行为变异额颞叶痴呆的执行功能障碍与显著性网络分离有关

IF 3.6 2区医学 Q2 NEUROIMAGING

Neuroimage-Clinical Pub Date : 2025-01-01 DOI:10.1016/j.nicl.2025.103853

Melanie A. Matyi , Hamsanandini Radhakrishnan , Christopher A. Olm , Jeffrey S. Phillips , Philip A. Cook , Emma Rhodes , James C. Gee , David J. Irwin , Corey T. McMillan , Lauren Massimo

{"title":"行为变异额颞叶痴呆的执行功能障碍与显著性网络分离有关","authors":"Melanie A. Matyi , Hamsanandini Radhakrishnan , Christopher A. Olm , Jeffrey S. Phillips , Philip A. Cook , Emma Rhodes , James C. Gee , David J. Irwin , Corey T. McMillan , Lauren Massimo","doi":"10.1016/j.nicl.2025.103853","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><div>The organization of the brain into distinct networks increases (i.e., differentiation) during development and decreases (i.e., de-differentiation) during healthy aging, changes that are associated with improvements and worsening of cognition, respectively. Given that behavioral variant frontotemporal degeneration (bvFTD) is a neurodegenerative disease associated with executive dysfunction and selective vulnerability of the salience network, we tested the hypotheses that bvFTD structural networks are de-differentiated compared to cognitively normal controls (CNC) and that network de-differentiation relates to worse executive function.</div></div><div><h3>Methods</h3><div>In a sample of 90 patients with bvFTD and 71 age-matched CNC with diffusion MRI data we generated probabilistic tractography maps and calculated system segregation, a metric that compares within-network to between-network connectivity, to reflect the extent to which brain networks were differentiated. Patients with bvFTD also completed tests of executive function (digit span backwards, phonemic fluency, category fluency) and a control task (lexical retrieval). We assessed group differences in system segregation, reflecting network differentiation, and, within bvFTD, associations between system segregation and neuropsychological test performance.</div></div><div><h3>Results</h3><div>Compared to CNC, patients with bvFTD exhibited lower system segregation of the salience (<em>p</em> < 0.001) and global brain network (<em>p</em> = 0.008). In bvFTD, lower salience network system segregation was associated with worse executive function (<em>p<sub>corrected</sub></em> = 0.021) but not lexical retrieval.</div></div><div><h3>Conclusions</h3><div>Results demonstrate associations between executive dysfunction and salience network de-differentiation in patients with bvFTD. Our findings indicate that brain network de-differentiation, reflecting reduced neural capacity for specialized processing, may contribute to the emergence of executive dysfunction in bvFTD.</div></div>","PeriodicalId":54359,"journal":{"name":"Neuroimage-Clinical","volume":"48 ","pages":"Article 103853"},"PeriodicalIF":3.6000,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Executive dysfunction relates to salience network desegregation in behavioural variant frontotemporal dementia\",\"authors\":\"Melanie A. Matyi , Hamsanandini Radhakrishnan , Christopher A. Olm , Jeffrey S. Phillips , Philip A. Cook , Emma Rhodes , James C. Gee , David J. Irwin , Corey T. McMillan , Lauren Massimo\",\"doi\":\"10.1016/j.nicl.2025.103853\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><h3>Background</h3><div>The organization of the brain into distinct networks increases (i.e., differentiation) during development and decreases (i.e., de-differentiation) during healthy aging, changes that are associated with improvements and worsening of cognition, respectively. Given that behavioral variant frontotemporal degeneration (bvFTD) is a neurodegenerative disease associated with executive dysfunction and selective vulnerability of the salience network, we tested the hypotheses that bvFTD structural networks are de-differentiated compared to cognitively normal controls (CNC) and that network de-differentiation relates to worse executive function.</div></div><div><h3>Methods</h3><div>In a sample of 90 patients with bvFTD and 71 age-matched CNC with diffusion MRI data we generated probabilistic tractography maps and calculated system segregation, a metric that compares within-network to between-network connectivity, to reflect the extent to which brain networks were differentiated. Patients with bvFTD also completed tests of executive function (digit span backwards, phonemic fluency, category fluency) and a control task (lexical retrieval). We assessed group differences in system segregation, reflecting network differentiation, and, within bvFTD, associations between system segregation and neuropsychological test performance.</div></div><div><h3>Results</h3><div>Compared to CNC, patients with bvFTD exhibited lower system segregation of the salience (<em>p</em> < 0.001) and global brain network (<em>p</em> = 0.008). In bvFTD, lower salience network system segregation was associated with worse executive function (<em>p<sub>corrected</sub></em> = 0.021) but not lexical retrieval.</div></div><div><h3>Conclusions</h3><div>Results demonstrate associations between executive dysfunction and salience network de-differentiation in patients with bvFTD. Our findings indicate that brain network de-differentiation, reflecting reduced neural capacity for specialized processing, may contribute to the emergence of executive dysfunction in bvFTD.</div></div>\",\"PeriodicalId\":54359,\"journal\":{\"name\":\"Neuroimage-Clinical\",\"volume\":\"48 \",\"pages\":\"Article 103853\"},\"PeriodicalIF\":3.6000,\"publicationDate\":\"2025-01-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Neuroimage-Clinical\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://www.sciencedirect.com/science/article/pii/S2213158225001238\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"NEUROIMAGING\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Neuroimage-Clinical","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2213158225001238","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"NEUROIMAGING","Score":null,"Total":0}

