Objective Tinnitus is a prevalent hearing disorder, which could have a devastating impact on a patient’s life. Functional studies have revealed connectivity pattern changes in the tinnitus brains that suggested a change of network dynamics as well as topological organization. However, no studies have yet provided evidence for the topological network changes in the gray matter. In this research, we aim to use the graph-theoretical approach to investigate the changes of topology in the tinnitus brain using structural MRI data, which could provide insights into the underlying anatomical basis for the neural mechanism in generating phantom sounds. Methods We collected 3D MRI images on 46 bilateral tinnitus patients and 46 age and gender-matched healthy controls. Brain networks were constructed with correlation matrices of the cortical thickness and subcortical volumes of 80 cortical/subcortical regions of interests. Global network properties were analyzed using local and global efficiency, clustering coefficient, and small-world coefficient, and regional network properties were evaluated using the betweenness coefficient for hub connectivity, and interregional correlations for edge properties. Between-group differences in cortical thickness and subcortical volumes were assessed using independent sample t-tests, and local efficiency, global efficiency, clustering coefficient, sigma, and interregional correlation were compared using non-parametric permutation tests. Results Tinnitus was found to have increased global efficiency, local efficiency, and cluster coefficient, indicating generally heightened connectivity of the network. The small-world coefficient remained normal for tinnitus, indicating intact small-worldness. Betweenness centrality analysis showed that hubs in the amygdala and parahippocampus were only found for tinnitus but not controls. In contrast, hubs in the auditory cortex, insula, and thalamus were only found for controls but not tinnitus. Interregional correlation analysis further found in tinnitus enhanced connectivity between the auditory cortex and prefrontal lobe, and decreased connectivity of the insula with anterior cingulate gyrus and parahippocampus. Conclusion These findings provided the first morphological evidence of altered topological organization of the brain networks in tinnitus. These alterations suggest that heightened efficiency of the brain network and altered auditory-limbic connection for tinnitus, which could be developed in compensation for the auditory deafferentation, leading to overcompensation and, ultimately, an emotional and cognitive burden.

中文翻译：

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改变耳鸣中灰质网络的拓扑模式：基于图论的研究

目的 耳鸣是一种普遍存在的听力障碍，可能对患者的生活造成毁灭性影响。功能研究揭示了耳鸣大脑中的连接模式变化，这表明网络动态和拓扑组织发生了变化。然而，尚未有研究提供灰质拓扑网络变化的证据。在这项研究中，我们的目标是使用图论方法利用结构 MRI 数据研究耳鸣大脑中拓扑结构的变化，这可以提供对产生幻音的神经机制的潜在解剖学基础的见解。方法 我们收集了 46 名双侧耳鸣患者和 46 名年龄和性别匹配的健康对照者的 3D MRI 图像。大脑网络是用 80 个感兴趣的皮层/皮层下区域的皮层厚度和皮层下体积的相关矩阵构建的。使用局部和全局效率、聚类系数和小世界系数分析全球网络属性，使用枢纽连通性的介数系数和边缘属性的区域间相关性评估区域网络属性。使用独立样本 t 检验评估皮质厚度和皮质下体积的组间差异，并使用非参数置换检验比较局部效率、全局效率、聚类系数、西格玛和区域间相关性。结果发现耳鸣提高了全局效率、局部效率和集群系数，表明网络的连通性普遍增强。耳鸣的小世界系数保持正常，表明小世界性完好。中介中心性分析表明，杏仁核和海马旁的中枢仅在耳鸣中被发现，而在对照组中则没有。相比之下，听觉皮层、脑岛和丘脑中的枢纽仅在对照组中发现，而在耳鸣中未发现。区域间相关性分析进一步发现耳鸣增强了听觉皮层和前额叶之间的连通性，并降低了岛叶与前扣带回和海马旁的连通性。结论 这些发现提供了耳鸣中脑网络拓扑结构改变的第一个形态学证据。