Decomposing Decision Components in the Stop-signal Task: A Model-based Approach to Individual Differences in Inhibitory Control

The stop-signal task, in which participants must inhibit prepotent responses, has been used to identify neural systems that vary with individual differences in inhibitory control. To explore how these differences relate to other aspects of decision making, a drift-diffusion model of simple decisions was fitted to stop-signal task data from go trials to extract measures of caution, motor execution time, and stimulus processing speed for each of 123 participants. These values were used to probe fMRI data to explore individual differences in neural activation. Faster processing of the go stimulus correlated with greater activation in the right frontal pole for both go and stop trials. On stop trials, stimulus processing speed also correlated with regions implicated in inhibitory control, including the right inferior frontal gyrus, medial frontal gyrus, and BG. Individual differences in motor execution time correlated with activation of the right parietal cortex. These findings suggest a robust relationship between the speed of stimulus processing and inhibitory processing at the neural level. This model-based approach provides novel insight into the interrelationships among decision components involved in inhibitory control and raises interesting questions about strategic adjustments in performance and inhibitory deficits associated with psychopathology.

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Transcranial Magnetic Stimulation and Functional MRI Reveal Cortical and Subcortical Interactions during Stop-signal Response Inhibition

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00309 ◽

2013 ◽

Vol 25 (2) ◽

pp. 157-174 ◽

Cited By ~ 65

Author(s):

Bram B. Zandbelt ◽

Mirjam Bloemendaal ◽

Janna Marie Hoogendam ◽

René S. Kahn ◽

Matthijs Vink

Keyword(s):

Inhibitory Control ◽

Primary Motor Cortex ◽

Functional Organization ◽

Stop Signal ◽

Stop Signal Task ◽

Reactive Inhibition ◽

Reactive Control ◽

Motor Complex ◽

Repetitive Tms ◽

The Right

Stopping an action requires suppression of the primary motor cortex (M1). Inhibitory control over M1 relies on a network including the right inferior frontal cortex (rIFC) and the supplementary motor complex (SMC), but how these regions interact to exert inhibitory control over M1 is unknown. Specifically, the hierarchical position of the rIFC and SMC with respect to each other, the routes by which these regions control M1, and the causal involvement of these regions in proactive and reactive inhibition remain unclear. We used off-line repetitive TMS to perturb neural activity in the rIFC and SMC followed by fMRI to examine effects on activation in the networks involved in proactive and reactive inhibition, as assessed with a modified stop-signal task. We found repetitive TMS effects on reactive inhibition only. rIFC and SMC stimulation shortened the stop-signal RT (SSRT) and a shorter SSRT was associated with increased M1 deactivation. Furthermore, rIFC and SMC stimulation increased right striatal activation, implicating frontostriatal pathways in reactive inhibition. Finally, rIFC stimulation altered SMC activation, but SMC stimulation did not alter rIFC activation, indicating that rIFC lies upstream from SMC. These findings extend our knowledge about the functional organization of inhibitory control, an important component of executive functioning, showing that rIFC exerts reactive control over M1 via SMC and right striatum.

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Establishing a Right Frontal Beta Signature for Stopping Action in Scalp EEG: Implications for Testing Inhibitory Control in Other Task Contexts

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01183 ◽

2018 ◽

Vol 30 (1) ◽

pp. 107-118 ◽

Cited By ~ 28

Author(s):

Johanna Wagner ◽

Jan R. Wessel ◽

Ayda Ghahremani ◽

Adam R. Aron

Keyword(s):

