Language Functional Connectivity Alterations During Resting State in Brain Arteriovenous Malformation Patients

IF 5 1区医学 Q1 NEUROSCIENCES

CNS Neuroscience & Therapeutics Pub Date : 2025-09-05 DOI:10.1111/cns.70602

Xiaofeng Deng, Qiji Shi, Zekun Han, Shuo Wang, Yong Cao, Xiaolin Chen, Yan Zhang, Bo Wang, Minyu Jian, Fangrong Zong, Jizong Zhao

{"title":"Language Functional Connectivity Alterations During Resting State in Brain Arteriovenous Malformation Patients","authors":"Xiaofeng Deng, Qiji Shi, Zekun Han, Shuo Wang, Yong Cao, Xiaolin Chen, Yan Zhang, Bo Wang, Minyu Jian, Fangrong Zong, Jizong Zhao","doi":"10.1111/cns.70602","DOIUrl":null,"url":null,"abstract":"<div>\n \n \n <section>\n \n <h3> Objectives</h3>\n \n <p>Unruptured brain arteriovenous malformations (AVMs) typically do not cause aphasia, even when the traditional language areas are affected by the nidus. We attempted to elucidate its language reorganization mechanism by analyzing the alterations in functional connectivity using functional connectivity (FC) and track-weighted static functional connectivity (TW-sFC) approaches.</p>\n </section>\n \n <section>\n \n <h3> Methods</h3>\n \n <p>This cross-sectional study prospectively enrolled patients with AVMs involving left-hemisphere language areas and healthy controls. All participants underwent resting-state functional magnetic resonance imaging (rs-fMRI) and diffusion tensor imaging scans. Conventional FC analysis was used to investigate the spatially segregated functional connectivity in the gray matter, and the TW-sFC method was applied to explore the functional connectivity constrained by the white matter.</p>\n </section>\n \n <section>\n \n <h3> Results</h3>\n \n <p>34 AVM patients with lesions involving the left cerebral hemisphere and 27 healthy subjects were included. FC analysis findings revealed decreased FC intensity between the left-hemisphere language-associated regions and their right-hemisphere homologs in AVM patients. Additionally, increased FC intensity was observed between the anterior cingulate cortex (ACC) and the language-related areas in bilateral cerebellar hemispheres (lobule VIII, VIIb, Crus I, and Crus II). The TW-sFC results demonstrated increased intensity in multiple right-hemisphere fiber bundles, the left anterior thalamic radiation (ATR) and the callosum.</p>\n </section>\n \n <section>\n \n <h3> Conclusions</h3>\n \n <p>Three factors may contribute to maintaining intact language function in AVM patients, including the weakened inhibitory effect from the left dominant cerebral hemisphere over the right cerebral hemisphere leading to activation of the potential language functions of the right cerebral hemisphere (inter-cerebral connection reorganization), the functional upregulation of the cerebral language areas by cerebellar language-related brain regions via ACC (cerebrocerebellar connection reorganization), as well as the enhanced functions of the brain areas surrounding the lesion in the left cerebral hemisphere (intracerebral connection reorganization).</p>\n </section>\n \n <section>\n \n <h3> Trial Registration</h3>\n \n <p>This study is registered in the Chinese Trial Registry (clinical trial number: ChiCTR1900020993)</p>\n </section>\n </div>","PeriodicalId":154,"journal":{"name":"CNS Neuroscience & Therapeutics","volume":"31 9","pages":""},"PeriodicalIF":5.0000,"publicationDate":"2025-09-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/cns.70602","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"CNS Neuroscience & Therapeutics","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/cns.70602","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}

引用次数: 0

Abstract

Objectives

Unruptured brain arteriovenous malformations (AVMs) typically do not cause aphasia, even when the traditional language areas are affected by the nidus. We attempted to elucidate its language reorganization mechanism by analyzing the alterations in functional connectivity using functional connectivity (FC) and track-weighted static functional connectivity (TW-sFC) approaches.

