Literature DB >> 34493541

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

Joshua R Tatz1,2,3, Cheol Soh1,3, Jan R Wessel4,2,3.   

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 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.
Copyright © 2021 the authors.

Entities:  

Keywords:  EEG; EMG; attentional capture; inhibitory control; motor inhibition; stop signal task

Mesh:

Year:  2021        PMID: 34493541      PMCID: PMC8528501          DOI: 10.1523/JNEUROSCI.1105-21.2021

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  54 in total

1.  Suppression of human cortico-motoneuronal excitability during the Stop-signal task.

Authors:  Reda Badry; Tatsuya Mima; Toshihiko Aso; Masahiro Nakatsuka; Mitsunari Abe; Dina Fathi; Nageh Foly; Hamdy Nagiub; Takashi Nagamine; Hidenao Fukuyama
Journal:  Clin Neurophysiol       Date:  2009-08-15       Impact factor: 3.708

2.  Reconsidering electrophysiological markers of response inhibition in light of trigger failures in the stop-signal task.

Authors:  P Skippen; W R Fulham; P T Michie; D Matzke; A Heathcote; F Karayanidis
Journal:  Psychophysiology       Date:  2020-07-29       Impact factor: 4.016

3.  Perceptual Surprise Improves Action Stopping by Nonselectively Suppressing Motor Activity via a Neural Mechanism for Motor Inhibition.

Authors:  Isabella C Dutra; Darcy A Waller; Jan R Wessel
Journal:  J Neurosci       Date:  2018-01-05       Impact factor: 6.167

4.  Differences in unity: The go/no-go and stop signal tasks rely on different mechanisms.

Authors:  Liisa Raud; René Westerhausen; Niamh Dooley; René J Huster
Journal:  Neuroimage       Date:  2020-01-25       Impact factor: 6.556

5.  On the ability to inhibit simple and choice reaction time responses: a model and a method.

Authors:  G D Logan; W B Cowan; K A Davis
Journal:  J Exp Psychol Hum Percept Perform       Date:  1984-04       Impact factor: 3.332

6.  Distinct frontal systems for response inhibition, attentional capture, and error processing.

Authors:  D J Sharp; V Bonnelle; X De Boissezon; C F Beckmann; S G James; M C Patel; M A Mehta
Journal:  Proc Natl Acad Sci U S A       Date:  2010-03-10       Impact factor: 11.205

7.  Saccade suppression exerts global effects on the motor system.

Authors:  Jan R Wessel; H Sequoyah Reynoso; Adam R Aron
Journal:  J Neurophysiol       Date:  2013-05-22       Impact factor: 2.714

8.  Common neural processes during action-stopping and infrequent stimulus detection: The frontocentral P3 as an index of generic motor inhibition.

Authors:  Darcy A Waller; Eliot Hazeltine; Jan R Wessel
Journal:  Int J Psychophysiol       Date:  2019-01-17       Impact factor: 2.997

9.  Canceling actions involves a race between basal ganglia pathways.

Authors:  Robert Schmidt; Daniel K Leventhal; Nicolas Mallet; Fujun Chen; Joshua D Berke
Journal:  Nat Neurosci       Date:  2013-07-14       Impact factor: 24.884

10.  Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism.

Authors:  Jan R Wessel; David E Huber
Journal:  PLoS Comput Biol       Date:  2019-07-29       Impact factor: 4.475

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  3 in total

1.  A causal role for the human subthalamic nucleus in non-selective cortico-motor inhibition.

Authors:  Jan R Wessel; Darcy A Diesburg; Nathan H Chalkley; Jeremy D W Greenlee
Journal:  Curr Biol       Date:  2022-07-15       Impact factor: 10.900

2.  Neural correlates of unpredictable Stop and non-Stop cues in overt and imagined execution.

Authors:  Alberto González-Villar; Santiago Galdo-Álvarez; María T Carrillo-de-la-Peña
Journal:  Psychophysiology       Date:  2022-02-27       Impact factor: 4.348

3.  Cortical sensorimotor activity in the execution and suppression of discrete and rhythmic movements.

Authors:  Mario Hervault; Pier-Giorgio Zanone; Jean-Christophe Buisson; Raoul Huys
Journal:  Sci Rep       Date:  2021-11-16       Impact factor: 4.379

  3 in total

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