Frontal Cortex ◽

Inhibitory Control ◽

Spectral Power ◽

Stop Signal ◽

Stop Signal Task ◽

Beta Band ◽

Unexpected Events ◽

Time Frequency ◽

Inferior Frontal Cortex ◽

The Right

Many studies have examined the rapid stopping of action as a proxy of human self-control. Several methods have shown that a critical focus for stopping is the right inferior frontal cortex. Moreover, electrocorticography studies have shown beta band power increases in the right inferior frontal cortex and in the BG for successful versus failed stop trials, before the time of stopping elapses, perhaps underpinning a prefrontal–BG network for inhibitory control. Here, we tested whether the same signature might be visible in scalp electroencephalography (EEG)—which would open important avenues for using this signature in studies of the recruitment and timing of prefrontal inhibitory control. We used independent component analysis and time–frequency approaches to analyze EEG from three different cohorts of healthy young volunteers (48 participants in total) performing versions of the standard stop signal task. We identified a spectral power increase in the band 13–20 Hz that occurs after the stop signal, but before the time of stopping elapses, with a right frontal topography in the EEG. This right frontal beta band increase was significantly larger for successful compared with failed stops in two of the three studies. We also tested the hypothesis that unexpected events recruit the same frontal system for stopping. Indeed, we show that the stopping-related right-lateralized frontal beta signature was also active after unexpected events (and we accordingly provide data and scripts for the method). These results validate a right frontal beta signature in the EEG as a temporally precise and functionally significant neural marker of the response inhibition process.

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The Role of the Frontal and Parietal Cortex in Proactive and Reactive Inhibitory Control: A Transcranial Direct Current Stimulation Study

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00888 ◽

2016 ◽

Vol 28 (1) ◽

pp. 177-186 ◽

Cited By ~ 35

Author(s):

Ying Cai ◽

Siyao Li ◽

Jing Liu ◽

Dawei Li ◽

Zifang Feng ◽

...

Keyword(s):

Inhibitory Control ◽

Direct Current ◽

Transcranial Direct Current Stimulation ◽

Stop Signal ◽

Causal Role ◽

Stop Signal Task ◽

Proactive Control ◽

Reactive Control ◽

The Right

Mounting evidence suggests that response inhibition involves both proactive and reactive inhibitory control, yet its underlying neural mechanisms remain elusive. In particular, the roles of the right inferior frontal gyrus (IFG) and inferior parietal lobe (IPL) in proactive and reactive inhibitory control are still under debate. This study aimed at examining the causal role of the right IFG and IPL in proactive and reactive inhibitory control, using transcranial direct current stimulation (tDCS) and the stop signal task. Twenty-two participants completed three sessions of the stop signal task, under anodal tDCS in the right IFG, the right IPL, or the primary visual cortex (VC; 1.5 mA for 15 min), respectively. The VC stimulation served as the active control condition. The tDCS effect for each condition was calculated as the difference between pre- and post-tDCS performance. Proactive control was indexed by the RT increase for go trials (or preparatory cost), and reactive control by the stop signal RT. Compared to the VC stimulation, anodal stimulation of the right IFG, but not that of the IPL, facilitated both proactive and reactive control. However, the facilitation of reactive control was not mediated by the facilitation of proactive control. Furthermore, tDCS did not affect the intraindividual variability in go RT. These results suggest a causal role of the right IFG, but not the right IPL, in both reactive and proactive inhibitory control.

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Effect of obesity on inhibitory control in preadolescents during stop-signal task. An event-related potentials study

International Journal of Psychophysiology ◽

10.1016/j.ijpsycho.2021.04.003 ◽

2021 ◽

Author(s):

Graciela C. Alatorre-Cruz ◽

Heather Downs ◽

Darcy Hagood ◽

Seth T. Sorensen ◽

D. Keith Williams ◽

...

Keyword(s):

Inhibitory Control ◽

Event Related Potentials ◽

Stop Signal ◽

Stop Signal Task ◽

Related Potentials

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Cortical silent period reflects individual differences in action stopping performance

Scientific Reports ◽

10.1038/s41598-021-94494-w ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Mario Paci ◽

Giulio Di Cosmo ◽

Mauro Gianni Perrucci ◽

Francesca Ferri ◽

Marcello Costantini

Keyword(s):

