A consensus guide to capturing the ability to inhibit actions and impulsive behaviors in the stop-signal task

Verbruggen, Frederick; Aron, Adam R.; Band, Guido P. H.; Beste, Christian; Bissett, Patrick G.; Brockett, Adam T.; Brown, Joshua W.; Chamberlain, Samuel R.; Chambers, Christopher D.; Colonius, Hans; Colzato, Lorenza S.; Corneil, Brian D.; Coxon, James P.; Dupuis, Annie; Eagle, Dawn M.; Garavan, Hugh; Greenhouse, Ian; Heathcote, Andrew; Huster, René J.; Jahfari, Sara; Kenemans, J. Leon; Leunissen, Inge; Li, Chiang‐Shan R.; Logan, Gordon D.; Matzke, Dora; Morein‐Zamir, Sharon; Murthy, Aditya; Paré, Martin; Poldrack, Russell A.; Ridderinkhof, K. Richard; Robbins, Trevor W.; Roesch, Matthew R.; Rubia, Katya; Schachar, Russell; Schall, Jeffrey D.; Stock, Ann‐Kathrin; Swann, Nicole C.; Thakkar, Katharine N.; Molen, Maurits W. van der; Vermeylen, Luc; Vink, Matthijs; Wessel, Jan R.; Whelan, Robert; Zandbelt, Bram B.; Boehler, C. Nico

doi:10.7554/elife.46323

Cited by 642 publications

(934 citation statements)

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“…Means were extracted for each subject for the following measures: Go-trial reaction time, failed Stop-trial reaction time, Stop-signal delay, Stopping accuracy, and Stop-signal reaction time, which was calculated via the integration method [24].…”

Section: Behavioral Analysismentioning

confidence: 99%

“…Here, we therefore investigate the characteristics of single-trial β-bursting in humans during both the initiation, and particularly, during the rapid cancellation of movement. A large sample of healthy human participants (N=234) performed the stop-signal task [23,24], a motor task that includes both instances of movement initiation (following a Go-signal) and movement cancellation (on trials that include a subsequent Stop-signal). We used noninvasive scalp-EEG recordings to investigate how β-bursting on individual trials indexes both processes and the interaction between them.…”

Section: Introductionmentioning

confidence: 99%

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β-bursts reveal the trial-to-trial dynamics of movement initiation and cancellation

Wessel

2019

Preprint

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The neurophysiological basis of motor processes and their control is of tremendous interest to basic researchers and clinicians alike. Notably, both movement initiation and cancellation are accompanied by prominent field potential changes in the β-frequency band . In trial-averages, movement initiation is indexed by β-band desynchronization over sensorimotor sites, while movement cancellation is signified by β-power increases over (pre)frontal areas. However, averaging misrepresents the true nature of the β-signal. As recent work has highlighted, raw β-band activity is characterized by short-lasting, burst-like events, rather than by steady modulations. To investigate how such β-bursts relate to movement initiation and cancellation in humans, we investigated scalp-recorded β-band activity in 234 healthy subjects performing the Stop-signal task. Four observations were made: First, both movement initiation and cancellation were indexed by systematic, localized changes in β-bursting. While β-bursting at bilateral sensorimotor sites steadily declined during movement initiation, β-bursting increased at fronto-central sites when Stopsignals instructed movement cancellation. Second, the amount of fronto-central β-bursting clearly distinguished successful from unsuccessful movement cancellation. Third, the emergence of fronto-central β-bursting coincided with the latency of the movement cancellation process, indexed by Stop-signal reaction time. Fourth, individual fronto-central β-bursts during movement cancellation were followed by a low-latency re-instantiation of bilateral sensorimotor β-bursting. These findings suggest that β-bursting is a fundamental signature of the motor system, reflecting a steady inhibition of motor cortex that is suppressed during movement initiation, and can be rapidly re-instantiated by frontal areas when movements have to be rapidly cancelled.3 Significance StatementMovement-related β-frequency (15-29Hz) changes are among the most prominent features of neural recordings across species, scales, and methods. However, standard averaging-based methods obscure the true dynamics of β-band activity, which is dominated by short-lived, burst-like events. Here, we demonstrate that both movement-initiation and cancellation in humans are characterized by unique trial-to-trial patterns of β-bursting.Movement initiation is characterized by steady reductions of β-bursting over bilateral sensorimotor sites. In contrast, during rapid movement cancellation, β-bursts first emerge over fronto-central sites typically associated with motor control, after which sensorimotor β-bursting re-initiates. These findings suggest a fundamentally novel, non-invasive measure of the neural interaction underlying movement-initiation and -cancellation, opening new avenues for the study of motor control in health and disease.

