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睡眠剥夺后连接中枢的多样性增强:来自扩散和功能磁共振成像的证据。

Enhanced diversity on connector hubs following sleep deprivation: Evidence from diffusion and functional magnetic resonance imaging.

机构信息

Sleep and NeuroImaging Center, Faculty of Psychology, Southwest University, Chongqing 400715, China; Key Laboratory of Cognition and Personality (Ministry of Education), Chongqing 400715, China.

Faculty of Psychology, Technische Universität Dresden, Dresden, Germany.

出版信息

Neuroimage. 2024 Oct 1;299:120837. doi: 10.1016/j.neuroimage.2024.120837. Epub 2024 Sep 4.

Abstract

Sleep deprivation has been demonstrated to exert widespread and intricate impacts on the brain network. The human brain network is a modular network composed of interconnected nodes. This network consists of provincial hubs and connector hubs, with provincial hubs having diverse connectivities within their own modules, while connector hubs distribute their connectivities across different modules. The latter is crucial for integrating information from various modules and ensuring the normal functioning of the modular brain. However, there has been a lack of systematic investigation into the impact of sleep deprivation on brain connector hubs. In this study, we utilized functional connectivity from resting-state functional magnetic resonance imaging, as well as structural connectivity from diffusion-weighted imaging, to systematically explore the variation of connector hub properties in the cerebral cortex after one night of sleep deprivation. The normalized participation coefficients (PCnorm) were utilized to identify connector hubs. In both the functional and structural networks, connector hubs exhibited a significant increase in average PCnorm, indicating the diversity enhancement of the connector hub following sleep deprivation. This enhancement is associated with increased network cost, reduced modularity, and decreased small-worldness, but enhanced global efficiency. This may potentially signify a compensatory mechanism within the brain following sleep deprivation. The significantly affected connector hubs were primarily observed in both the Control Network and Salience Network. We believe that the observed results reflect the increasing demand on the brain to invest more effort at preventing performance deterioration after sleep loss, in exchange for increased communication efficiency, especially involving systems responsible for neural resource allocation and cognitive control. These results have been replicated in an independent dataset. In conclusion, this study has enhanced our understanding of the compensatory mechanism in the brain response to sleep deprivation. This compensation is characterized by an enhancement in the connector hubs responsible for inter-modular communication, especially those related to neural resource and cognitive control. As a result, this compensation comes with a higher network cost but leads to an improvement in global communication efficiency, akin to a more random-like network manner.

摘要

睡眠剥夺已被证明对大脑网络产生广泛而复杂的影响。人类大脑网络是一个由相互连接的节点组成的模块化网络。这个网络由局部枢纽和连接枢纽组成,局部枢纽在其自身模块内具有不同的连接度,而连接枢纽则在不同的模块之间分配其连接度。后者对于整合来自不同模块的信息和确保模块化大脑的正常功能至关重要。然而,目前还缺乏系统研究睡眠剥夺对大脑连接枢纽的影响。在这项研究中,我们利用静息态功能磁共振成像的功能连接,以及扩散加权成像的结构连接,系统地研究了一夜睡眠剥夺后大脑皮层中连接枢纽属性的变化。我们使用归一化参与系数(PCnorm)来识别连接枢纽。在功能和结构网络中,连接枢纽的平均 PCnorm 显著增加,表明睡眠剥夺后连接枢纽的多样性增强。这种增强与网络成本的增加、模块性的降低和小世界性的降低有关,但全局效率增加。这可能是大脑在睡眠剥夺后的一种代偿机制。受显著影响的连接枢纽主要出现在控制网络和突显网络中。我们认为,观察到的结果反映了大脑在睡眠剥夺后为了防止性能下降而增加投入的需求增加,以换取更高的通信效率,特别是涉及负责神经资源分配和认知控制的系统。这些结果在一个独立的数据集上得到了复制。总之,本研究增强了我们对大脑对睡眠剥夺反应的代偿机制的理解。这种补偿的特点是增强了负责模块间通信的连接枢纽,特别是那些与神经资源和认知控制相关的连接枢纽。因此,这种补偿伴随着更高的网络成本,但导致全局通信效率的提高,类似于更随机的网络方式。

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