Methods

This cross-sectional study prospectively enrolled patients with AVMs involving left-hemisphere language areas and healthy controls. All participants underwent resting-state functional magnetic resonance imaging (rs-fMRI) and diffusion tensor imaging scans. Conventional FC analysis was used to investigate the spatially segregated functional connectivity in the gray matter, and the TW-sFC method was applied to explore the functional connectivity constrained by the white matter.

Results

34 AVM patients with lesions involving the left cerebral hemisphere and 27 healthy subjects were included. FC analysis findings revealed decreased FC intensity between the left-hemisphere language-associated regions and their right-hemisphere homologs in AVM patients. Additionally, increased FC intensity was observed between the anterior cingulate cortex (ACC) and the language-related areas in bilateral cerebellar hemispheres (lobule VIII, VIIb, Crus I, and Crus II). The TW-sFC results demonstrated increased intensity in multiple right-hemisphere fiber bundles, the left anterior thalamic radiation (ATR) and the callosum.

Conclusions

Three factors may contribute to maintaining intact language function in AVM patients, including the weakened inhibitory effect from the left dominant cerebral hemisphere over the right cerebral hemisphere leading to activation of the potential language functions of the right cerebral hemisphere (inter-cerebral connection reorganization), the functional upregulation of the cerebral language areas by cerebellar language-related brain regions via ACC (cerebrocerebellar connection reorganization), as well as the enhanced functions of the brain areas surrounding the lesion in the left cerebral hemisphere (intracerebral connection reorganization).

Trial Registration

This study is registered in the Chinese Trial Registry (clinical trial number: ChiCTR1900020993)

Abstract Image

查看原文本刊更多论文

脑动静脉畸形患者静息状态下语言功能连通性的改变

目的未破裂的脑动静脉畸形（AVMs）通常不会导致失语，即使传统的语言区受到病灶的影响。我们试图通过功能连接（FC）和轨迹加权静态功能连接（TW-sFC）方法分析其功能连接的变化来阐明其语言重组机制。方法本横断面研究前瞻性纳入左半球语言区的动静脉畸形患者和健康对照。所有参与者接受静息状态功能磁共振成像（rs-fMRI）和扩散张量成像扫描。传统的FC分析方法用于研究灰质中空间分离的功能连通性，TW-sFC方法用于研究受白质约束的功能连通性。结果包括34例左脑半球病变的AVM患者和27例正常人。FC分析结果显示，AVM患者左半球语言相关区域和右半球同源区域之间的FC强度降低。此外，在前扣带皮层（ACC）和双侧小脑半球的语言相关区域（小叶VIII， vib， Crus I和Crus II）之间观察到FC强度增加。TW-sFC结果显示右半球多个纤维束、左丘脑前辐射（ATR）和胼胝体的强度增加。结论AVM患者保持完整语言功能可能有三个因素：左优势脑半球对右脑半球的抑制作用减弱，导致右脑潜在语言功能激活（脑间连接重组）；小脑语言相关脑区通过ACC（脑小脑连接重组）上调大脑语言区功能，以及左脑半球病变周围脑区功能增强（脑内连接重组）。本研究已在中国试验注册中心注册（临床试验号：ChiCTR1900020993）。

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

CNS Neuroscience & Therapeutics 医学-神经科学

CiteScore

7.30

自引率

12.70%

发文量

240

审稿时长

2 months

期刊介绍： CNS Neuroscience & Therapeutics provides a medium for rapid publication of original clinical, experimental, and translational research papers, timely reviews and reports of novel findings of therapeutic relevance to the central nervous system, as well as papers related to clinical pharmacology, drug development and novel methodologies for drug evaluation. The journal focuses on neurological and psychiatric diseases such as stroke, Parkinson’s disease, Alzheimer’s disease, depression, schizophrenia, epilepsy, and drug abuse.