated on a sample of routine EEG from the same patient's cohort.

Results: No correlation was found between EWI fluctuations and CTS density during the EEG-fMRI recordings, while they showed an anticorrelated trend when drowsiness was followed by proper sleep in routine EEG traces. According to PPI findings, EWI fluctuations modulate the connectivity between the brain networks engaged by CTS and the left frontal operculum.

Conclusions: While CTS frequency per se seems unrelated to drowsiness, wakefulness oscillations modulate the connectivity between CTS generators and key regions of the language circuitry, a cognitive function often impaired in SeLECTS.

Significance: This work advances our understanding of (a) interaction between CTS occurrence and vigilance fluctuations and (b) possible mechanisms responsible for language disruption in SeLECTS.

Keywords: Drowsiness; EEG-fMRI; Functional connectivity; PPI; Self-limited epilepsies.

MeSH terms

  • Adolescent
  • Adult
  • Brain* / diagnostic imaging
  • Brain* / physiology
  • Child
  • Electroencephalography* / methods
  • Epilepsy, Rolandic / physiopathology
  • Female
  • Humans
  • Magnetic Resonance Imaging*
  • Male
  • Nerve Net* / diagnostic imaging
  • Nerve Net* / physiology
  • Sleep Stages / physiology
  • Wakefulness* / physiology
  • Young Adult