Individual Differences ◽

Response Inhibition ◽

Primary Motor Cortex ◽

Silent Period ◽

Intracortical Inhibition ◽

Stop Signal ◽

Stop Signal Task ◽

Behavioral Differences ◽

Cortical Silent Period ◽

Stop Signal Reaction Time

AbstractInhibitory control is the ability to suppress inappropriate movements and unwanted actions, allowing to regulate impulses and responses. This ability can be measured via the Stop Signal Task, which provides a temporal index of response inhibition, namely the stop signal reaction time (SSRT). At the neural level, Transcranial Magnetic Stimulation (TMS) allows to investigate motor inhibition within the primary motor cortex (M1), such as the cortical silent period (CSP) which is an index of GABAB-mediated intracortical inhibition within M1. Although there is strong evidence that intracortical inhibition varies during action stopping, it is still not clear whether differences in the neurophysiological markers of intracortical inhibition contribute to behavioral differences in actual inhibitory capacities. Hence, here we explored the relationship between intracortical inhibition within M1 and behavioral response inhibition. GABABergic-mediated inhibition in M1 was determined by the duration of CSP, while behavioral inhibition was assessed by the SSRT. We found a significant positive correlation between CSP’s duration and SSRT, namely that individuals with greater levels of GABABergic-mediated inhibition seem to perform overall worse in inhibiting behavioral responses. These results support the assumption that individual differences in intracortical inhibition are mirrored by individual differences in action stopping abilities.

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Inhibitory Control is Slowed in Patients with Right Superior Medial Frontal Damage

Journal of Cognitive Neuroscience ◽

10.1162/jocn.2006.18.11.1843 ◽

2006 ◽

Vol 18 (11) ◽

pp. 1843-1849 ◽

Cited By ~ 160

Author(s):

Darlene Floden ◽

Donald T. Stuss

Keyword(s):

Inhibitory Control ◽

Stop Signal Task ◽

Inhibitory System ◽

Frontal Lobe Lesions ◽

Comprehensive Knowledge ◽

Neural Underpinnings ◽

Neurologically Normal ◽

The Right ◽

Shed Light ◽

Rule Out

Inhibitory control is an essential part of behavior. Comprehensive knowledge of the neural underpinnings will shed light on complex behavior, its breakdown in neurological and psychological disorders, and current and future techniques for the pharmacological or structural remediation of disinhibition. This study investigated the neural mechanisms involved in rapid response inhibition. The stop signal task was used to estimate inhibitory speed in a group of neurologically normal control subjects and patients with discrete frontal lobe lesions. Task procedures were controlled to rule out probable confounds related to strategic changes in task effort. The findings indicate that the frontal lobes are necessary for inhibitory control and, furthermore, that the integrity of the right superior medial frontal region is key for rapid inhibitory control under conditions controlling for strategically slow responses, forcing reliance more on a rapid, “kill-switch” inhibitory system. These results are interpreted within an anatomical framework of corticospinal motor control.

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Maturational trajectories of white matter microstructure underlying the right presupplementary motor area reflect individual improvements in motor response cancellation in children and adolescents

10.1101/2020.03.13.990507 ◽

2020 ◽

Author(s):

Kathrine Skak Madsen ◽

Louise Baruël Johansen ◽

Wesley K. Thompson ◽

Hartwig R. Siebner ◽

Terry L. Jernigan ◽

...

Keyword(s):