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Section: Behavioral Analysismentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

β-bursts reveal the trial-to-trial dynamics of movement initiation and cancellation

Wessel

2019

Preprint

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“…Dysfunctions in behavioral inhibition are involved in many human disorders, including drug addiction (Ersche et al 2012). A standard test of behavioral inhibition is the stop-signal task (Logan & Cowan 1984;Verbruggen et al 2019), in which subjects attempt to respond rapidly to a Go cue, but withhold responding if the Go cue is quickly followed by a Stop cue. The stop-signal task has been invaluable for revealing specific cortical-basal ganglia mechanisms involved in both movement initiation ("Going"; e.g.…”

Section: Introductionmentioning

confidence: 99%

Globus pallidus dynamics reveal covert strategies for behavioral inhibition

Schmidt

Berke

2020

Preprint

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Flexible behavior requires restraint or cancellation of actions that are no longer appropriate. This behavioral inhibition critically relies on frontal cortex -basal ganglia circuits. A central node within the basal ganglia, the globus pallidus pars externa (GPe), has been hypothesized to mediate "proactive" inhibition: being prepared to stop an action if needed. Here we investigate the population dynamics of rat GPe neurons during preparation-to-stop, stopping, and going.Rats could selectively engage proactive inhibition towards one specific action, as shown by slowed reaction times (RTs) for that action. While proactive inhibition was engaged, GPe population activity occupied state-space locations farther from the trajectory followed during normal movement initiation. Furthermore, the specific state-space location was predictive of distinct types of errors: failures to stop, failures to go, and incorrect choices. The slowed RTs on correct proactive trials reflected a starting bias towards the alternative action, which was overcome before making progress towards action initiation. Our results demonstrate that rats can exert cognitive control via strategic positioning of their GPe network state.

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“…We used the last half of the task trials to get a stable estimate of the SSD50, where subjects are able to inhibit 50% of their responses. SSRT was calculated, following the recently published consensus guidelines, using the recommended least-biased non-parametric integration method with replacement of go omissions (Verbruggen et al, 2019). Notably, there were no Go omissions in our data.…”

Section: Stop-signal Taskmentioning

confidence: 99%

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

Madsen

Johansen

Thompson

et al. 2020

Preprint

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The ability to effectively suppress motor response tendencies is essential for focused and goaldirected 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. Highlights• Motor response cancellation, i.e. SSRT, improvement plateaued at 13-14 years of age • Fractional anisotropy (FA) captured maturation of white matter (WM) microstructure• FA in the WM underlying right preSMA (preSMAFA) reflected SSRT improvement with age• Individual SSRT improvement depended on mean right preSMAFA across all DTI sessions • Children with lower mean right preSMAFA had the steepest improvements in SSRT

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A consensus guide to capturing the ability to inhibit actions and impulsive behaviors in the stop-signal task

Cited by 642 publications

References 30 publications

β-bursts reveal the trial-to-trial dynamics of movement initiation and cancellation

β-bursts reveal the trial-to-trial dynamics of movement initiation and cancellation

Globus pallidus dynamics reveal covert strategies for behavioral inhibition

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

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