Dynamic brain network states in human generalized spike-wave discharges

Area of Science:

• Neuroscience
• Epilepsy Research
• Brain Network Dynamics

Background:

• Generalized spike-wave discharges (GSWDs) in idiopathic generalized epilepsy (IGE) are traditionally viewed as having sudden onsets and offsets.
• Rodent models suggest GSWDs emerge within dynamic brain network state evolutions.
• Previous human studies indicated potential pre-discharge cortical activity and altered network connectivity.

Purpose of the Study:

• To investigate if GSWDs in human IGE emerge during dynamic brain network state evolution.
• To characterize the temporal evolution of functional brain connectivity before, during, and after GSWDs in IGE patients.

Main Methods:

• Simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) were used in 43 IGE patients and 34 healthy controls.
• Analysis focused on 95 GSWDs from 20 patients, comparing network states during discharge epochs with non-discharge epochs and controls.
• MRI signal amplitude changes and phase synchrony (functional connectivity) were analyzed across 90 brain regions.

Main Results:

• MRI signal amplitude changes occurred at and after EEG onset, involving sequential activation of parietal, frontal, and thalamic regions.
• Significant functional connectivity was observed in frontal, parietal, and occipital cortical networks during GSWDs and for 20 seconds after EEG offset.
• A sensorimotor network showed elevated synchrony in patients (with and without GSWDs) compared to controls, with specific pre-discharge connectivity changes. A posterior cortical network exhibited reduced synchrony in patients with GSWDs prior to discharge onset.

Conclusions:

• GSWDs in IGE are embedded within a longer period of evolving brain network states, extending before and after the discharge.
• Persistently high sensorimotor network synchrony and transiently low posterior network synchrony may predispose individuals to GSWD onset.
• These findings challenge the notion of abrupt GSWD onset and highlight the dynamic nature of brain network states in IGE.