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

Division of Experimental Medicine, Imperial College London, London W12 0NN, United Kingdom.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 03/2010; 107(13):6106-11. DOI: 10.1073/pnas.1000175107
Source: PubMed


Stopping an action in response to an unexpected event requires both that the event is attended to, and that the action is inhibited. Previous neuroimaging investigations of stopping have failed to adequately separate these cognitive elements. Here we used a version of the widely used Stop Signal Task that controls for the attentional capture of stop signals. This allowed us to fractionate the contributions of frontal regions, including the right inferior frontal gyrus and medial frontal cortex, to attentional capture, response inhibition, and error processing. A ventral attentional system, including the right inferior frontal gyrus, has been shown to respond to unexpected stimuli. In line with this evidence, we reasoned that lateral frontal regions support attentional capture, whereas medial frontal regions, including the presupplementary motor area (pre-SMA), actually inhibit the ongoing action. We tested this hypothesis by contrasting the brain networks associated with the presentation of unexpected stimuli against those associated with outright stopping. Functional MRI images were obtained in 26 healthy volunteers. Successful stopping was associated with activation of the right inferior frontal gyrus, as well as the pre-SMA. However, only activation of the pre-SMA differentiated stopping from a high-level baseline that controlled for attentional capture. As expected, unsuccessful attempts at stopping activated the anterior cingulate cortex. In keeping with work in nonhuman primates these findings demonstrate that successful motor inhibition is specifically associated with pre-SMA activation.

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Available from: Xavier De Boissezon, Oct 17, 2014
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    • "By comparing two groups of participants who differed only in the amount of slowing on continue trials but not in any other go or stop measures, we found that temporary suppression of right pre-SMA activity prolonged the RT on continue trials of those who exhibited low slowing but not those with high slowing, whereas no significant effect on performance was found after rIFG stimulation. These results replicate Sharp et al.'s [45] findings and provide new causal evidence that the right posterior pre-SMA is associated with response slowing during conditional stopping. More importantly, the differential group response in the pre-SMA TMS condition suggests that it could be the right pre-SMA's efficiency in updating motor planning and reinitiating a partially inhibited response that was associated with the amount of slowing in response to continue trials. "
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    ABSTRACT: Although both the presupplementary motor area (pre-SMA) and the right inferior frontal gyrus (rIFG) have been demonstrated to be critical for response inhibition, there is still considerable disagreement over the roles they play in the process. In the present study, we investigated the causal relations of the pre-SMA and the rIFG in a conditional stop-signal task by applying offline theta-burst transcranial magnetic stimulation. The task introduced a continue condition, which requires the same motor response as in a go trial but captures attention as in a stop trial. We found great individual differences in the amount of slowing on continue trials. Temporary suppression of pre-SMA activity prolonged the continue RT in participants who slowed little in response to continue trials, whereas disruption of the rIFG did not lead to significant changes in performance irrespective of the degree of slowing. Our results contribute to the understanding of the role of the pre-SMA by providing causal evidence that it is involved in response slowing on continue trials during conditional stopping, and it is likely that its efficiency in updating motor planning and reinitiating an inhibited response was associated with the amount of slowing. Copyright © 2015. Published by Elsevier B.V.
    Behavioural brain research 08/2015; DOI:10.1016/j.bbr.2015.08.024 · 3.03 Impact Factor
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    • "A few studies with the stop task have attempted to control for attentional capture in healthy adult populations with different results. Sharp et al. (2010) added infrequent continue signals to the stop task to control for attentional capture. Brain activation for the control and successful inhibition conditions overlapped in the rIFG, with only activation in the pre-SMA being uniquely associated with inhibition. "
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    ABSTRACT: The stop-signal task has been used extensively to investigate the neural correlates of inhibition deficits in children with ADHD. However, previous findings of atypical brain activation during the stop-signal task in children with ADHD may be confounded with attentional processes, precluding strong conclusions on the nature of these deficits. In addition, there are recent concerns on the construct validity of the SSRT metric. The aim of this study was to control for confounding factors and improve the specificity of the stop-signal task to investigate inhibition mechanisms in children with ADHD. FMRI was used to measure inhibition related brain activation in 17 typically developing children (TD) and 21 children with ADHD, using a highly controlled version of the stop-signal task. Successful inhibition trials were contrasted with control trials that were comparable in frequency, visual presentation and absence of motor response. We found reduced brain activation in children with ADHD in key inhibition areas, including the right inferior frontal gyrus/insula, and anterior cingulate/dorsal medial prefrontal cortex. Using a more stringent controlled design, this study replicated and specified previous findings of atypical brain activation in ADHD during motor response inhibition. Copyright © 2015 Elsevier Ireland Ltd. All rights reserved.
    Psychiatry Research: Neuroimaging 07/2015; 233(2). DOI:10.1016/j.pscychresns.2015.07.007 · 2.42 Impact Factor
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    • "Moreover, we have previously shown that repetitive transcranial magnetic stimulation over the rIFG induces faster response inhibition (Zandbelt et al., 2013a), providing additional evidence in support of the notion that this region is involved in the detection of a salient stop-signal (i.e. the automatic stopping of the white bar moving ). Our finding is also in line with previous studies revealing the importance of the rIFG for the detection of task-relevant stimuli (Duann et al., 2009; Hampshire et al., 2010; Sharp et al., 2010). Furthermore, the rIFG and rIPC are known for their role in working memory needed for flexible adjustments of actions based on context (Nee & Brown, 2013). "
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    ABSTRACT: The subjective belief of what will happen plays an important role across many cognitive domains, including response inhibition. However, tasks that study inhibition do not distinguish between the processing of objective contextual cues indicating stop-signal probability and the subjective expectation that a stop-signal will or will not occur. Here we investigated the effects of stop-signal probability and the expectation of a stop-signal on proactive inhibition. Twenty participants performed a modified stop-signal anticipation task while being scanned with functional magnetic resonance imaging. At the beginning of each trial, the stop-signal probability was indicated by a cue (0% or > 0%), and participants had to indicate whether they expected a stop-signal to occur (yes/no/don't know). Participants slowed down responding on trials with a > 0% stop-signal probability, but this proactive response slowing was even greater when they expected a stop-signal to occur. Analyses were performed in brain regions previously associated with proactive inhibition. Activation in the striatum, supplementary motor area and left dorsal premotor cortex during the cue period was increased when participants expected a stop-signal to occur. In contrast, activation in the right inferior frontal gyrus and right inferior parietal cortex activity during the stimulus-response period was related to the processing of contextual cues signalling objective stop-signal probability, regardless of expectation. These data show that proactive inhibition depends on both the processing of objective contextual task information and the subjective expectation of stop-signals. © 2015 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
    European Journal of Neuroscience 04/2015; 41(8). DOI:10.1111/ejn.12879 · 3.18 Impact Factor
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