引用次数: 0

摘要

大脑组织成不同的网络在发育过程中增加（即分化），在健康衰老过程中减少（即去分化），这些变化分别与认知的改善和恶化有关。鉴于行为变异性额颞叶变性（bvFTD）是一种与执行功能障碍和显著性网络选择性易感性相关的神经退行性疾病，我们测试了bvFTD结构网络与认知正常对照（CNC）相比去分化的假设，以及网络去分化与更差的执行功能有关。方法在90例bvFTD患者和71例年龄匹配的CNC患者的弥散MRI数据样本中，我们生成了概率神经束图并计算了系统隔离，这是一种比较网络内和网络间连通性的指标，以反映大脑网络分化的程度。bvFTD患者还完成了执行功能测试（数字跨度向后、音位流畅性、类别流畅性）和控制任务（词汇检索）。我们评估了系统隔离的组间差异，反映了网络差异，并在bvFTD中评估了系统隔离与神经心理测试表现之间的关系。结果与CNC相比，bvFTD患者表现出较低的系统分离性(p <；0.001)和全球脑网络（p = 0.008）。在bvFTD中，较低的显著性网络系统分离与较差的执行功能相关（pcorrected = 0.021），但与词汇检索无关。结论bvFTD患者执行功能障碍与突出网络去分化之间存在关联。我们的研究结果表明，大脑网络去分化，反映了专门处理神经能力的降低，可能导致bvFTD中执行功能障碍的出现。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

查看原文本刊更多论文

Executive dysfunction relates to salience network desegregation in behavioural variant frontotemporal dementia

Background

The organization of the brain into distinct networks increases (i.e., differentiation) during development and decreases (i.e., de-differentiation) during healthy aging, changes that are associated with improvements and worsening of cognition, respectively. Given that behavioral variant frontotemporal degeneration (bvFTD) is a neurodegenerative disease associated with executive dysfunction and selective vulnerability of the salience network, we tested the hypotheses that bvFTD structural networks are de-differentiated compared to cognitively normal controls (CNC) and that network de-differentiation relates to worse executive function.

Methods

In a sample of 90 patients with bvFTD and 71 age-matched CNC with diffusion MRI data we generated probabilistic tractography maps and calculated system segregation, a metric that compares within-network to between-network connectivity, to reflect the extent to which brain networks were differentiated. Patients with bvFTD also completed tests of executive function (digit span backwards, phonemic fluency, category fluency) and a control task (lexical retrieval). We assessed group differences in system segregation, reflecting network differentiation, and, within bvFTD, associations between system segregation and neuropsychological test performance.

Results

Compared to CNC, patients with bvFTD exhibited lower system segregation of the salience (p < 0.001) and global brain network (p = 0.008). In bvFTD, lower salience network system segregation was associated with worse executive function (p_corrected = 0.021) but not lexical retrieval.

Conclusions

Results demonstrate associations between executive dysfunction and salience network de-differentiation in patients with bvFTD. Our findings indicate that brain network de-differentiation, reflecting reduced neural capacity for specialized processing, may contribute to the emergence of executive dysfunction in bvFTD.

求助全文

通过发布文献求助，成功后即可免费获取论文全文。去求助

来源期刊

Neuroimage-Clinical NEUROIMAGING-

CiteScore

7.50

自引率

4.80%

发文量

368

审稿时长

52 days

期刊介绍： NeuroImage: Clinical, a journal of diseases, disorders and syndromes involving the Nervous System, provides a vehicle for communicating important advances in the study of abnormal structure-function relationships of the human nervous system based on imaging. The focus of NeuroImage: Clinical is on defining changes to the brain associated with primary neurologic and psychiatric diseases and disorders of the nervous system as well as behavioral syndromes and developmental conditions. The main criterion for judging papers is the extent of scientific advancement in the understanding of the pathophysiologic mechanisms of diseases and disorders, in identification of functional models that link clinical signs and symptoms with brain function and in the creation of image based tools applicable to a broad range of clinical needs including diagnosis, monitoring and tracking of illness, predicting therapeutic response and development of new treatments. Papers dealing with structure and function in animal models will also be considered if they reveal mechanisms that can be readily translated to human conditions.