Common and unique neurophysiological processes that support the stopping and revising of actions.

IF 4.4 2区 医学 Q1 NEUROSCIENCES
Mario Hervault, Jan R Wessel
{"title":"Common and unique neurophysiological processes that support the stopping and revising of actions.","authors":"Mario Hervault, Jan R Wessel","doi":"10.1523/JNEUROSCI.1537-24.2025","DOIUrl":null,"url":null,"abstract":"<p><p>Inhibitory control is a crucial cognitive-control ability for behavioral flexibility, which has been extensively investigated through action-stopping tasks. Multiple neurophysiological features have been proposed as 'signatures' of inhibitory control during action-stopping, though the processes indexed by these signatures are still controversially discussed. The present study aimed to disentangle these processes by comparing simple stopping situations with those in which additional action revisions were needed. Three experiments in female and male humans were performed to characterize the neurophysiological dynamics involved in action-stopping and -changing, with hypotheses derived from recently developed two-stage 'pause-then-cancel' models of inhibitory control. Both stopping and revising an action triggered an early, broad 'pause'-process, marked by frontal EEG β-frequency bursting and non-selective suppression of corticospinal excitability. However, EMG showed that motor activity was only partially inhibited by this 'pause', and that this activity could be modulated during action-revision. In line with two-stage models of inhibitory control, subsequent frontocentral EEG activity after this initial 'pause' selectively scaled depending on the required action revisions, with more activity observed for more complex revisions. This demonstrates the presence of a selective, effector-specific 'retune' phase as the second process involved in action-stopping and -revision. Together, these findings show that inhibitory control is implemented over an extended period of time and in at least two phases. We are further able to align the most commonly proposed neurophysiological signatures to these phases and show that they are differentially modulated by the complexity of action-revision.<b>Significance Statement</b> Inhibitory control is one of the most important control processes by which humans can regulate their behavior. Multiple neurophysiological signatures have been proposed to index inhibitory control. However, these play out on different time scales and appear to reflect different aspects of cognitive control, which are controversially debated.Recent two-stage models of inhibitory control have proposed that two phases implement the revisions of actions: 'pause' and 'retune'. Here, we provide the first empirical evidence for this proposition: Action revisions engendered a common, low-latency 'pause' process, during which motor activity is broadly suppressed. Later activity, however, distinguishes between simple stopping of actions and more complex action revisions. These findings provide novel insights into the sequential dynamics of human action control.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4000,"publicationDate":"2025-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/JNEUROSCI.1537-24.2025","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Inhibitory control is a crucial cognitive-control ability for behavioral flexibility, which has been extensively investigated through action-stopping tasks. Multiple neurophysiological features have been proposed as 'signatures' of inhibitory control during action-stopping, though the processes indexed by these signatures are still controversially discussed. The present study aimed to disentangle these processes by comparing simple stopping situations with those in which additional action revisions were needed. Three experiments in female and male humans were performed to characterize the neurophysiological dynamics involved in action-stopping and -changing, with hypotheses derived from recently developed two-stage 'pause-then-cancel' models of inhibitory control. Both stopping and revising an action triggered an early, broad 'pause'-process, marked by frontal EEG β-frequency bursting and non-selective suppression of corticospinal excitability. However, EMG showed that motor activity was only partially inhibited by this 'pause', and that this activity could be modulated during action-revision. In line with two-stage models of inhibitory control, subsequent frontocentral EEG activity after this initial 'pause' selectively scaled depending on the required action revisions, with more activity observed for more complex revisions. This demonstrates the presence of a selective, effector-specific 'retune' phase as the second process involved in action-stopping and -revision. Together, these findings show that inhibitory control is implemented over an extended period of time and in at least two phases. We are further able to align the most commonly proposed neurophysiological signatures to these phases and show that they are differentially modulated by the complexity of action-revision.Significance Statement Inhibitory control is one of the most important control processes by which humans can regulate their behavior. Multiple neurophysiological signatures have been proposed to index inhibitory control. However, these play out on different time scales and appear to reflect different aspects of cognitive control, which are controversially debated.Recent two-stage models of inhibitory control have proposed that two phases implement the revisions of actions: 'pause' and 'retune'. Here, we provide the first empirical evidence for this proposition: Action revisions engendered a common, low-latency 'pause' process, during which motor activity is broadly suppressed. Later activity, however, distinguishes between simple stopping of actions and more complex action revisions. These findings provide novel insights into the sequential dynamics of human action control.

求助全文
约1分钟内获得全文 求助全文
来源期刊
Journal of Neuroscience
Journal of Neuroscience 医学-神经科学
CiteScore
9.30
自引率
3.80%
发文量
1164
审稿时长
12 months
期刊介绍: JNeurosci (ISSN 0270-6474) is an official journal of the Society for Neuroscience. It is published weekly by the Society, fifty weeks a year, one volume a year. JNeurosci publishes papers on a broad range of topics of general interest to those working on the nervous system. Authors now have an Open Choice option for their published articles
×
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