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Dynamic whole-brain metabolic connectivity during vestibular compensation in the rat
NeuroImage ( IF 5.7 ) Pub Date : 2021-02-01 , DOI: 10.1016/j.neuroimage.2020.117588
Maximilian Grosch , Magdalena Lindner , Peter Bartenstein , Thomas Brandt , Marianne Dieterich , Sibylle Ziegler , Andreas Zwergal

Unilateral damage to the inner ear results in an acute vestibular syndrome, which is compensated within days to weeks due to adaptive cerebral plasticity. This process, called central vestibular compensation (VC), involves a wide range of functional and structural mechanisms at the cellular and network level. The short-term dynamics of whole-brain functional network recruitment and recalibration during VC has not been depicted in vivo. The purpose of this study was to investigate the interplay of separate and distinct brain regions and in vivo networks in the course of VC by sequential [18F]-FDG-PET-based statistical and graph theoretical analysis with the aim of revealing the metabolic connectome before and 1, 3, 7, and 15 days post unilateral labyrinthectomy (UL) in the rat. Temporal changes in metabolic brain connectivity were determined by Pearson's correlation (|r| > 0.5, p < 0.001) of regional cerebral glucose metabolism (rCGM) in 57 segmented brain regions. Metabolic connectivity analysis was compared to univariate voxel-wise statistical analysis of rCGM over time and to behavioral scores of static and dynamic sensorimotor recovery. Univariate statistical analysis revealed an ipsilesional relative rCGM decrease (compared to baseline) and a contralesional rCGM increase in vestibular and limbic networks and an increase in bilateral cerebellar and sensorimotor networks. Quantitative analysis of the metabolic connections showed a maximal increase from baseline to day 3 post UL (interhemispheric: 2-fold, ipsilesional: 3-fold, contralesional: 12-fold) and a gradual decline until day 15 post UL, which paralleled the dynamics of vestibular symptoms. In graph theoretical analysis, an increase in connectivity occurred especially within brain regions associated with brainstem-cerebellar and thalamocortical vestibular networks and cortical sensorimotor networks. At the symptom peak (day 3 post UL), brain networks were found to be organized in large ensembles of distinct and highly connected hubs of brain regions, which separated again with progressing VC. Thus, we found rapid changes in network organization at the subcortical and cortical level and in both hemispheres, which may indicate an initial functional substitution of vestibular loss and subsequent recalibration and reorganization of sensorimotor networks during VC.

中文翻译:

大鼠前庭代偿期间的动态全脑代谢连接

内耳的单侧损伤导致急性前庭综合征,由于适应性脑可塑性,该综合征可在数天至数周内得到补偿。这个过程称为中央前庭代偿 (VC),涉及细胞和网络级别的广泛功能和结构机制。VC 期间全脑功能网络募集和重新校准的短期动态尚未在体内描述。本研究的目的是通过基于连续 [18F]-FDG-PET 的统计和图论分析研究 VC 过程中独立和不同的大脑区域与体内网络的相互作用,目的是揭示之前的代谢连接组。大鼠单侧迷路切除术 (UL) 后 1、3、7 和 15 天。大脑代谢连接的时间变化由皮尔逊相关性 (|r| > 0.5, p < 0.001) 在 57 个分段大脑区域中的局部脑葡萄糖代谢 (rCGM) 确定。将代谢连接分析与 rCGM 随时间的单变量体素统计分析以及静态和动态感觉运动恢复的行为评分进行比较。单变量统计分析显示同侧相对 rCGM 减少(与基线相比)和前庭和边缘网络的对侧 rCGM 增加以及双侧小脑和感觉运动网络的增加。代谢联系的定量分析显示从基线到 UL 后第 3 天的最大增加(半球间:2 倍,同侧:3 倍,对侧:12 倍)并且逐渐下降,直到 UL 后第 15 天,这与前庭症状的动态平行。在图论分析中,连接性的增加尤其发生在与脑干-小脑和丘脑皮质前庭网络和皮质感觉运动网络相关的大脑区域内。在症状高峰期(UL 后第 3 天),发现大脑网络被组织成由不同且高度连接的大脑区域集线器组成的大型集合,随着 VC 的进展,这些集线器再次分离。因此,我们发现皮层下和皮层水平以及两个半球的网络组织发生了快速变化,这可能表明前庭丧失的初始功能替代以及随后 VC 期间感觉运动网络的重新校准和重组。连接性的增加尤其发生在与脑干-小脑和丘脑皮质前庭网络和皮质感觉运动网络相关的大脑区域内。在症状高峰期(UL 后第 3 天),发现大脑网络被组织成由不同且高度连接的大脑区域集线器组成的大型集合,随着 VC 的进展,这些集线器再次分离。因此,我们发现皮层下和皮层水平以及两个半球的网络组织发生了快速变化,这可能表明前庭丧失的初始功能替代以及随后 VC 期间感觉运动网络的重新校准和重组。连接性的增加尤其发生在与脑干-小脑和丘脑皮质前庭网络和皮质感觉运动网络相关的大脑区域内。在症状高峰期(UL 后第 3 天),发现大脑网络被组织成由不同且高度连接的大脑区域集线器组成的大型集合,随着 VC 的进展,这些集线器再次分离。因此,我们发现皮层下和皮层水平以及两个半球的网络组织发生了快速变化,这可能表明前庭丧失的初始功能替代以及随后 VC 期间感觉运动网络的重新校准和重组。发现大脑网络被组织成由不同且高度连接的大脑区域中心组成的大型集合,随着 VC 的进展,这些中心再次分离。因此,我们发现皮层下和皮层水平以及两个半球的网络组织发生了快速变化,这可能表明前庭丧失的初始功能替代以及随后 VC 期间感觉运动网络的重新校准和重组。发现大脑网络被组织成由不同且高度连接的大脑区域中心组成的大型集合,随着 VC 的进展,这些中心再次分离。因此,我们发现皮层下和皮层水平以及两个半球的网络组织发生了快速变化,这可能表明前庭丧失的初始功能替代以及随后 VC 期间感觉运动网络的重新校准和重组。
更新日期:2021-02-01
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