Response inhibition in the stop-signal paradigm

doi:10.1016/j.tics.2008.07.005

Trends in Cognitive Sciences

Volume 12, Issue 11, November 2008, Pages 418-424

https://doi.org/10.1016/j.tics.2008.07.005 Get rights and content

Response inhibition is a hallmark of executive control. The concept refers to the suppression of actions that are no longer required or that are inappropriate, which supports flexible and goal-directed behavior in ever-changing environments. The stop-signal paradigm is most suitable for the study of response inhibition in a laboratory setting. The paradigm has become increasingly popular in cognitive psychology, cognitive neuroscience and psychopathology. We review recent findings in the stop-signal literature with the specific aim of demonstrating how each of these different fields contributes to a better understanding of the processes involved in inhibiting a response and monitoring stopping performance, and more generally, discovering how behavior is controlled.

Section snippets

Successful stopping: inhibition and performance monitoring

In the stop-signal paradigm, subjects perform a go task such as reporting the identity of a stimulus. Occasionally, the go stimulus is followed by a stop signal, which instructs subjects to withhold the response (Figure 1). Stopping a response requires a fast control mechanism that prevents the execution of the motor response [1]. This process interacts with slower control mechanisms that monitor and adjust performance [2].

Neural substrates of stopping and monitoring

Going is associated with activation of a cortico-basal-ganglia-thalamocortical circuit [13]. Recent studies using a variety of methods indicate that stopping is associated with activation of a fronto-basal-ganglia circuit that includes inferior frontal gyrus (IFG; ventrolateral prefrontal cortex), middle frontal gyrus (dorsolateral prefrontal cortex), medial frontal gyrus (MFG) and basal ganglia 14, 15, 16, 17, 18. Results are sometimes inconsistent between studies, possibly because they used

Inhibitory disorders and psychopathology

Response-inhibition deficits have been linked to several psychopathological and neurological disorders. Some disorders, such as autism [37] and schizophrenia [38], are associated with general cognitive impairments in addition to inhibitory deficits. Other disorders, such as attention-deficit/hyperactivity disorder (ADHD) (for a metanalysis, see Ref. [39]) and compulsive disorders [40], are described specifically as inhibitory disorders. In the following sections, we review stop-signal studies

Concluding remarks

The stop-signal paradigm has become a popular tool for the study of response inhibition in cognitive psychology, cognitive neuroscience and psychopathology. Through this paradigm, findings from different fields of research have stimulated each other, leading to integrative, converging conclusions about cognitive control processes involved in stopping and performance monitoring. Cognitive psychologists modeled response inhibition as a race between a go process and a stop process. Cognitive

Acknowledgements

F.V and G.L thank Jeff Schall, Tom Palmeri, Leanne Boucher, Arnaud Szmalec, Matt Crump and three anonymous reviewers for their useful comments on this manuscript, and Jeff Shall for providing the data for Figure I in Box 1. F.V. is a Postdoctoral Fellow of the Research Foundation – Flanders (FWO-Vlaanderen). The work in G.L.'s laboratory is supported by grant BCS 0646588 from the National Science Foundation, grant FA9550–07–1-0192 from the Air Force Office of Scientific Research and grant

References (74)

W.P.M. van den Wildenberg et al.
Developmental trends in simple and selective inhibition of compatible and incompatible responses
J. Exp. Child Psychol.
(2004)
E.E. Emeric
Influence of history on saccade countermanding performance in humans and macaque monkeys
Vision Res.
(2007)
K. Rubia
Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection
Neuroimage
(2003)
P. Nachev
The role of the pre-supplementary motor area in the control of action
Neuroimage
(2007)
K.R. Ridderinkhof
Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning
Brain Cogn.
(2004)
P.G. Enticott
Response inhibition and impulsivity in schizophrenia
Psychiatry Res.
(2008)
A.R. Aron et al.
The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder
Biol. Psychiatry
(2005)
C. Kieling
Neurobiology of attention deficit hyperactivity disorder
Child Adolesc. Psychiatr. Clin. N. Am.
(2008)
M. Liotti
Abnormal brain activity related to performance monitoring and error detection in children with ADHD
Cortex
(2005)
M.T. Fillmore et al.
Impaired inhibitory control of behavior in chronic cocaine users
Drug Alcohol Depend.
(2002)

J.R. Monterosso

Deficits in response inhibition associated with chronic methamphetamine abuse

Drug Alcohol Depend.

