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Neuronal networks in children with continuous spikes and waves during slow sleep
Michael Siniatchkin1, Kristina Groening, Jan Moehring
1Neuropaediatric Department, Paediatric Hospital, Christian-Albrechts-University, Schwanenweg 20, Kiel, Germany. m.siniatchkin@pedneuro.uni-kiel.de
Insights
Continuous spikes and waves during slow sleep (CSWS) cause cognitive deficits. This study used EEG-fMRI to reveal brain activations and deactivations in children with CSWS, identifying key affected networks.
Area of Science:
- Neuroscience
- Pediatric Neurology
- Epileptology
Background:
- Epileptic encephalopathy with continuous spikes and waves during slow sleep (CSWS) is characterized by significant interictal epileptiform discharges during sleep and associated cognitive impairments.
- The underlying pathophysiological mechanisms and neuropsychological deficits in CSWS remain poorly understood, necessitating further investigation into brain activity patterns.
Purpose of the Study:
- To investigate the haemodynamic changes associated with epileptic activity in children with CSWS using simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI).
- To compare fMRI findings with electric source analysis to understand the initiation and propagation pathways of epileptic activity and their impact on brain function.
Main Methods:
- Simultaneous EEG and fMRI were acquired in 12 children diagnosed with symptomatic or cryptogenic CSWS.
- Blood oxygenation-level-dependent (BOLD) changes related to epileptic spikes were analyzed using statistical parametric mapping.
- Electric source analysis was performed using a distributed linear inverse solution to compare with fMRI results.
Main Results:
- All patients exhibited significant spike-related BOLD signal changes, including both activations and deactivations (P < 0.05, family-wise error corrected).
- Consistent activations were observed in the bilateral perisylvian region, insula, and cingulate gyrus across patients.
- Spike-related deactivations were predominantly found in the default mode network (DMN) structures, including the precuneus, parietal cortex, and medial frontal cortex.
Conclusions:
- Despite etiological heterogeneity, patients with CSWS share a common activated neuronal network involving the perisylvian region, insula, and cingulate gyrus.
- fMRI-derived activations likely represent both the initiation and propagation pathways of epileptiform discharges.
- Deactivations in the DMN suggest that CSWS-related epileptiform activity disrupts normal neurophysiological function, contributing to cognitive deficits.
Abstract:
Epileptic encephalopathy with continuous spikes and waves during slow sleep is an age-related disorder characterized by the presence of interictal epileptiform discharges during at least >85% of sleep and cognitive deficits associated with this electroencephalography pattern. The pathophysiological mechanisms of continuous spikes and waves during slow sleep and neuropsychological deficits associated with this condition are still poorly understood. Here, we investigated the haemodynamic changes associated with epileptic activity using simultaneous acquisitions of electroencephalography and functional magnetic resonance imaging in 12 children with symptomatic and cryptogenic continuous spikes and waves during slow sleep. We compared the results of magnetic resonance to electric source analysis carried out using a distributed linear inverse solution at two time points of the averaged epileptic spike. All patients demonstrated highly significant spike-related positive (activations) and negative (deactivations) blood oxygenation-level-dependent changes (P < 0.05, family-wise error corrected). The activations involved bilateral perisylvian region and cingulate gyrus in all cases, bilateral frontal cortex in five, bilateral parietal cortex in one and thalamus in five cases. Electrical source analysis demonstrated a similar involvement of the perisylvian brain regions in all patients, independent of the area of spike generation. The spike-related deactivations were found in structures of the default mode network (precuneus, parietal cortex and medial frontal cortex) in all patients and in caudate nucleus in four. Group analyses emphasized the described individual differences. Despite aetiological heterogeneity, patients with continuous spikes and waves during slow sleep were characterized by activation of the similar neuronal network: perisylvian region, insula and cingulate gyrus. Comparison with the electrical source analysis results suggests that the activations correspond to both initiation and propagation pathways. The deactivations in structures of the default mode network are consistent with the concept of epileptiform activity impacting on normal brain function by inducing repetitive interruptions of neurophysiological function.
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