He Yirong, Zeng Debin, Li Qiongling, Chu Lei, Dong Xiaoxi, Liang Xinyuan, Sun Lianglong, Liao Xuhong, Zhao Tengda, Chen Xiaodan, Lei Tianyuan, Men Weiwei, Wang Yanpei, Wang Daoyang, Hu Mingming, Pan Zhiying, Zhang Haibo, Liu Ningyu, Tan Shuping, Gao Jia-Hong, Qin Shaozheng, Tao Sha, Dong Qi, He Yong, Li Shuyu
State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China.
Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science & Medical Engineering, Beihang University, Beijing, China.
PLoS Biol. 2025 Apr 1;23(4):e3002710. doi: 10.1371/journal.pbio.3002710. eCollection 2025 Apr.
From childhood to adolescence, the structural organization of the human brain undergoes dynamic and regionally heterogeneous changes across multiple scales, from synapses to macroscale white matter pathways. However, during this period, the developmental process of multiscale structural architecture, its association with cortical morphological changes, and its role in the maturation of functional organization remain largely unknown. Here, using two independent multimodal imaging developmental datasets aged 6-14 years, we investigated developmental process of multiscale cortical organization by constructing an in vivo multiscale structural connectome model incorporating white matter tractography, cortico-cortical proximity, and microstructural similarity. By employing the gradient mapping method, the principal gradient derived from the multiscale structural connectome effectively recapitulated the sensory-association axis. Our findings revealed a continuous expansion of the multiscale structural gradient space during development, characterized by enhanced differentiation between primary sensory and higher-order transmodal regions along the principal gradient. This age-related differentiation paralleled regionally heterogeneous changes in cortical morphology. Furthermore, the developmental changes in coupling between multiscale structural and functional connectivity were correlated with functional specialization refinement, as evidenced by changes in the participation coefficient. Notably, the differentiation of the principal multiscale structural gradient was associated with improved cognitive abilities, such as enhanced working memory and attention performance, and potentially underpinned by synaptic and hormone-related biological processes. These findings advance our understanding of the intricate maturation process of brain structural organization and its implications for cognitive performance.
从童年到青春期,人类大脑的结构组织在多个尺度上经历动态且区域异质性的变化,从突触到宏观尺度的白质通路。然而,在此期间,多尺度结构架构的发育过程、其与皮质形态变化的关联以及其在功能组织成熟中的作用仍 largely 未知。在这里,我们使用两个独立的 6 - 14 岁多模态成像发育数据集,通过构建一个结合白质纤维束成像、皮质 - 皮质邻近性和微观结构相似性的体内多尺度结构连接组模型,研究了多尺度皮质组织的发育过程。通过采用梯度映射方法,从多尺度结构连接组导出的主梯度有效地概括了感觉 - 关联轴。我们的研究结果表明,发育过程中多尺度结构梯度空间持续扩展,其特征是沿着主梯度,初级感觉区域和高阶跨模态区域之间的分化增强。这种与年龄相关的分化与皮质形态的区域异质性变化平行。此外,多尺度结构和功能连接之间耦合的发育变化与功能专业化细化相关,参与系数的变化证明了这一点。值得注意的是,主要多尺度结构梯度的分化与认知能力的提高相关,如工作记忆和注意力表现的增强,并且可能由突触和激素相关的生物学过程支撑。这些发现推进了我们对大脑结构组织复杂成熟过程及其对认知表现影响的理解。