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: 9.81). 03/2010; 107(13):6106-11. DOI: 10.1073/pnas.1000175107
Source: PubMed

ABSTRACT 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
    • "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; DOI:10.1016/j.pscychresns.2015.07.007 · 2.83 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 · 3.67 Impact Factor
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    • "This confounds attentional processing demands, such as attentional orienting and target detection with response control and inhibition [Dodds et al., 2011; Levy and Wagner, 2011] although see [Smith et al., 2006] for an exception). As attentional orienting and response control and inhibition activate overlapping fronto-parietal regions [Dodds et al., 2011; Hampshire et al., 2010; Sharp et al., 2010], it may well be that group differences in motor-inhibition reported in recent metaanalyses [Cortese et al., 2012; Hart et al., 2013] may not be attributable to response-inhibition or response-control abnormalities per se. "
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    ABSTRACT: Adult ADHD has been linked to impaired motor response inhibition and reduced associated activation in the right inferior frontal cortex (IFC). However, it is unclear whether abnormal inferior frontal activation in adult ADHD is specifically related to a response inhibition deficit or reflects a more general deficit in attentional processing. Using functional magnetic resonance imaging, we tested a group of 19 ADHD patients with no comorbidities and a group of 19 healthy control volunteers on a modified go/no-go task that has been shown previously to distinguish between cortical responses related to response inhibition and attentional shifting. Relative to the healthy controls, ADHD patients showed increased commission errors and reduced activation in inferior frontal cortex during response inhibition. Crucially, this reduced activation was observed when controlling for attentional processing, suggesting that hypoactivation in right IFC in ADHD is specifically related to impaired response inhibition. The results are consistent with the notion of a selective neurocognitive deficit in response inhibition in adult ADHD associated with abnormal functional activation in the prefrontal cortex, whilst ruling out likely group differences in attentional orienting, arousal and motivation. Hum Brain Mapp, 2014. © 2014 The Authors Human Brain Mapping Published by Wiley Periodicals, Inc.
    Human Brain Mapping 10/2014; 35(10). DOI:10.1002/hbm.22539 · 6.92 Impact Factor
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