Objective

Rolandic 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).

Methods

This 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.

Results

Children 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.

Conclusion

The 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.

中文翻译：

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新诊断的良性癫痫单侧或双侧中央颞区尖峰的功能连接改变：多频 MEG 研究

客观的

Rolandic 癫痫 (RE) 是儿童癫痫综合征的最常见形式之一。这种情况通常伴有单侧或双侧中央颞部癫痫性放电。尽管有“良性”一词，但许多研究报告称，患有中心颞叶尖峰 (BECTS) 的良性癫痫儿童表现出一系列普遍存在的认知困难。此外，现有研究表明，单侧和双侧中心颞峰可能通过不同的机制影响认知。因此，本研究旨在调查具有单侧中心颞部棘波 (U-BECTS) 和双侧中心颞部棘波 (B-BECTS) 的良性癫痫儿童的认知障碍和静息状态网络拓扑结构。

方法

该研究招募了 14 名患有 U-BECTS 的儿童和 14 名患有 B-BECTS 的儿童。此后，使用第四版韦氏智力量表 (WISC-IV) 对 28 名 BECTS 儿童和 14 名健康对照儿童的认知进行了评估。此外，通过脑磁图（MEG）记录大脑静息状态的大脑磁信号，并在源级计算虚拟传感器波形，构建了大脑的功能网络。此外，图论（GT）分析被用来评估大脑网络的特性。

结果

与 U-BECTS 组的儿童相比，B-BECTS 组的儿童癫痫发作更早。此外，与健康对照组相比，B-BECTS 和 U-BECTS 组的全面智商 (FSIQ)、言语理解指数 (VCI) 和工作记忆指数 (WMI) 得分均较低，尽管 B-BECTS 组中只有儿童-BECTS 类别的感知推理指数 (PRI) 分数较低。结果还表明，两个 BECTS 组在特定频段的额叶皮层连通性都有所增加。值得注意的是，B-BECTS 儿童在 1-4-Hz 和 80-250-Hz 频段表现出更加无序和随机的网络。而且，GT分析显示，B-BECTS儿童在80-250-Hz频段具有较低的聚类系数和特征路径长度，在4-8-Hz频段具有较高的连接强度。另一方面，与健康对照组相比，U-BECTS 组在 8-12Hz 频段具有更高的聚类系数。相关性分析表明，U-BECTS 类别中的网络参数、临床特征和神经心理学数据之间存在负相关。

结论

研究结果表明，患有 BECTS 的儿童表现出弥漫性早期认知缺陷。此外，静息状态次优网络拓扑结构可能是 BECTS 儿童认知障碍的机制。该研究还表明，患有 B-BECTS 的儿童可能面临更高的认知障碍风险。