Common and Unique Inhibitory Control Signatures of Action-Stopping and Attentional Capture Suggest That Actions Are Stopped in Two Stages

• Published in: The Journal of neuroscience Vol. 41; no. 42; pp. 8826 - 8838
• Main Authors: Tatz, Joshua R., Soh, Cheol, Wessel, Jan R.
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 20.10.2021
• Subjects: Adolescent; Adult; Attention - physiology; Cognitive ability; EEG; Electroencephalography; Electroencephalography - methods; Electromyography; Entanglement; Environmental effects; Evoked Potentials, Motor - physiology; Excitability; Female; Human performance; Humans; Inhibition, Psychological; Latency; Male; Motor task performance; Multivariate analysis; Pattern analysis; Photic Stimulation - methods; Psychomotor Performance - physiology; Pyramidal tracts; Questions; Reaction Time - physiology; Salience; Signal processing; Signatures; Young Adult; attentional capture; motor inhibition; stop signal task; EEG; inhibitory control; EMG
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.1105-21.2021

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. SIGNIFICANCE STATEMENT 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.