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

Abstract

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 stopand 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.

Neural correlates of unpredictable Stop and non‐Stop cues in overt and imagined execution

“…However, its highest classification accuracy was between 400 ms and 600 ms, coincident with the P3 component. This observation is in accordance with a recent study using multivariate pattern analysis, that found that ERPs evoked by Stop signal could be decoded from “ignore” signals (analogous to our CGo signals) from 180 ms after signal onset, although better classification accuracy was observed at P3 latencies (Tatz et al, 2021 ). Finally, an interesting finding is that the peak in decoding accuracy in the imagined condition reached levels similar to those observed in the overt condition, suggesting that the ability to discriminate between CGo and Stop EEG signals is also maintained in mental rehearsal.…”

“…This idea is in line with the theory that surprise is accompanied by automatically engaged motor inhibition (Iacullo et al, 2020 ; Wessel & Aron, 2017 ); and also with the model “pause‐then‐cancel” which proposes that inhibition occurs in two steps. A first step, “pause”, which is initially activated after the presentation of surprising stimuli; and a second step, “cancel” (or continue for the case of CGo signals), that occurs after further evaluation of the stimuli (Schmidt & Berke, 2017 ; Tatz et al, 2021 ).…”

“…Although Stop‐P3 has been related to the engagement of inhibitory processes (Enriquez‐Geppert et al, 2010 ; Wessel & Aron, 2015 ), it seems more likely that this component is related to post‐inhibitory operations, such as performance monitoring (Huster et al, 2020 ; Skippen et al, 2020 ), since behavioral inhibition precedes the onset of P3. However, the fact that the amplitude of this component is greater for Stop signals than for other infrequent stimuli that do not require motor inhibition suggests that Stop‐P3 does reflect processes that are specific for action‐stopping (Tatz et al, 2021 ). In the time‐frequency domain, stop signals are associated to increased mid‐frontal theta power‐related to conflict detection and the N2 component‐, reduced posterior alpha power ‐ related to visual attention processes‐, and changes in mu and beta oscillations over central scalp locations ‐associated with sensory and motor functions‐ (Galdo‐Alvarez et al, 2016 ; González‐Villar et al, 2016 ; Huster et al, 2013 ; Wagner et al, 2018 ).…”

Multiple Brain Sources Are Differentially Engaged in the Inhibition of Distinct Action Types

“…The absence of a significant P3 when evaluating the IC-D activity in the rhythmic experiment or, inversely, the IC-R activity in the discrete one suggests that the P3 signature is specific to the engaged inhibition brain component. This pattern of findings indicates that P3 is a clear-cut neural marker of action inhibition in the context of stop-signal reactions (Fine et al, 2020;Hynd et al, 2021;Tatz et al, 2021;Wessel & Aron, 2015). In addition, an N2 wave was exclusively evoked by the IC-R in the rhythmic ABORT R but not in any other condition.…”

Right inferior frontal cortex damage impairs the initiation of inhibitory control, but not its implementation

“…Crucially, however, any attempt to disentangle the domain-general detection of a salient stimulus from the stopping-specific implementation of inhibitory control is complicated by another factor. Namely, all salient stimuli, even those presented outside of stop-signal contexts, lead to an automatic, physiological inhibition of the motor system (Dutra et al, 2018; Tatz et al, 2021; Wessel, 2018; Wessel & Aron, 2017). For example, salient stimuli lead to a non-selective inhibition of cortico-motor excitability (Iacullo et al, 2020), activate basal ganglia regions involved in inhibitory pathways (Wessel et al, 2016), reduce isometrically exerted force (Novembre et al, 2018, ; 2019), and increase motoric response times (e.g., Parmentier, 2008).…”