(2005)

J.T. Nigg

Poor response inhibition as a predictor of problem drinking and illicit drug use in adolescents at risk for alcoholism and other substance use disorders

J. Am. Acad. Child Adolesc. Psychiatry

(2006)

G.P.H. Band

Horse-race model simulations of the stop-signal procedure

Acta Psychol. (Amst.)

(2003)

F. Verbruggen

The interaction between stop signal inhibition and distractor interference in the flanker and Stroop task

Acta Psychol. (Amst.)

(2004)

F. Verbruggen

Effects of stimulus-stimulus compatibility and stimulus-response compatibility on response inhibition

Acta Psychol. (Amst.)

(2005)

A.R. Aron

Inhibition and the right inferior frontal cortex

Trends Cogn. Sci.

(2004)

J. Derrfuss

Cognitive control in the posterior frontolateral cortex: evidence from common activations in task coordination, interference control, and working memory

Neuroimage

(2004)

C.R. Camalier

Dynamics of saccade target selection: race model analysis of double step and search step saccade production in human and macaque

Vision Res.

(2007)

G.D. Logan

On the ability to inhibit thought and action: a user's guide to the stop signal paradigm

Verbruggen, F. and Logan, G.D. Proactive adjustments of response strategies in the stop-signal paradigm. J. Exp....

G.D. Logan et al.

On the ability to inhibit thought and action: a theory of an act of control

Psychol. Rev.

(1984)

B.R. Williams

Development of inhibitory control across the life span

Dev. Psychol.

(1999)

B.K. Rush

Accounting for cognitive aging: context processing, inhibition or processing speed?

Aging Neuropsychol. Cogn.

(2006)

V. Stuphorn et al.

Executive control of countermanding saccades by the supplementary eye field

Nat. Neurosci.

(2006)

F. Verbruggen

Short-term aftereffects of response inhibition: repetition priming or between-trial control adjustments?

J. Exp. Psychol. Hum. Percept. Perform.

(2008)

R.J. Schachar

Evidence for an error monitoring deficit in attention deficit hyperactivity disorder

J. Abnorm. Child Psychol.

(2004)

F. Verbruggen et al.

Long-term aftereffects of response inhibition: memory retrieval, task goals, and cognitive control

J. Exp. Psychol. Hum. Percept. Perform.

(2008)

Verbruggen, F. and Logan, G.D. Automatic and controlled response inhibition: associative learning in the go/no-go and...

G.E. Alexander

Basal ganglia-thalamocortical circuits - parallel substrates for motor, oculomotor, prefrontal and limbic functions

Prog. Brain Res.

(1990)

A.R. Aron

Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI

J. Neurosci.

(2007)

C.S.R. Li

Imaging response inhibition in a stop-signal task: neural correlates independent of signal monitoring and post-response processing

J. Neurosci.

(2006)

A.R. Aron et al.

Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus

J. Neurosci.

(2006)

A.D. Chevrier

Dissociation of response inhibition and performance monitoring in the stop signal task using event-related fMRI

Hum. Brain Mapp.

(2007)

K. Rubia

Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior Cingulate during error-related processes

Hum. Brain Mapp.

(2007)

C.D. Chambers

Dissociable mechanisms of cognitive control in prefrontal and premotor cortex

J. Neurophysiol.

(2007)

C.D. Chambers

Executive “brake failure” following deactivation of human frontal lobe

J. Cogn. Neurosci.

(2006)

A.R. Aron

Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans

Nat. Neurosci.

