Apathy scores in Parkinson’s disease relate to EEG components in an incentivized motor task

Soojin Lee, Esther Song, Maria Zhu, S. Appel-Cresswell, Martin J. McKeown
{"title":"Apathy scores in Parkinson’s disease relate to EEG components in an incentivized motor task","authors":"Soojin Lee, Esther Song, Maria Zhu, S. Appel-Cresswell, Martin J. McKeown","doi":"10.1093/braincomms/fcae025","DOIUrl":null,"url":null,"abstract":"\n Apathy is one of the most prevalent non-motor symptoms of Parkinson’s disease and is characterized by decreased goal-directed behavior due to a lack of motivation and/or impaired emotional reactivity. Despite its high prevalence, the neurophysiological mechanisms underlying apathy in Parkinson’s disease, which may guide neuromodulation interventions, are poorly understood. Here, we investigated the neural oscillatory characteristics of apathy in Parkinson’s disease using EEG data recorded during an incentivized motor task.\n Thirteen Parkinson’s disease patients with apathy and 13 Parkinson’s disease patients without apathy as well as 12 healthy controls were instructed to squeeze a hand grip device to earn a monetary reward proportional to the grip force they used. Event-related spectral perturbations during the presentation of a reward cue and squeezing were analyzed using multi-set canonical correlation analysis to detect different orthogonal components of temporally-consistent event-related spectral perturbations across trials and participants.\n The first component, predominantly located over parietal regions, demonstrated suppression of low-beta (12–20 Hz) power (i.e., beta desynchronization) during reward cue presentation that was significantly smaller in Parkinson’s disease patients with apathy compared to healthy controls. Unlike traditional event-related spectral perturbation analysis, the beta-desynchronization in this component was significantly correlated with clinical apathy scores. Higher monetary rewards resulted in larger beta desynchronization in heathy controls but not Parkinson’s disease patients. The second component contained gamma and theta frequencies and demonstrated exaggerated theta (4–8 Hz) power in Parkinson’s disease patients with apathy during the reward cue and squeezing compared to healthy controls, and this was positively correlated with Montreal Cognitive Assessment scores. The third component, over central regions, demonstrated significantly different beta power across groups, with apathetic groups having the lowest beta power.\n Our results emphasize that altered low-beta and theta oscillations are critical for reward processing and motor planning in Parkinson’s disease patients with apathy, and these may provide a target for non-invasive neuromodulation.","PeriodicalId":504765,"journal":{"name":"Brain Communications","volume":"357 7","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2024-02-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Brain Communications","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/braincomms/fcae025","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

Apathy is one of the most prevalent non-motor symptoms of Parkinson’s disease and is characterized by decreased goal-directed behavior due to a lack of motivation and/or impaired emotional reactivity. Despite its high prevalence, the neurophysiological mechanisms underlying apathy in Parkinson’s disease, which may guide neuromodulation interventions, are poorly understood. Here, we investigated the neural oscillatory characteristics of apathy in Parkinson’s disease using EEG data recorded during an incentivized motor task. Thirteen Parkinson’s disease patients with apathy and 13 Parkinson’s disease patients without apathy as well as 12 healthy controls were instructed to squeeze a hand grip device to earn a monetary reward proportional to the grip force they used. Event-related spectral perturbations during the presentation of a reward cue and squeezing were analyzed using multi-set canonical correlation analysis to detect different orthogonal components of temporally-consistent event-related spectral perturbations across trials and participants. The first component, predominantly located over parietal regions, demonstrated suppression of low-beta (12–20 Hz) power (i.e., beta desynchronization) during reward cue presentation that was significantly smaller in Parkinson’s disease patients with apathy compared to healthy controls. Unlike traditional event-related spectral perturbation analysis, the beta-desynchronization in this component was significantly correlated with clinical apathy scores. Higher monetary rewards resulted in larger beta desynchronization in heathy controls but not Parkinson’s disease patients. The second component contained gamma and theta frequencies and demonstrated exaggerated theta (4–8 Hz) power in Parkinson’s disease patients with apathy during the reward cue and squeezing compared to healthy controls, and this was positively correlated with Montreal Cognitive Assessment scores. The third component, over central regions, demonstrated significantly different beta power across groups, with apathetic groups having the lowest beta power. Our results emphasize that altered low-beta and theta oscillations are critical for reward processing and motor planning in Parkinson’s disease patients with apathy, and these may provide a target for non-invasive neuromodulation.
帕金森病患者的冷漠评分与激励性运动任务中的脑电图成分有关
淡漠是帕金森病最常见的非运动症状之一,其特征是由于缺乏动机和/或情绪反应能力受损而导致目标导向行为减少。尽管帕金森病的发病率很高,但人们对帕金森病患者神经失调的神经生理学机制却知之甚少,而这种机制可以指导神经调节干预措施。在此,我们使用在激励性运动任务中记录的脑电图数据,研究了帕金森病患者淡漠的神经振荡特征。13 名帕金森病患者和 13 名无帕金森病患者以及 12 名健康对照者被要求挤压一个手握装置,以获得与他们使用的握力成正比的金钱奖励。使用多组典型相关分析法对奖励提示和挤压过程中的事件相关频谱扰动进行了分析,以检测不同试验和参与者之间时间上一致的事件相关频谱扰动的不同正交成分。第一个成分主要位于顶叶区域,显示了在奖励线索呈现期间低贝塔(12-20 Hz)功率的抑制(即贝塔去同步化),与健康对照组相比,帕金森病伴发淡漠患者的抑制明显较小。与传统的事件相关频谱扰动分析不同,该分量中的β不同步与临床淡漠评分有显著相关性。在健康对照组中,较高的金钱奖励会导致较大的贝塔失同步,而在帕金森病患者中则不会。第二个成分包含伽马和θ频率,与健康对照组相比,帕金森病患者在奖励提示和挤压过程中的θ(4-8赫兹)功率夸大,这与蒙特利尔认知评估得分呈正相关。中心区域的第三个成分显示出各组间明显不同的贝塔功率,其中冷漠组的贝塔功率最低。我们的研究结果强调,低贝塔和θ振荡的改变对于帕金森病患者的奖赏处理和运动规划至关重要,这些可能为非侵入性神经调控提供了目标。
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
小红书