Subthalamic control of impulsive actions: insights from deep brain stimulation in Parkinson's disease.

IF 10.6 1区 医学 Q1 CLINICAL NEUROLOGY
Brain Pub Date : 2024-11-04 DOI:10.1093/brain/awae184
Damian M Herz, Michael J Frank, Huiling Tan, Sergiu Groppa
{"title":"Subthalamic control of impulsive actions: insights from deep brain stimulation in Parkinson's disease.","authors":"Damian M Herz, Michael J Frank, Huiling Tan, Sergiu Groppa","doi":"10.1093/brain/awae184","DOIUrl":null,"url":null,"abstract":"<p><p>Control of actions allows adaptive, goal-directed behaviour. The basal ganglia, including the subthalamic nucleus, are thought to play a central role in dynamically controlling actions through recurrent negative feedback loops with the cerebral cortex. Here, we summarize recent translational studies that used deep brain stimulation to record neural activity from and apply electrical stimulation to the subthalamic nucleus in people with Parkinson's disease. These studies have elucidated spatial, spectral and temporal features of the neural mechanisms underlying the controlled delay of actions in cortico-subthalamic networks and demonstrated their causal effects on behaviour in distinct processing windows. While these mechanisms have been conceptualized as control signals for suppressing impulsive response tendencies in conflict tasks and as decision threshold adjustments in value-based and perceptual decisions, we propose a common framework linking decision-making, cognition and movement. Within this framework, subthalamic deep brain stimulation can lead to suboptimal choices by reducing the time that patients take for deliberation before committing to an action. However, clinical studies have consistently shown that the occurrence of impulse control disorders is reduced, not increased, after subthalamic deep brain stimulation surgery. This apparent contradiction can be reconciled when recognizing the multifaceted nature of impulsivity, its underlying mechanisms and modulation by treatment. While subthalamic deep brain stimulation renders patients susceptible to making decisions without proper forethought, this can be disentangled from effects related to dopamine comprising sensitivity to benefits versus costs, reward delay aversion and learning from outcomes. Alterations in these dopamine-mediated mechanisms are thought to underlie the development of impulse control disorders and can be relatively spared with reduced dopaminergic medication after subthalamic deep brain stimulation. Together, results from studies using deep brain stimulation as an experimental tool have improved our understanding of action control in the human brain and have important implications for treatment of patients with neurological disorders.</p>","PeriodicalId":9063,"journal":{"name":"Brain","volume":null,"pages":null},"PeriodicalIF":10.6000,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11531846/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Brain","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1093/brain/awae184","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Control of actions allows adaptive, goal-directed behaviour. The basal ganglia, including the subthalamic nucleus, are thought to play a central role in dynamically controlling actions through recurrent negative feedback loops with the cerebral cortex. Here, we summarize recent translational studies that used deep brain stimulation to record neural activity from and apply electrical stimulation to the subthalamic nucleus in people with Parkinson's disease. These studies have elucidated spatial, spectral and temporal features of the neural mechanisms underlying the controlled delay of actions in cortico-subthalamic networks and demonstrated their causal effects on behaviour in distinct processing windows. While these mechanisms have been conceptualized as control signals for suppressing impulsive response tendencies in conflict tasks and as decision threshold adjustments in value-based and perceptual decisions, we propose a common framework linking decision-making, cognition and movement. Within this framework, subthalamic deep brain stimulation can lead to suboptimal choices by reducing the time that patients take for deliberation before committing to an action. However, clinical studies have consistently shown that the occurrence of impulse control disorders is reduced, not increased, after subthalamic deep brain stimulation surgery. This apparent contradiction can be reconciled when recognizing the multifaceted nature of impulsivity, its underlying mechanisms and modulation by treatment. While subthalamic deep brain stimulation renders patients susceptible to making decisions without proper forethought, this can be disentangled from effects related to dopamine comprising sensitivity to benefits versus costs, reward delay aversion and learning from outcomes. Alterations in these dopamine-mediated mechanisms are thought to underlie the development of impulse control disorders and can be relatively spared with reduced dopaminergic medication after subthalamic deep brain stimulation. Together, results from studies using deep brain stimulation as an experimental tool have improved our understanding of action control in the human brain and have important implications for treatment of patients with neurological disorders.

丘脑下部对冲动行为的控制:从帕金森病的深部脑刺激中获得的启示。
对行动的控制可使行为具有适应性和目标导向性。包括丘脑下核在内的基底神经节被认为在通过与大脑皮层的反复负反馈环路动态控制行动方面发挥着核心作用。在此,我们总结了最近的一些转化研究,这些研究利用脑深部刺激来记录帕金森病患者的神经活动,并对丘脑下核进行电刺激。这些研究阐明了大脑皮层-丘脑下核网络中控制行动延迟的神经机制的空间、频谱和时间特征,并证明了它们在不同的处理窗口中对行为的因果效应。虽然这些机制已被概念化为在冲突任务中抑制冲动反应倾向的控制信号,以及在基于价值和感知的决策中作为决策阈值调整,但我们提出了一个将决策、认知和运动联系起来的共同框架。在这一框架内,脑下丘脑深部刺激可减少患者在做出行动前的考虑时间,从而导致次优选择。然而,临床研究却一致表明,在接受脑下深部刺激手术后,冲动控制障碍的发生率会降低,而不是增加。如果认识到冲动的多面性、其潜在机制以及治疗对其的调节作用,这种明显的矛盾是可以调和的。虽然脑下深部刺激会使患者容易在没有经过适当深思熟虑的情况下做出决定,但这可以与多巴胺的影响区分开来,多巴胺的影响包括对收益与成本的敏感性、奖励延迟厌恶和从结果中学习。这些由多巴胺介导的机制的改变被认为是冲动控制障碍发展的基础,而眼下丘脑下深部脑刺激术后减少多巴胺能药物的用量,可以相对避免这些改变。总之,以脑深部刺激为实验工具的研究结果增进了我们对人脑行动控制的了解,对治疗神经系统疾病患者具有重要意义。
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
Brain
Brain 医学-临床神经学
CiteScore
20.30
自引率
4.10%
发文量
458
审稿时长
3-6 weeks
期刊介绍: Brain, a journal focused on clinical neurology and translational neuroscience, has been publishing landmark papers since 1878. The journal aims to expand its scope by including studies that shed light on disease mechanisms and conducting innovative clinical trials for brain disorders. With a wide range of topics covered, the Editorial Board represents the international readership and diverse coverage of the journal. Accepted articles are promptly posted online, typically within a few weeks of acceptance. As of 2022, Brain holds an impressive impact factor of 14.5, according to the Journal Citation Reports.
×
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