Department of Psychological and Brain Sciences, University of Iowa, Iowa City, Iowa 52245.
Department of Neurology, University of Iowa Hospitals and Clinics, Iowa City, Iowa 52242.
J Neurosci. 2021 Oct 20;41(42):8826-8838. doi: 10.1523/JNEUROSCI.1105-21.2021. Epub 2021 Sep 7.
The ability to stop an already initiated action is paramount to adaptive behavior. Much scientific debate in the field of human action-stopping currently focuses on two interrelated questions. (1) Which cognitive and neural processes uniquely underpin the implementation of inhibitory control when actions are stopped after explicit stop signals, and which processes are instead commonly evoked by all salient signals, even those that do not require stopping? (2) Why do purported (neuro)physiological signatures of inhibition occur at two different latencies after stop signals? Here, we address both questions via two preregistered experiments that combined measurements of corticospinal excitability, EMG, and whole-scalp EEG. Adult human subjects performed a stop signal task that also contained "ignore" signals: equally salient signals that did not require stopping but rather completion of the Go response. We found that both stop- and ignore signals produced equal amounts of early-latency inhibition of corticospinal excitability and EMG, which took place ∼150 ms following either signal. Multivariate pattern analysis of the whole-scalp EEG data further corroborated that this early processing stage was shared between stop- and ignore signals, as neural activity following the two signals could not be decoded from each other until a later time period. In this later period, unique activity related to stop signals emerged at frontocentral scalp sites, reflecting an increased stop signal P3. These findings suggest a two-step model of action-stopping, according to which an initial, universal inhibitory response to the saliency of the stop signal is followed by a slower process that is unique to outright stopping. Humans often have to stop their ongoing actions when indicated by environmental stimuli (stop signals). Successful action-stopping requires both the ability to detect these salient stop signals and to subsequently inhibit ongoing motor programs. Because of this tight entanglement of attentional control and motor inhibition, identifying unique neurophysiological signatures of action-stopping is difficult. Indeed, we report that recently proposed early-latency signatures of motor inhibition during action-stopping are also found after salient signals that do not require stopping. However, using multivariate pattern analysis of scalp-recorded neural data, we also identified subsequent neural activity that uniquely distinguished action-stopping from saliency detection. These results suggest that actions are stopped in two stages: the first common to all salient events and the second unique to action-stopping.
停止已经启动的动作的能力对于适应行为至关重要。目前,人类行为停止领域的许多科学争论都集中在两个相互关联的问题上。(1) 在明确的停止信号后停止动作时,哪些认知和神经过程独特地支持抑制控制的实施,而哪些过程则是所有显著信号共同引起的,即使这些信号不需要停止?(2) 为什么抑制的所谓(神经)生理特征会在停止信号后出现两种不同的潜伏期?在这里,我们通过两项结合了皮质脊髓兴奋性、肌电图和全头皮脑电图测量的预先注册实验来解决这两个问题。成年人类受试者执行了一个停止信号任务,其中还包含“忽略”信号:同样显著的信号,不需要停止,而是需要完成 Go 反应。我们发现,停止和忽略信号都会产生皮质脊髓兴奋性和肌电图的早期潜伏期抑制,这发生在信号发出后约 150 毫秒。全头皮 EEG 数据的多变量模式分析进一步证实,这个早期处理阶段在停止和忽略信号之间是共享的,因为在两个信号之后,两个信号的神经活动不能相互解码,直到稍后的时间段。在这个后期阶段,与停止信号相关的独特活动出现在额中央头皮部位,反映了停止信号 P3 的增加。这些发现表明,行为停止是一个两步模型,根据该模型,对停止信号显著度的初始普遍抑制反应之后是一个较慢的过程,该过程是停止的特有过程。当环境刺激(停止信号)指示时,人类通常必须停止正在进行的动作。成功的行为停止既需要能够检测到这些显著的停止信号,又需要随后抑制正在进行的运动程序。由于注意力控制和运动抑制的紧密交织,很难确定行为停止的独特神经生理特征。事实上,我们报告说,最近提出的在停止信号下进行动作时的早期潜伏期运动抑制的特征也存在于不需要停止的显著信号之后。然而,我们通过对头皮记录的神经数据进行多变量模式分析,还确定了随后唯一区分动作停止和显著性检测的神经活动。这些结果表明,动作分两个阶段停止:第一个阶段对所有显著事件都是共同的,第二个阶段对动作停止是独特的。