Weak Higher-Order Interactions in Macroscopic Functional Networks of the Resting Brain

Weak Higher-Order Interactions in Macroscopic Functional Networks of the Resting Brain
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静息大脑宏观功能网络中的弱高阶相互作用

DOI:
10.1523/jneurosci.0451-17.2017
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发表时间:
2017
期刊:
The Journal of Neuroscience
影响因子:
--
通讯作者:
Shan Yu
Shan Yu
中科院分区:
其他
文献类型:
--
作者:
Xuhui Huang;Kaibin Xu;Congying Chu;Tianzi Jiang;Shan Yu

文献摘要

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不同脑区之间的相互作用通常通过功能连通性(FC)分析来检测,这完全基于测量活动的两两相关性。然而,超越两两水平的相互作用,即高阶相互作用(hoi),对于理解许多复杂系统的行为至关重要。到目前为止,hoi是否存在于大脑区域以及它们如何影响大脑活动在很大程度上仍然是难以捉摸的。为了解决这些问题,在这里,我们分析了100名人类受试者(46名男性和54名女性)在静息状态下从6个典型的大脑宏观功能网络记录的血氧水平依赖(BOLD)信号。通过检查二值化的BOLD信号,我们发现无论网络大小、拓扑结构、空间接近程度、空间尺度以及是否对全局信号进行回归,单个网络内部和网络之间的hoi都非常弱。为了研究弱hoi的潜在机制,我们分析了网络模型的动力学,并发现在模型的整体动态特征与经验数据相似且接近线性波动状态的情况下,在广泛的关键参数范围内,hoi通常较弱。我们的研究结果表明,弱HOI可能是大脑宏观功能网络的一般特性,这意味着在这种规模上成对相互作用在塑造大脑活动方面占主导地位,并保证了广泛使用的基于成对的FC方法的有效性。解释大脑不同区域的活动如何通过相互作用进行协调,对于揭示大脑各种功能的潜在机制至关重要。传统上,这种交互结构通常使用基于成对的功能网络分析来研究。目前尚不清楚是否超过两两水平的相互作用(高阶相互作用或hoi)在这一过程中起任何作用。在这里,我们表明hoi在宏观脑网络中通常是弱的。我们还提出了一种可能的动力机制,可能是这种现象的基础。这些结果为广泛使用的基于成对的方法在分析大脑网络中的有效性提供了合理的解释。更重要的是,它揭示了一个以前未知的,大脑宏观功能系统的简单组织。
Interactions among different brain regions are usually examined through functional connectivity (FC) analysis, which is exclusively based on measuring pairwise correlations in activities. However, interactions beyond the pairwise level, that is, higher-order interactions (HOIs), are vital in understanding the behavior of many complex systems. So far, whether HOIs exist among brain regions and how they can affect the brain's activities remains largely elusive. To address these issues, here, we analyzed blood oxygenation level-dependent (BOLD) signals recorded from six typical macroscopic functional networks of the brain in 100 human subjects (46 males and 54 females) during the resting state. Through examining the binarized BOLD signals, we found that HOIs within and across individual networks were both very weak regardless of the network size, topology, degree of spatial proximity, spatial scales, and whether the global signal was regressed. To investigate the potential mechanisms underlying the weak HOIs, we analyzed the dynamics of a network model and also found that HOIs were generally weak within a wide range of key parameters provided that the overall dynamic feature of the model was similar to the empirical data and it was operating close to a linear fluctuation regime. Our results suggest that weak HOI may be a general property of brain's macroscopic functional networks, which implies the dominance of pairwise interactions in shaping brain activities at such a scale and warrants the validity of widely used pairwise-based FC approaches. SIGNIFICANCE STATEMENT To explain how activities of different brain areas are coordinated through interactions is essential to revealing the mechanisms underlying various brain functions. Traditionally, such an interaction structure is commonly studied using pairwise-based functional network analyses. It is unclear whether the interactions beyond the pairwise level (higher-order interactions or HOIs) play any role in this process. Here, we show that HOIs are generally weak in macroscopic brain networks. We also suggest a possible dynamical mechanism that may underlie this phenomenon. These results provide plausible explanation for the effectiveness of widely used pairwise-based approaches in analyzing brain networks. More importantly, it reveals a previously unknown, simple organization of the brain's macroscopic functional systems.