Preterm birth leads to impaired rich-club organization and fronto-paralimbic/limbic structural connectivity in newborns
Preterm birth leads to impaired rich-club organization and fronto-paralimbic/limbic structural connectivity in newborns
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DOI：
10.1016/j.neuroimage.2020.117440
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发表时间：
2021-01-15
期刊：
影响因子：
5.7
通讯作者：
Huppi, Petra S.
中科院分区：
文献类型：
--
作者：
de Almeida, Joana Sa;Meskaldji, Djalel-Eddine;Huppi, Petra S.
早产在大脑生长和组织的关键时期扰乱大脑发育，并且已知与神经发育障碍的风险增加有关。研究早产儿全脑结构连接的改变可能会更好地理解与该人群中观察到的后期神经认知缺陷相关的神经生物学机制，我们旨在研究早产对足月新生儿全脑结构网络组织的影响。在这项队列研究中，24名足月相当年龄的极早产儿（VPT-TEA）和14名足月（FT）新生儿在足月时接受了脑MRI检查，包括T2加权成像和弥散MRI，用于通过应用概率约束球形去卷积全脑纤维束成像重建脑连接体。大脑网络的拓扑特性通过图论方法进行了量化。总体而言，VPT-TEA婴儿的大脑网络表现出增加的分离和减少的整合能力，表现为增加的聚类系数，增加的模块性，增加的特征路径长度，减少的全局效率和减少的丰富俱乐部系数。此外，与FT相比，VPT-TEA婴儿在各种皮质-皮质、皮质-皮质下和皮质下内网络中的连接强度降低，其中大多数是大脑半球内的额-额边缘和额-边缘。VPT-TEA婴儿的半球间连接也减少了，即通过连接到左楔前叶或左背扣带回-这两个区域被发现是FT的枢纽，但不是VPT-TEA婴儿。此外，VPT-TEA组的默认模式网络（DMN）的后部区域，即楔前叶和后扣带回的结构连接性降低。我们的发现表明，与FT婴儿相比，VPT-TEA婴儿的大脑网络显示出更多的模块化，弱化了丰富的俱乐部连接和降低了整体效率，这表明从局部结构的延迟过渡，专注于短程连接，到一个更分散的架构，在这些婴儿中有有效的远程连接。在额边缘/边缘和后部DMN区域的连接中断可能是以前在早产儿人群中报道的行为和社会认知困难的基础。
Prematurity disrupts brain development during a critical period of brain growth and organization and is known to be associated with an increased risk of neurodevelopmental impairments. Investigating whole-brain structural connectivity alterations accompanying preterm birth may provide a better comprehension of the neurobiological mechanisms related to the later neurocognitive deficits observed in this population.Using a connectome approach, we aimed to study the impact of prematurity on neonatal whole-brain structural network organization at term-equivalent age. In this cohort study, twenty-four very preterm infants at term-equivalent age (VPT-TEA) and fourteen full-term (FT) newborns underwent a brain MRI exam at term age, comprising T2-weighted imaging and diffusion MRI, used to reconstruct brain connectomes by applying probabilistic constrained spherical deconvolution whole-brain tractography. The topological properties of brain networks were quantified through a graph-theoretical approach. Furthermore, edge-wise connectivity strength was compared between groups.Overall, VPT-TEA infants' brain networks evidenced increased segregation and decreased integration capacity, revealed by an increased clustering coefficient, increased modularity, increased characteristic path length, decreased global efficiency and diminished rich-club coefficient. Furthermore, in comparison to FT, VPT-TEA infants had decreased connectivity strength in various cortico-cortical, cortico-subcortical and intra-subcortical networks, the majority of them being intra-hemispheric fronto-paralimbic and fronto-limbic. Inter-hemispheric connectivity was also decreased in VPT-TEA infants, namely through connections linking to the left precuneus or left dorsal cingulate gyrus - two regions that were found to be hubs in FT but not in VPT-TEA infants. Moreover, posterior regions from Default-Mode-Network (DMN), namely precuneus and posterior cingulate gyrus, had decreased structural connectivity in VPT-TEA group.Our finding that VPT-TEA infants' brain networks displayed increased modularity, weakened rich-club connectivity and diminished global efficiency compared to FT infants suggests a delayed transition from a local architecture, focused on short-range connections, to a more distributed architecture with efficient long-range connections in those infants. The disruption of connectivity in fronto-paralimbic/limbic and posterior DMN regions might underlie the behavioral and social cognition difficulties previously reported in the preterm population.