White Matter ◽

Children And Adolescents ◽

Fractional Anisotropy ◽

Motor Response ◽

Stop Signal ◽

Motor Area ◽

Stop Signal Task ◽

List Type ◽

White Matter Microstructure ◽

The Right

AbstractThe ability to effectively suppress motor response tendencies is essential for focused and goal-directed behavior. Here, we tested the hypothesis that developmental improvement in the ability to cancel a motor response is reflected by maturational changes in the white matter underlying the right presupplementary motor area (preSMA) and posterior inferior frontal gyrus (IFG), two cortical key areas of the fronto-basal ganglia “stopping” network. Eighty-eight typically-developing children and adolescents, aged 7-19 years, were longitudinally assessed with the stop-signal task (SST) and diffusion tensor imaging (DTI) of the brain over a period of six years. Participants were examined from two to nine times with an average of 6.6 times, resulting in 576 SST-DTI datasets. We applied tract-based spatial statistics to extract mean fractional anisotropy (FA) from regions-of-interest in the white matter underlying the right IFG (IFGFA) and right preSMA (preSMAFA) at each time point. Motor response cancelation performance, estimated with the stop-signal reaction time (SSRT), improved with age. Initially well performing children plateaued around the age of 11 years, while initially poor performers caught up at the age of 13-14 years. White matter microstructure continued to mature across the investigated age range. Males generally displayed linear maturational trajectories, while females displayed more curvilinear trajectories that leveled off around 12-14 years of age. Maturational increases in right preSMAFA but not right IFGFA were associated with developmental improvements in SSRT. This association differed depending on the mean right preSMAFA across the individual maturational trajectory. Children with lower mean right preSMAFA exhibited poorer SSRT performance at younger ages but steeper developmental trajectories of SSRT improvement. Children with higher mean right preSMAFA exhibited flatter trajectories of SSRT improvement along with faster SSRT already at the first assessments. The results suggest that no further improvement in motor response cancellation is achieved once a certain level of maturity in the white matter underlying the right preSMA is reached. Similar dynamics may apply to other behavioral read-outs and brain structures and, thus, need to be considered in longitudinal MRI studies designed to map brain structural correlates of behavioral changes during development.HighlightsMotor response cancellation, i.e. SSRT, improvement plateaued at 13-14 years of ageFractional anisotropy (FA) captured maturation of white matter (WM) microstructureFA in the WM underlying right preSMA (preSMAFA) reflected SSRT improvement with ageIndividual SSRT improvement depended on mean right preSMAFA across all DTI sessionsChildren with lower mean right preSMAFA had the steepest improvements in SSRT

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BOLD differences normally attributed to inhibitory control predict symptoms, not task-directed inhibitory control in ADHD

10.1101/699728 ◽

2019 ◽

Author(s):

Andre Chevrier ◽

Russell J. Schachar

Keyword(s):

Inhibitory Control ◽

Error Detection ◽

Healthy Subjects ◽

Stop Signal ◽

Therapeutic Interventions ◽

Stop Signal Task ◽

Neural Processing ◽

Significant Group ◽

Significant Group Difference ◽

Symptomatic Behavior

AbstractBackgroundAltered brain activity that has been observed in attention deficit hyperactivity disorder (ADHD) while performing cognitive control tasks like the stop signal task (SST), has generally been interpreted as reflecting either weak (under-active) or compensatory (over-active) versions of the same functions as in healthy controls. If so, then regional activities that correlate with the efficiency of inhibitory control (i.e. stop signal reaction time, SSRT) in healthy subjects should also correlate with SSRT in ADHD. Here we test the alternate hypothesis that BOLD differences might instead reflect the redirection of neural processing resources normally used for task-directed inhibitory control, toward actively managing symptomatic behavior. If so, then activities that correlate with SSRT in TD should instead correlate with inattentive and hyperactive symptoms in ADHD.MethodsWe used fMRI in 14 typically developing (TD) and 14 ADHD adolescents performing the SST, and in a replication sample of 14 healthy adults. First we identified significant group BOLD differences during all phases of activity in the SST (i.e. warning, response, reactive inhibition, error detection and post-error slowing). Next, we correlated these phases of activity with SSRT in TD, and with SSRT, inattentive and hyperactive symptom scores in ADHD. We then identified whole brain significant correlations in regions of significant group difference in activity.ResultsOnly three regions of significant group difference were correlated with SSRT in TD and replication groups (left and right inferior frontal gyri (IFG) during error detection, and hypothalamus during post-error slowing). Consistent with regions of altered activity managing symptomatic behavior instead of task-directed behavior, left IFG correlated with greater inattentive score, right IFG correlated with lower hyperactive score, and hypothalamus correlated with greater inattentive score and oppositely correlated with SSRT compared to TD.ConclusionsResults are consistent with stimuli that elicit task-directed integration of neural processing in healthy subjects, instead directing integrated function towards managing symptomatic behavior in ADHD. The ability of the current approach to determine whether altered neural activities reflect comparable functions in ADHD and control groups has broad implications for the development and monitoring of therapeutic interventions.

