Department of Psychological and Brain Sciences, University of Iowa, Iowa City, Iowa.
Interdisciplinary Graduate Program in Neuroscience, University of Iowa, Iowa City, Iowa.
J Neurophysiol. 2021 Feb 1;125(2):648-660. doi: 10.1152/jn.00571.2020. Epub 2021 Jan 13.
By stopping actions even after their initiation, humans can flexibly adapt ongoing behavior to changing circumstances. The neural processes underlying the inhibition of movement during action stopping are still controversial. In the 90s, a fronto-central event-related potential (ERP) was discovered in the human EEG response to stop signals in the classic stop-signal task, alongside a proposal that this "stop-signal P3" reflects an inhibitory process. Indeed, both amplitude and onset of the stop-signal P3 relate to overt behavior and movement-related EEG activity in ways predicted by the dominant models of action-stopping. However, neither EEG nor behavior allow direct inferences about the presence or absence of neurophysiological inhibition of the motor cortex, making it impossible to definitively relate the stop-signal P3 to inhibition. Here, we therefore present a multimethod investigation of the relationship between the stop-signal P3 and GABAergic signaling in primary motor cortex, as indexed by paired-pulse transcranial magnetic stimulation (TMS). In detail, we measured short-interval intracortical inhibition (SICI), a marker of inhibitory GABA activity in M1, in a group of 41 human participants who also performed the stop-signal task while undergoing EEG recordings. In line with the P3-inhibition hypothesis, we found that subjects with stronger inhibitory GABA activity in M1 also showed both faster onsets and larger amplitudes of the stop-signal P3. This provides direct evidence linking the properties of this ERP to a true physiological index of motor system inhibition. We discuss these findings in the context of recent theoretical developments and empirical findings regarding the neural implementation of motor inhibition. The neural mechanisms underlying rapid action stopping in humans are subject to intense debate, in part because recordings of neural signals purportedly reflecting inhibitory motor control are hard to directly relate to the true, physiological inhibition of motor cortex. For the first time, the current study combines EEG and transcranial magnetic stimulation (TMS) methods to demonstrate a direct correspondence between fronto-central control-related EEG activity following signals to cancel an action and the physiological inhibition of primary motor cortex.
通过在动作开始后停止动作，人类可以灵活地根据不断变化的环境调整正在进行的行为。在动作停止过程中，抑制运动的神经过程仍存在争议。在 90 年代，在经典的停止信号任务中，人类 EEG 对停止信号的反应中发现了一种额-中央事件相关电位（ERP），同时提出这种“停止信号 P3”反映了一种抑制过程。事实上，停止信号 P3 的幅度和起始都与显性的动作停止模型所预测的行为和与运动相关的 EEG 活动有关。然而，EEG 和行为都不能直接推断运动皮层是否存在或不存在神经生理抑制，因此无法将停止信号 P3 与抑制作用明确相关联。在这里，我们通过经颅磁刺激（TMS）的成对脉冲研究，对停止信号 P3 与初级运动皮层中的 GABA 能信号之间的关系进行了多方法研究。详细来说，我们在 41 名人类参与者中测量了短间隔皮质内抑制（SICI），这是 M1 中抑制性 GABA 活动的标志物，这些参与者在进行 EEG 记录的同时还执行了停止信号任务。与 P3 抑制假说一致，我们发现 M1 中 GABA 抑制性活动较强的受试者的停止信号 P3 起始更快，幅度更大。这为将该 ERP 的特性直接与运动系统抑制的真正生理指标联系起来提供了直接证据。我们在关于运动抑制的神经实施的最新理论发展和实证发现的背景下讨论了这些发现。人类快速动作停止的神经机制受到了激烈的争论，部分原因是据称反映抑制性运动控制的神经信号的记录很难直接与运动皮层的真正生理抑制联系起来。这项研究首次将 EEG 和经颅磁刺激（TMS）方法结合起来，证明了在信号取消动作后，与额中央控制相关的 EEG 活动与初级运动皮层的生理抑制之间存在直接对应关系。
