Neural dynamics impairments in amyotrophic lateral sclerosis patients and their associations with clinical characteristics: An observational cohort study

IF 3.7 3区 医学 Q2 NEUROSCIENCES
Wei Zheng , Jing Luo , Yong Yang , Xia Guo , Fei Song , Feng Li , Fei Xiao
{"title":"Neural dynamics impairments in amyotrophic lateral sclerosis patients and their associations with clinical characteristics: An observational cohort study","authors":"Wei Zheng ,&nbsp;Jing Luo ,&nbsp;Yong Yang ,&nbsp;Xia Guo ,&nbsp;Fei Song ,&nbsp;Feng Li ,&nbsp;Fei Xiao","doi":"10.1016/j.brainresbull.2025.111482","DOIUrl":null,"url":null,"abstract":"<div><h3>Background and purpose</h3><div>Amyotrophic lateral sclerosis (ALS) is a fatal neurodegenerative disease of the central nervous system. It remains unclear whether pathological changes in ALS can lead to abnormalities in neural dynamics and how these abnormalities relate to key clinical characteristics of ALS.</div></div><div><h3>Methods</h3><div>Nonlinear neural dynamics analyses of electroencephalography (EEG) sensorimotor channels were conducted using recurrence quantification analysis (RQA), permutation Lempel-Ziv complexity (PLZC), shannon entropy (ShannonE) and permutation entropy (PermEn). Whole-brain spatiotemporal topological dynamics were assessed using microstate analysis.</div></div><div><h3>Results</h3><div>The study shows that the nonlinear neural dynamics across all frequency bands in the sensorimotor channels of ALS patients are impaired (reduction in Shannon Entropy of Diagonal Line Length Distribution [ENTR]). Frequency-specific nonlinear neural dynamics indicate increased nonlinear neural dynamics in high-frequency bands (with increases in PLZC in beta2 (20–25 Hz)). Nonlinear neural dynamics in low-frequency bands decreases (with decreases in ShannonE in theta (4–7 Hz)) and is negatively correlated with disease duration. ENTR across all frequency bands and ShannonE in the theta band of the sensorimotor channels are potential protective factors for ALS. Furthermore, sensorimotor channel analysis shows a close relationship with whole-brain spatiotemporal topological neural dynamics. Duration A is positively correlated with RR, DET and ENTR, while Occurrence B is negatively correlated with it.</div></div><div><h3>Conclusions</h3><div>The study demonstrates widespread abnormalities in the neural dynamics of ALS, which are closely related to clinical characteristics of ALS. There is also a close relationship between the neural dynamics of sensorimotor channels and whole-brain spatiotemporal topological dynamics in ALS patients.</div></div>","PeriodicalId":9302,"journal":{"name":"Brain Research Bulletin","volume":"229 ","pages":"Article 111482"},"PeriodicalIF":3.7000,"publicationDate":"2025-07-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Brain Research Bulletin","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0361923025002941","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Background and purpose

Amyotrophic lateral sclerosis (ALS) is a fatal neurodegenerative disease of the central nervous system. It remains unclear whether pathological changes in ALS can lead to abnormalities in neural dynamics and how these abnormalities relate to key clinical characteristics of ALS.

Methods

Nonlinear neural dynamics analyses of electroencephalography (EEG) sensorimotor channels were conducted using recurrence quantification analysis (RQA), permutation Lempel-Ziv complexity (PLZC), shannon entropy (ShannonE) and permutation entropy (PermEn). Whole-brain spatiotemporal topological dynamics were assessed using microstate analysis.

Results

The study shows that the nonlinear neural dynamics across all frequency bands in the sensorimotor channels of ALS patients are impaired (reduction in Shannon Entropy of Diagonal Line Length Distribution [ENTR]). Frequency-specific nonlinear neural dynamics indicate increased nonlinear neural dynamics in high-frequency bands (with increases in PLZC in beta2 (20–25 Hz)). Nonlinear neural dynamics in low-frequency bands decreases (with decreases in ShannonE in theta (4–7 Hz)) and is negatively correlated with disease duration. ENTR across all frequency bands and ShannonE in the theta band of the sensorimotor channels are potential protective factors for ALS. Furthermore, sensorimotor channel analysis shows a close relationship with whole-brain spatiotemporal topological neural dynamics. Duration A is positively correlated with RR, DET and ENTR, while Occurrence B is negatively correlated with it.

Conclusions

The study demonstrates widespread abnormalities in the neural dynamics of ALS, which are closely related to clinical characteristics of ALS. There is also a close relationship between the neural dynamics of sensorimotor channels and whole-brain spatiotemporal topological dynamics in ALS patients.
肌萎缩侧索硬化症患者的神经动力学损伤及其与临床特征的关系:一项观察性队列研究
背景与目的肌萎缩性侧索硬化症(ALS)是一种致命的中枢神经系统退行性疾病。目前尚不清楚ALS的病理改变是否会导致神经动力学异常,以及这些异常与ALS的关键临床特征之间的关系。方法采用递归量化分析(RQA)、排列Lempel-Ziv复杂度(PLZC)、shannon熵(shanone)和排列熵(PermEn)对脑电图感觉运动通道进行非线性神经动力学分析。采用微态分析评估全脑时空拓扑动力学。结果研究表明,ALS患者感觉运动通道中所有频带的非线性神经动力学均受到损害(对角线长度分布香农熵(Shannon Entropy of Diagonal Line Length Distribution, ENTR)减小)。频率特异性非线性神经动力学表明,高频波段非线性神经动力学增加(β 2的PLZC增加(20-25 Hz))。低频带非线性神经动力学降低(theta(4-7 Hz)的shanone降低),并与病程负相关。所有频带的ENTR和感觉运动通道theta频带的ShannonE是ALS的潜在保护因素。此外,感觉运动通道分析显示与全脑时空拓扑神经动力学密切相关。病程A与RR、DET、ENTR呈正相关,病程B与RR、DET、ENTR呈负相关。结论肌萎缩侧索硬化症神经动力学异常广泛存在,与临床特征密切相关。肌萎缩侧索硬化症患者感觉运动通道的神经动力学与全脑时空拓扑动力学也有密切的关系。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Brain Research Bulletin
Brain Research Bulletin 医学-神经科学
CiteScore
6.90
自引率
2.60%
发文量
253
审稿时长
67 days
期刊介绍: The Brain Research Bulletin (BRB) aims to publish novel work that advances our knowledge of molecular and cellular mechanisms that underlie neural network properties associated with behavior, cognition and other brain functions during neurodevelopment and in the adult. Although clinical research is out of the Journal''s scope, the BRB also aims to publish translation research that provides insight into biological mechanisms and processes associated with neurodegeneration mechanisms, neurological diseases and neuropsychiatric disorders. The Journal is especially interested in research using novel methodologies, such as optogenetics, multielectrode array recordings and life imaging in wild-type and genetically-modified animal models, with the goal to advance our understanding of how neurons, glia and networks function in vivo.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术官方微信