(2003)

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Humans express volition by making voluntary choices which, relative to forced choices, can motivate cognitive performance in a variety of tasks. However, a task that requires the generation of motor responses on the basis of external sensory stimulation involves complex underlying cognitive processes, e.g., pre-response processing, response selection, and response execution. The present study investigated how these underlying processes are facilitated by voluntary choice-making. In five experiments, participants were free or forced to choose a task-irrelevant picture from two alternatives, and then completed a conflict task, i.e., Flanker, Stroop, Simon, Stroop-Simon, or Flanker-Simon task, where the conflict effect could occur at different processing levels. Results consistently showed that responses in all tasks were generally faster after voluntary (vs. forced) choices. Importantly, the conflict effect at the response-execution level (i.e., the Simon effect), but not the conflict effect at the pre-response and response-selection levels (i.e., the Flanker and Stroop effects), was reduced by the voluntary choice-making. Model fitting revealed that the peak amplitude of automatic motor activations in the response-execution conflict was smaller after voluntary (vs. forced) choices. These findings suggest that volition motivates subsequent cognitive performance at the response-execution level by attenuating task-irrelevant motor activations.
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Response inhibition is classically investigated using the go/no-go (GNGT) and stop-signal task (SST), which conceptually measure different subprocesses of inhibition. Further, different task versions with varying levels of additional executive control demands exist, making it difficult to identify the core neural correlates of response inhibition independent of variations in task complexity. Using neuroimaging meta-analyses, we show that a divergent pattern of regions is consistently involved in the GNGT versus SST, arguing for different mechanisms involved when performing the two tasks. Further, for the GNGT a strong effect of task complexity was found, with regions of the multiple demand network (MDN) consistently involved particularly in the complex GNGT. In contrast, both standard and complex SST recruited the MDN to a similar degree. These results complement behavioral evidence suggesting that inhibitory control becomes automatic after some practice and is performed without input of higher control regions in the classic, standard GNGT, but continues to be implemented in a top-down controlled fashion in the SST.

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Trends in Cognitive Sciences

ReviewResponse inhibition in the stop-signal paradigm

Section snippets

Successful stopping: inhibition and performance monitoring

Neural substrates of stopping and monitoring

Inhibitory disorders and psychopathology

Concluding remarks

Acknowledgements

J. Exp. Child Psychol.

Vision Res.

Neuroimage

Neuroimage

Brain Cogn.

Psychiatry Res.

Biol. Psychiatry

Child Adolesc. Psychiatr. Clin. N. Am.

Cortex

Drug Alcohol Depend.

Drug Alcohol Depend.

J. Am. Acad. Child Adolesc. Psychiatry

Acta Psychol. (Amst.)

Acta Psychol. (Amst.)

Acta Psychol. (Amst.)

Trends Cogn. Sci.

Neuroimage

Vision Res.

On the ability to inhibit thought and action: a user's guide to the stop signal paradigm

On the ability to inhibit thought and action: a theory of an act of control

Psychol. Rev.

Development of inhibitory control across the life span

Dev. Psychol.

Accounting for cognitive aging: context processing, inhibition or processing speed?

Aging Neuropsychol. Cogn.

Executive control of countermanding saccades by the supplementary eye field

Nat. Neurosci.

Short-term aftereffects of response inhibition: repetition priming or between-trial control adjustments?

J. Exp. Psychol. Hum. Percept. Perform.

Evidence for an error monitoring deficit in attention deficit hyperactivity disorder

J. Abnorm. Child Psychol.

Long-term aftereffects of response inhibition: memory retrieval, task goals, and cognitive control

J. Exp. Psychol. Hum. Percept. Perform.

Basal ganglia-thalamocortical circuits - parallel substrates for motor, oculomotor, prefrontal and limbic functions

Prog. Brain Res.

Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI

J. Neurosci.

Imaging response inhibition in a stop-signal task: neural correlates independent of signal monitoring and post-response processing

J. Neurosci.

Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus

J. Neurosci.

Dissociation of response inhibition and performance monitoring in the stop signal task using event-related fMRI

Hum. Brain Mapp.

Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior Cingulate during error-related processes

Hum. Brain Mapp.

Dissociable mechanisms of cognitive control in prefrontal and premotor cortex

J. Neurophysiol.

Executive “brake failure” following deactivation of human frontal lobe

J. Cogn. Neurosci.

Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans

Nat. Neurosci.

Review
Response inhibition in the stop-signal paradigm