Neuronal networks in children with continuous spikes and waves during slow sleep

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.

Epilepsy‐related brain networks in ring chromosome 20 syndrome: An EEG‐fMRI study

“…26 By means of EEG-fMRI coregistration, a common bilateral BOLD increase in the perisylvian regions (plus thalamus and cingulate cortex) was observed in CSWS patients, independent of the etiology and the initial spike focus of the single cases. 12 This finding supports the notion that the involvement of these cortical regions is crucial for the neuropsychological impairment and the behavioral regression that accompany this disorder. It is then possible that the perisylvian cortex disruption represents a sort of common signature of different epileptic encephalopathies characterized by regression of acquired skills in children and adolescents.…”

“…EEG-fMRI studies have recently contributed to the understanding of the epileptic networks involved in different epileptic encephalopathies (EEs). To date, studies have been published in continuous spike-and-wave during sleep (CSWS), Lennox-Gastaut syndrome (LGS), and West (WS) syndromes, [11][12][13][14] revealing the existence of specific networks involved during the pathologic activity in such conditions. In [r (20)] syndrome, we recently showed that the typical theta-delta rhythm is generated within the frontoparietal cortices, suggesting a dysfunction of the premotor/sensorimotor systems.…”

Sequential Prefrontal Lobe Volume Changes in Epileptic Patients with Continuous Spikes and Waves During Slow Sleep

“…Independent of etiology and individual area of initial epileptic activity, patients with CSWS may be characterized by a consistent specific neuronal network of activation. In a recent study, the activation in the perisylvian/prefrontal network was associated with both activation in the thalamocortical network and deactivation in the default mode network (Siniatchkin et al, 2010). Our results and these findings suggest that children with CSWS may have abnormalities in the frontal lobe even if the epileptic focus is not frontal.…”

Encephalopathy with Electrical Status Epilepticus in Slow Wave Sleep – a review with an emphasis on regional (perisylvian) aspects

“…PET and SPECT studies have revealed hypermetabolism and hypoperfusion in the perisylvian region and temporo-parietal cortex associated with ESES without and with LKS (Fueki et al, 1988;Gaggero et al, 1995;Maquet et al, 2000) and lesional cases also; how unilateral perisylvian dominance with MRI and fMRI (Hegyi et al, 2009;Siniatchkin et al, (2010). The early FDG-PET study of showed that among six patients studied during the active phase of ESES, five had unilateral, focal/ regional increase of glucose metabolism in the cortex.…”

“…The thalamic nuclei remained symmetrical despite significant cortical asymmetries, suggesting either that cortico-thalamic neurons do not participate in the generation of spike-and-wave discharges or that they are inhibited by the pathologic mechanisms. Siniatchkin et al (2010) in a series of 12 patients with continuous electrical pattern simultaneously performed fMRI and EEG source analysis. They have found a common neuronal network activated during the discharges.…”