Department of Psychiatry, Beijing Children's Hospital, Capital Medical University, National Center for Children's Health, Beijing, China.
State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China.
PLoS Biol. 2024 Sep 18;22(9):e3002653. doi: 10.1371/journal.pbio.3002653. eCollection 2024 Sep.
The modular structure of functional connectomes in the human brain undergoes substantial reorganization during development. However, previous studies have implicitly assumed that each region participates in one single module, ignoring the potential spatial overlap between modules. How the overlapping functional modules develop and whether this development is related to gray and white matter features remain unknown. Using longitudinal multimodal structural, functional, and diffusion MRI data from 305 children (aged 6 to 14 years), we investigated the maturation of overlapping modules of functional networks and further revealed their structural associations. An edge-centric network model was used to identify the overlapping modules, and the nodal overlap in module affiliations was quantified using the entropy measure. We showed a regionally heterogeneous spatial topography of the overlapping extent of brain nodes in module affiliations in children, with higher entropy (i.e., more module involvement) in the ventral attention, somatomotor, and subcortical regions and lower entropy (i.e., less module involvement) in the visual and default-mode regions. The overlapping modules developed in a linear, spatially dissociable manner, with decreased entropy (i.e., decreased module involvement) in the dorsomedial prefrontal cortex, ventral prefrontal cortex, and putamen and increased entropy (i.e., increased module involvement) in the parietal lobules and lateral prefrontal cortex. The overlapping modular patterns captured individual brain maturity as characterized by chronological age and were predicted by integrating gray matter morphology and white matter microstructural properties. Our findings highlight the maturation of overlapping functional modules and their structural substrates, thereby advancing our understanding of the principles of connectome development.
人脑功能连接组的模块化结构在发育过程中经历了实质性的重组。然而,以前的研究隐含地假设每个区域都参与一个单一的模块,而忽略了模块之间的潜在空间重叠。重叠的功能模块如何发展,以及这种发展是否与灰质和白质特征有关,仍然未知。我们使用来自 305 名儿童(6 至 14 岁)的纵向多模态结构、功能和弥散 MRI 数据,研究了功能网络重叠模块的成熟情况,并进一步揭示了它们的结构关联。采用基于边的网络模型来识别重叠模块,并使用熵测度量化模块归属中的节点重叠。我们展示了儿童大脑节点在模块归属中重叠程度的区域异质性空间拓扑结构,在腹侧注意、躯体运动和皮质下区域的熵(即更多模块参与)较高,而在视觉和默认模式区域的熵(即较少模块参与)较低。重叠模块以线性、空间可分离的方式发展,背内侧前额叶皮质、腹侧前额叶皮质和壳核中的熵(即模块参与度降低)降低,顶叶小叶和外侧前额叶皮质中的熵(即模块参与度增加)增加。捕获个体大脑成熟度的重叠模块模式以年龄为特征,并通过整合灰质形态和白质微观结构特性进行预测。我们的研究结果强调了重叠功能模块及其结构基础的成熟,从而推进了我们对连接组发展原则的理解。