Nonoptimal component placement of the human connectome supports variable brain dynamics.
Nonoptimal component placement of the human connectome supports variable brain dynamics.
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DOI：
10.1162/netn_a_00282
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发表时间：
2023
影响因子：
4.7
通讯作者：
Kaiser, Marcus
中科院分区：
文献类型：
--
作者：
Hayward, Christopher James;Huo, Siyu;Chen, Xue;Kaiser, Marcus
神经系统是由多个约束塑造的，在区域通信与建立和维护物理连接的成本之间取得平衡。有人建议减少神经投射的长度，减少它们对生物体的空间和新陈代谢的影响。然而，长距离连接在不同物种的连接中很普遍，因此，另一种理论提出，大脑通过适当的区域定位来最小化总的布线长度，称为组件放置优化，而不是通过重新布线来减少长度。以前对非人类灵长类动物的研究通过确定非最佳组件位置来驳斥这一观点，在这种位置上，大脑区域的空间重新排列导致总布线长度减少。在这里，我们第一次在人类身上测试组件放置优化。我们显示了来自Human Connectome Project的样本中所有受试者(N=280；年龄22-30岁；138名女性)的非最佳组件放置，这表明存在限制-例如区域之间处理步骤的减少-与高昂的空间和新陈代谢成本竞争。此外，通过模拟大脑区域之间的交流，我们认为这种次优的组件布置支持有利于认知的动态变化。大脑的解剖组织是由相互竞争的限制因素塑造的，这些限制因素既要改善大脑功能，又要降低连接组布线的成本。考虑到这种权衡，我们发现人脑中的区域并不能最小化它们之间的连接总长度。这种非最佳的组织结构主要归因于额叶和枕叶/顶叶，它们之间的连接充当了让遥远的大脑区域进行交流的捷径。通过使用大脑活动模型，我们认为连接体的这种次优空间布置促进了大脑活动的波动，使大脑能够进行灵活的行为反应。总而言之，这突出表明，尽管大脑结构在空间上不是最优的，但它可能提供支持有效认知的动态优势。
Neural systems are shaped by multiple constraints, balancing region communication with the cost of establishing and maintaining physical connections. It has been suggested that the lengths of neural projections be minimized, reducing their spatial and metabolic impact on the organism. However, long-range connections are prevalent in the connectomes across various species, and thus, rather than rewiring connections to reduce length, an alternative theory proposes that the brain minimizes total wiring length through a suitable positioning of regions, termed component placement optimization. Previous studies in nonhuman primates have refuted this idea by identifying a nonoptimal component placement, where a spatial rearrangement of brain regions in silico leads to a reduced total wiring length. Here, for the first time in humans, we test for component placement optimization. We show a nonoptimal component placement for all subjects in our sample from the Human Connectome Project (N = 280; aged 22–30 years; 138 females), suggesting the presence of constraints—such as the reduction of processing steps between regions—that compete with the elevated spatial and metabolic costs. Additionally, by simulating communication between brain regions, we argue that this suboptimal component placement supports dynamics that benefit cognition. The anatomical organization of the brain is shaped by competing constraints for improving brain function while reducing the costs for connectome wiring. Concerning this trade-off, we find that regions within the human brain are not positioned to minimize the total length of their connections. This nonoptimal organization is mainly attributed to frontal and occipital/parietal lobes, with connections between them acting as shortcuts allowing distant brain areas to communicate. By using a model of brain activity, we argue that this suboptimal spatial arrangement of the connectome promotes fluctuations in brain activity, enabling the brain to undertake flexible behavioral responses. Altogether, this highlights that brain structure, while spatially suboptimal, may offer dynamic advantages that support effective cognition.