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The motor inhibitory network in patients with asymmetrical Parkinson’s disease: An fMRI study

Brain Imaging and Behavior ◽

10.1007/s11682-021-00587-5 ◽

2022 ◽

Author(s):

Francis R. Loayza ◽

Ignacio Obeso ◽

Rafael González Redondo ◽

Federico Villagra ◽

Elkin Luis ◽

...

Keyword(s):

Parkinson’S Disease ◽

Parkinson's Disease ◽

Subthalamic Nucleus ◽

Inferior Frontal Gyrus ◽

Stop Signal ◽

Stop Signal Task ◽

Healthy Controls ◽

Inhibitory Network ◽

Fmri Study ◽

The Right

AbstractRecent imaging studies with the stop-signal task in healthy individuals indicate that the subthalamic nucleus, the pre-supplementary motor area and the inferior frontal gyrus are key components of the right hemisphere “inhibitory network”. Limited information is available regarding neural substrates of inhibitory processing in patients with asymmetric Parkinson’s disease. The aim of the current fMRI study was to identify the neural changes underlying deficient inhibitory processing on the stop-signal task in patients with predominantly left-sided Parkinson’s disease. Fourteen patients and 23 healthy controls performed a stop-signal task with the left and right hands. Behaviorally, patients showed delayed response inhibition with either hand compared to controls. We found small imaging differences for the right hand, however for the more affected left hand when behavior was successfully inhibited we found reduced activation of the inferior frontal gyrus bilaterally and the insula. Using the stop-signal delay as regressor, contralateral underactivation in the right dorsolateral prefrontal cortex, inferior frontal and anterior putamen were found in patients. This finding indicates dysfunction of the right inhibitory network in left-sided Parkinson’s disease. Functional connectivity analysis of the left subthalamic nucleus showed a significant increase of connectivity with bilateral insula. In contrast, the right subthalamic nucleus showed increased connectivity with visuomotor and sensorimotor regions of the cerebellum. We conclude that altered inhibitory control in left-sided Parkinson’s disease is associated with reduced activation in regions dedicated to inhibition in healthy controls, which requires engagement of additional regions, not observed in controls, to successfully stop ongoing actions.

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Handedness Does Not Impact Inhibitory Control, but Movement Execution and Reactive Inhibition Are More under a Left-Hemisphere Control

Symmetry ◽

10.3390/sym13091602 ◽

2021 ◽

Vol 13 (9) ◽

pp. 1602

Author(s):

Christian Mancini ◽

Giovanni Mirabella

Keyword(s):

Left Hemisphere ◽

Inhibitory Control ◽

Right Hemisphere ◽

Dominant Role ◽

Hemispheric Specialization ◽

Arm Movement ◽

Proactive Inhibition ◽

Stop Signal Task ◽

The Right

The relationship between handedness, laterality, and inhibitory control is a valuable benchmark for testing the hypothesis of the right-hemispheric specialization of inhibition. According to this theory, and given that to stop a limb movement, it is sufficient to alter the activity of the contralateral hemisphere, then suppressing a left arm movement should be faster than suppressing a right-arm movement. This is because, in the latter case, inhibitory commands produced in the right hemisphere should be sent to the other hemisphere. Further, as lateralization of cognitive functions in left-handers is less pronounced than in right-handers, in the former, the inhibitory control should rely on both hemispheres. We tested these predictions on a medium-large sample of left- and right-handers (n = 52). Each participant completed two sessions of the reaching versions of the stop-signal task, one using the right arm and one using the left arm. We found that reactive and proactive inhibition do not differ according to handedness. However, we found a significant advantage of the right versus the left arm in canceling movements outright. By contrast, there were no differences in proactive inhibition. As we also found that participants performed movements faster with the right than with the left arm, we interpret our results in light of the dominant role of the left hemisphere in some aspects of motor control.

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