Second Clinical School, Lanzhou University, Lanzhou 730000, China; Department of Magnetic Resonance, Lanzhou University Second Hospital, Lanzhou 730000, China.
Department of Radiology, Huashan Hospital, Fudan University, Shanghai 200040, China.
Neuroimage Clin. 2022;36:103160. doi: 10.1016/j.nicl.2022.103160. Epub 2022 Aug 23.
Alterations in white matter microstructure and functional activity have been demonstrated to be involved in the central nervous system mechanism of classic trigeminal neuralgia (CTN). However, the rich-club organization and related topological alterations in the CTN brain networks remain unclear.
We simultaneously collected diffusion-tensor imaging (DTI) and resting state functional magnetic resonance imaging (rs-fMRI) data from 29 patients with CTN (9 males, mean age = 54.59 years) and 34 matched healthy controls (HCs) (12 males, mean age = 54.97 years) to construct structural networks (SNs) and functional networks (FNs). Rich-club organization was determined separately based on each group's SN and different kinds of connections. For both network types, we calculated the basic connectivity properties (network density and strength) and topological properties (global/local/nodal efficiency and small worldness). Moreover, SN-FN coupling was obtained. The relationships between all those properties and clinical measures were evaluated.
Compared to their FN, the SN of CTN patients was disrupted more severely, including its topological properties (reduced network efficiency and small-worldness), and a decrease in network density and strength was observed. Patients showed reorganization of the rich-club architecture, wherein the nodes with decreased nodal efficiency in the SN were mainly non-hub regions, and the local connections were closely related to altered global efficiency and whole brain coupling. While the cortical-subcortical connections of feeder were found to be strengthened in the SN of patients, the coupling between networks increased in all types of connections. Finally, disease severity (duration, pain intensity, and affective alterations) was negatively correlated with coupling (rich-club, feeder, and whole brain) and network strength (the rich-club of the SN and local connections of the FN). A positive correlation was only found between pain intensity and the coupling of local connections.
The SN of patients with CTN may be more vulnerable. Accompanied by the reorganization of the rich-club, the less efficient network communication and the impaired functional dynamics were largely attributable to the dysfunction of non-hub regions. As compensation, the pain transmission pathway of feeder connections involving in pain processing and emotional regulation may strengthen. The local and feeder sub-networks may serve as potential biomarkers for diagnosis or prognosis.
已经证明，白质微观结构和功能活动的改变与经典三叉神经痛（CTN）的中枢神经系统机制有关。然而，CTN 脑网络中的丰富俱乐部组织及其相关拓扑改变仍不清楚。
我们同时从 29 例 CTN 患者（9 例男性，平均年龄 54.59 岁）和 34 例匹配的健康对照者（12 例男性，平均年龄 54.97 岁）中采集扩散张量成像（DTI）和静息态功能磁共振成像（rs-fMRI）数据，以构建结构网络（SN）和功能网络（FN）。分别根据每个组的 SN 和不同类型的连接确定丰富俱乐部组织。对于两种网络类型，我们计算了基本连接特性（网络密度和强度）和拓扑特性（全局/局部/节点效率和小世界性）。此外，还获得了 SN-FN 耦合。评估了所有这些特性与临床测量之间的关系。
与他们的 FN 相比，CTN 患者的 SN 受到更严重的破坏，包括其拓扑特性（降低的网络效率和小世界性），并且观察到网络密度和强度降低。患者表现出丰富俱乐部架构的重新组织，其中 SN 中节点效率降低的节点主要是非枢纽区域，而局部连接与改变的全局效率和整个大脑耦合密切相关。虽然在患者的 SN 中发现了馈线的皮质-皮质下连接增强，但在所有类型的连接中，网络之间的耦合增加。最后，疾病严重程度（持续时间、疼痛强度和情感改变）与耦合（丰富俱乐部、馈线和整个大脑）和网络强度（SN 的丰富俱乐部和 FN 的局部连接）呈负相关。仅发现疼痛强度与局部连接的耦合呈正相关。
CTN 患者的 SN 可能更脆弱。伴随着丰富俱乐部的重组，效率较低的网络通信和功能动态受损主要归因于非枢纽区域的功能障碍。作为补偿，涉及疼痛处理和情绪调节的馈线连接的疼痛传递途径可能会增强。局部和馈线子网可能是诊断或预后的潜在生物标志物。
