Increased beta synchronization underlies perception-action hyperbinding in functional movement disorders.

IF 4.1 Q1 CLINICAL NEUROLOGY
Brain communications Pub Date : 2024-10-09 eCollection Date: 2024-01-01 DOI:10.1093/braincomms/fcae301
Bernhard Pastötter, Anne Weissbach, Adam Takacs, Josephine Moyé, Julius Verrel, Fabian Chwolka, Julia Friedrich, Theresa Paulus, Simone Zittel, Tobias Bäumer, Christian Frings, Christian Beste, Alexander Münchau
{"title":"Increased beta synchronization underlies perception-action hyperbinding in functional movement disorders.","authors":"Bernhard Pastötter, Anne Weissbach, Adam Takacs, Josephine Moyé, Julius Verrel, Fabian Chwolka, Julia Friedrich, Theresa Paulus, Simone Zittel, Tobias Bäumer, Christian Frings, Christian Beste, Alexander Münchau","doi":"10.1093/braincomms/fcae301","DOIUrl":null,"url":null,"abstract":"<p><p>Functional movement disorders are amongst the most common and disabling neurological conditions, placing a significant burden on the healthcare system. Despite the frequency and importance of functional movement disorders, our understanding of the underlying pathophysiology is limited, hindering the development of causal treatment options. Traditionally, functional movement disorders were considered as a psychiatric condition, associated with involuntary movements triggered by psychological stressors. Recent neurophysiological studies have unveiled cognitive alterations in affected individuals, suggesting that functional movement disorders might be better characterized by overarching neural principles governing cognitive functions. For instance, recent research has shown that the retrieval of stimulus-response bindings is altered in patients with functional movement disorders. Building upon these recent findings, our study delves into whether the initial integration of stimulus and response information is also disrupted in patients with functional movement disorders. To accomplish this, we reanalysed previously collected EEG data using refined analysis methods that provide insights into oscillatory activity and functional neuroanatomy associated with the integration of stimulus-response bindings. Our results demonstrate that post-movement beta synchronization (i) predicts behavioural stimulus-response binding and (ii) is significantly increased in patients with functional movement disorders compared to healthy controls. Utilizing beamformer analysis, we localized the difference effect to a cluster centred around the left supplementary motor area and the correlation effect to the right supplementary motor area. Extending beyond recent research that focused on the retrieval of stimulus-response bindings, our present findings reveal that the integration of stimulus and response information is already impaired in patients with functional movement disorders. These results uncover a phenomenon of hyperbinding between perception and action, which may represent a fundamental mechanism contributing to the movement impairments in patients with functional movement disorders.</p>","PeriodicalId":93915,"journal":{"name":"Brain communications","volume":"6 5","pages":"fcae301"},"PeriodicalIF":4.1000,"publicationDate":"2024-10-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11462440/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Brain communications","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/braincomms/fcae301","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Functional movement disorders are amongst the most common and disabling neurological conditions, placing a significant burden on the healthcare system. Despite the frequency and importance of functional movement disorders, our understanding of the underlying pathophysiology is limited, hindering the development of causal treatment options. Traditionally, functional movement disorders were considered as a psychiatric condition, associated with involuntary movements triggered by psychological stressors. Recent neurophysiological studies have unveiled cognitive alterations in affected individuals, suggesting that functional movement disorders might be better characterized by overarching neural principles governing cognitive functions. For instance, recent research has shown that the retrieval of stimulus-response bindings is altered in patients with functional movement disorders. Building upon these recent findings, our study delves into whether the initial integration of stimulus and response information is also disrupted in patients with functional movement disorders. To accomplish this, we reanalysed previously collected EEG data using refined analysis methods that provide insights into oscillatory activity and functional neuroanatomy associated with the integration of stimulus-response bindings. Our results demonstrate that post-movement beta synchronization (i) predicts behavioural stimulus-response binding and (ii) is significantly increased in patients with functional movement disorders compared to healthy controls. Utilizing beamformer analysis, we localized the difference effect to a cluster centred around the left supplementary motor area and the correlation effect to the right supplementary motor area. Extending beyond recent research that focused on the retrieval of stimulus-response bindings, our present findings reveal that the integration of stimulus and response information is already impaired in patients with functional movement disorders. These results uncover a phenomenon of hyperbinding between perception and action, which may represent a fundamental mechanism contributing to the movement impairments in patients with functional movement disorders.

功能性运动障碍中感知-动作超结合的基础是β同步性增加。
功能性运动障碍是最常见的致残性神经系统疾病之一,给医疗系统带来了沉重的负担。尽管功能性运动障碍很常见,也很重要,但我们对其潜在病理生理学的了解却很有限,这阻碍了因果治疗方案的开发。传统上,功能性运动障碍被认为是一种精神疾病,与心理压力引发的不自主运动有关。最近的神经生理学研究揭示了受影响个体的认知改变,表明功能性运动障碍可能更适合用支配认知功能的总体神经原理来描述。例如,最近的研究表明,功能性运动障碍患者对刺激-反应绑定的检索发生了改变。在这些最新发现的基础上,我们的研究深入探讨了功能性运动障碍患者对刺激和反应信息的初始整合是否也会受到干扰。为此,我们使用精细的分析方法重新分析了之前收集的脑电图数据,从而深入了解了与刺激-反应结合相关的振荡活动和功能神经解剖学。我们的研究结果表明,运动后的贝塔同步(i)可预测行为刺激-反应结合,(ii)与健康对照组相比,功能性运动障碍患者的贝塔同步显著增加。利用波束成形器分析,我们将差异效应定位在以左侧辅助运动区为中心的集群上,将相关效应定位在右侧辅助运动区上。我们目前的研究结果表明,功能性运动障碍患者对刺激和反应信息的整合能力已经受损。这些结果揭示了感知与行动之间的超结合现象,这可能是导致功能性运动障碍患者运动障碍的基本机制。
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
CiteScore
7.00
自引率
0.00%
发文量
0
审稿时长
6 weeks
×
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:481959085
Book学术官方微信