Systematically altered connectome gradient in benign childhood epilepsy with centrotemporal spikes: Potential effect on cognitive function

IF 3.4 2区医学 Q2 NEUROIMAGING Neuroimage-Clinical Pub Date : 2024-01-01 DOI:10.1016/j.nicl.2024.103628

Jie Hu , Guiqin Chen , Zhen Zeng , Haifeng Ran , Ruoxi Zhang , Qiane Yu , Yuxin Xie , Yulun He , Fuqin Wang , Xuhong Li , Kexing Huang , Heng Liu , Tijiang Zhang

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Abstract

Objective

Benign childhood epilepsy with centrotemporal spikes (BECTS) affects brain network hierarchy and cognitive function; however, it remains unclear how hierarchical change affects cognition in patients with BECTS. A major aim of this study was to examine changes in the macro-network function hierarchy in BECTS and its potential contribution to cognitive function.

Methods

Overall, the study included 50 children with BECTS and 69 healthy controls. Connectome gradient analysis was used to determine the brain network hierarchy of each group. By comparing gradient scores at each voxel level and network between groups, we assessed changes in whole-brain voxel-level and network hierarchy. Functional connectivity was used to detect the functional reorganization of epilepsy caused by these abnormal brain regions based on these aberrant gradients. Lastly, we explored the relationships between the change gradient and functional connectivity values and clinical variables and further predicted the cognitive function associated with BECTS gradient changes.

Results

In children with BECTS, the gradient was extended at different network and voxel levels. The gradient scores frontoparietal network was increased in the principal gradient of patients with BECTS. The left precentral gyrus (PCG) and right angular gyrus gradient scores were significantly increased in the principal gradient of children with BECTS. Moreover, in regions of the brain with abnormal principal gradients, functional connectivity was disrupted. The left PCG gradient score of children with BECTS was correlated with the verbal intelligence quotient (VIQ), and the disruption of functional connectivity in brain regions with abnormal principal gradients was closely related to cognitive function. VIQ was significantly predicted by the principal gradient map of patients.

Significance

The results indicate connectome gradient disruption in children with BECTS and its relationship to cognitive function, thereby increasing our understanding of the functional connectome hierarchy and providing potential biomarkers for cognitive function of children with BECTS.

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良性儿童癫痫伴中心颞区棘波的连通组梯度发生系统性改变：对认知功能的潜在影响

目的伴有中心颞区棘波的良性儿童癫痫（BECTS）会影响大脑网络层次结构和认知功能；然而，目前仍不清楚层次结构的变化如何影响BECTS患者的认知能力。本研究的一个主要目的是研究 BECTS 患者宏观网络功能层次的变化及其对认知功能的潜在贡献。研究采用连接组梯度分析来确定每组的大脑网络层次结构。通过比较组间每个体素水平和网络的梯度得分，我们评估了全脑体素水平和网络层次结构的变化。根据这些异常梯度，我们使用功能连接来检测这些异常脑区导致的癫痫功能重组。最后，我们探讨了变化梯度和功能连接值与临床变量之间的关系，并进一步预测了与 BECTS 梯度变化相关的认知功能。在 BECTS 患者的主要梯度中，前顶叶网络的梯度得分有所增加。在 BECTS 患儿的主要梯度中，左侧中央前回（PCG）和右侧角回梯度得分显著增加。此外，在主梯度异常的大脑区域，功能连接也受到破坏。BECTS患儿的左侧PCG梯度得分与言语智商（VIQ）相关，主梯度异常的脑区功能连接的破坏与认知功能密切相关。研究结果表明了BECTS患儿的连接组梯度破坏及其与认知功能的关系，从而加深了我们对功能连接组层次的理解，并为BECTS患儿的认知功能提供了潜在的生物标记。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Neuroimage-Clinical NEUROIMAGING-

CiteScore

7.50

自引率

4.80%

发文量

368

审稿时长

52 days

期刊介绍： NeuroImage: Clinical, a journal of diseases, disorders and syndromes involving the Nervous System, provides a vehicle for communicating important advances in the study of abnormal structure-function relationships of the human nervous system based on imaging. The focus of NeuroImage: Clinical is on defining changes to the brain associated with primary neurologic and psychiatric diseases and disorders of the nervous system as well as behavioral syndromes and developmental conditions. The main criterion for judging papers is the extent of scientific advancement in the understanding of the pathophysiologic mechanisms of diseases and disorders, in identification of functional models that link clinical signs and symptoms with brain function and in the creation of image based tools applicable to a broad range of clinical needs including diagnosis, monitoring and tracking of illness, predicting therapeutic response and development of new treatments. Papers dealing with structure and function in animal models will also be considered if they reveal mechanisms that can be readily translated to human conditions.