Cognitive Control Network and Language Reorganization in Patients with Brain Tumors.

Luca Pasquini, Antonio Napolitano, Leonardo Spitoni, Maurizio Schmid, Francesco Dellepiane, Mehrnaz Jenabi, Kyung Peck, Andrei Holodny
{"title":"Cognitive Control Network and Language Reorganization in Patients with Brain Tumors.","authors":"Luca Pasquini, Antonio Napolitano, Leonardo Spitoni, Maurizio Schmid, Francesco Dellepiane, Mehrnaz Jenabi, Kyung Peck, Andrei Holodny","doi":"10.3174/ajnr.A8638","DOIUrl":null,"url":null,"abstract":"<p><strong>Background and purpose: </strong>The interaction between language and other cognitive networks in patients harboring brain tumors is poorly understood. We studied the modification of the cognitive control network (CCN) induced by brain tumors and its participation in language reorganization. We hypothesized that patients with brain tumors and reorganized language would show a modification of the CCN compared with patients who remain left dominant.</p><p><strong>Materials and methods: </strong>Patients were selected with the criteria: newly diagnosed, pathologically-confirmed left-hemispheric tumor; single lesions; right-handedness; task-based and resting-state fMRI; no artifacts. Age-matched healthy controls (HC) were recruited from open-source databases. Language laterality was calculated by using task-based fMRI. We obtained the CCN through ad hoc independent component analysis on resting-state fMRI. Differences in CCN between patients and HC were characterized by cosine similarity (CS) and earth mover's distance (EMD). Changes related to language reorganization and patients' speech were assessed with the <i>t</i> test (<i>P</i> < .05). Results were corrected for multiple comparisons.</p><p><strong>Results: </strong>One hundred forty-two right-handed patients (35 low-grade and 88 high-grade gliomas; 19 metastases) and 184 HC were included. Two independent components of the CCN were obtained. The <i>t</i> test confirmed significant effects of lateralization on the CCN (<i>P</i> = .004). Modification of CCN was associated with fewer speech deficits 1 week after surgery (<i>P</i> = .005).</p><p><strong>Conclusions: </strong>This study provides evidence that modifications of CCN occur in the setting of language reorganization. Patients exhibiting these modifications perform better at speech evaluation after surgery, suggesting a role of cognitive control in compensating for speech deficits when language reorganizes.</p>","PeriodicalId":93863,"journal":{"name":"AJNR. American journal of neuroradiology","volume":" ","pages":"1238-1248"},"PeriodicalIF":0.0000,"publicationDate":"2025-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12152808/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"AJNR. American journal of neuroradiology","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.3174/ajnr.A8638","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0

Abstract

Background and purpose: The interaction between language and other cognitive networks in patients harboring brain tumors is poorly understood. We studied the modification of the cognitive control network (CCN) induced by brain tumors and its participation in language reorganization. We hypothesized that patients with brain tumors and reorganized language would show a modification of the CCN compared with patients who remain left dominant.

Materials and methods: Patients were selected with the criteria: newly diagnosed, pathologically-confirmed left-hemispheric tumor; single lesions; right-handedness; task-based and resting-state fMRI; no artifacts. Age-matched healthy controls (HC) were recruited from open-source databases. Language laterality was calculated by using task-based fMRI. We obtained the CCN through ad hoc independent component analysis on resting-state fMRI. Differences in CCN between patients and HC were characterized by cosine similarity (CS) and earth mover's distance (EMD). Changes related to language reorganization and patients' speech were assessed with the t test (P < .05). Results were corrected for multiple comparisons.

Results: One hundred forty-two right-handed patients (35 low-grade and 88 high-grade gliomas; 19 metastases) and 184 HC were included. Two independent components of the CCN were obtained. The t test confirmed significant effects of lateralization on the CCN (P = .004). Modification of CCN was associated with fewer speech deficits 1 week after surgery (P = .005).

Conclusions: This study provides evidence that modifications of CCN occur in the setting of language reorganization. Patients exhibiting these modifications perform better at speech evaluation after surgery, suggesting a role of cognitive control in compensating for speech deficits when language reorganizes.

脑肿瘤患者的认知控制网络与语言重组。
背景与目的:脑肿瘤患者的语言与其他认知网络之间的相互作用尚不清楚。我们研究了脑肿瘤诱导的认知控制网络(CCN)的改变及其在语言重组中的作用。我们假设患有脑肿瘤和语言重组的患者与左显性患者相比,CCN会发生改变。材料和方法:患者入选标准:新诊断、病理证实的左半球肿瘤;单一的病变;正确的用手习惯;任务型和静息态fMRI;没有工件。从开源数据库中招募年龄匹配的健康对照(HC)。使用基于任务的功能磁共振成像计算语言侧性。我们通过静息状态fMRI的特设独立分量分析获得CCN。通过余弦相似度(CS)和推土机距离(EMD)表征患者与HC之间CCN的差异。结果:142例右撇子患者(低级别胶质瘤35例,高级别胶质瘤88例;19例转移)和184例HC。得到了CCN的两个独立分量。t检验证实侧化对CCN有显著影响(p=0.004)。CCN改良与术后1周言语缺陷减少相关(p=0.005)。结论:本研究提供了CCN在语言重组环境下发生改变的证据。表现出这些改变的患者在手术后的言语评估中表现更好,这表明认知控制在语言重组时补偿言语缺陷的作用。缩写:AD =非典型显性;CCN =认知控制网络;CS =余弦相似性;EMD =推土机距离;功能磁共振成像;组信息导向ICA;HGG =高级胶质瘤;LD =左显性;LGG =低级别胶质瘤;LI=侧度指数;ROI =兴趣区域;rsn =静息状态网络。
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
自引率
0.00%
发文量
0
×
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