Altered functional connectivity in newly diagnosed benign epilepsy with unilateral or bilateral centrotemporal spikes: A multi-frequency MEG study

Abstract

ObjectiveRolandic epilepsy (RE) is one of the most common forms of epilepsy syndromes in children. The condition is usually accompanied with either unilateral or bilateral centrotemporal epileptic discharge. Despite the term “benign”, many studies have reported that children with benign epilepsy with centrotemporal spikes (BECTS) display a range of pervasive cognitive difficulties. In addition, existing research suggests that unilateral and bilateral centrotemporal spikes may affect cognition through different mechanisms. Consequently, the present study aimed to investigate cognitive impairment and the resting-state network topology of children with benign epilepsy with unilateral centrotemporal spikes (U-BECTS) and with bilateral centrotemporal spikes (B-BECTS). MethodsThis study recruited 14 children with U-BECTS and 14 with B-BECTS. Thereafter, cognition was assessed in 28 children with BECTS and 14 healthy controls, using the fourth edition of the Wechsler Intelligence Scale (WISC-IV). Additionally, the functional network of the brain was constructed through magnetoencephalography (MEG) to record the resting-state brain magnetic signals of the brain and by computing virtual sensor waveforms at the source level. Moreover, graph theory (GT) analysis was used to assess the properties of the brain network. ResultsChildren in the B-BECTS group had an earlier onset of epilepsy compared to those in the U-BECTS category. In addition, both the B-BECTS and U-BECTS groups had lower Full Scale Intelligence Quotient (FSIQ), Verbal Comprehension Index (VCI), and Working Memory Index (WMI) scores, compared to the healthy controls although only children in the B-BECTS category had lower Perceptual Reasoning Index (PRI) scores. The results also showed that both BECTS groups had increased frontal cortex connectivity in specific frequency bands. Notably, children with B-BECTS showed a more disorderly and randomized network in the 1–4-Hz and 80–250-Hz frequency bands. Moreover, GT analysis showed that children with B-BECTS had lower clustering coefficient and characteristic path length in the 80–250-Hz frequency bands and higher connection strength in the 4–8-Hz frequency bands. On the other hand, the U-BECTS group had a higher clustering coefficient in the 8–12-Hz frequency bands, compared to the healthy controls. Correlation analysis revealed that there were negative correlations between network parameters, clinical characteristics, and neuropsychological data in the U-BECTS category. ConclusionThe findings revealed that children with BECTS display a diffuse early cognitive deficit. In addition, resting-state suboptimal network topology may be the mechanism of cognitive impairment in children with BECTS. The study also showed that and children with B-BECTS may be at a higher risk of cognitive impairment.