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
    • "Our data are not consistent with this idea since AI exhibited stronger responses on error trials, in addition to an early increase of activity induced by the salient cues. This electrophysiological pattern may support an account of AI activity that would incorporate over time the effects of stimulus saliency and error-related signals (such as errorawareness ).This interpretation is consistent with several noninvasive neuroimaging studies that either show similar functional responses in AI using an identical paradigm (Ramautar et al. 2006;Sharp et al. 2010) or that report a similar gradient of response within AI with higher BOLD responses when contrasting error to novelty processes (Wessel et al. 2012) or conscious to unconscious errors (Ullsperger et al. 2010;Klein et al. 2013;Charles et al. 2014). Distinguishing pure error-related components from subjective saliency effects that arise in the context of error awareness is by definition a much more complex endeavor. "
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    ABSTRACT: The ability to monitor our own errors is mediated by a network that includes dorsomedial prefrontal cortex (dmPFC) and anterior insula (AI). However, the dynamics of the underlying neurophysiological processes remain unclear. In particular, whether AI is on the receiving or driving end of the error-monitoring network is unresolved. Here, we recorded intracerebral electroencephalography signals simultaneously from AI and dmPFC in epileptic patients while they performed a stop-signal task. We found that errors selectively modulated broadband neural activity in human AI. Granger causality estimates revealed that errors were immediately followed by a feedforward influence from AI onto anterior cingulate cortex and, subsequently, onto presupplementary motor area. The reverse pattern of information flow was observed on correct responses. Our findings provide the first direct electrophysiological evidence indicating that the anterior insula rapidly detects and conveys error signals to dmPFC, while the latter might use this input to adapt behavior following inappropriate actions.
    No preview · Article · Jan 2016 · Cerebral Cortex
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    • "By comparing how participants responded to go and continue signals in the stop-signal task, we found that, as expected, participants did not respond to a continue signal the same way as to a go signal. As reported in Sharp et al.'s [45] study, participants consistently took longer to respond to a continue signal than to a go signal. Importantly , we also found that this fundamental difference between go and continue RTs was not affected by TMS. "
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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.
    Full-text · Article · Jan 2016 · Behavioural Brain Research
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    • "Whereas reactive inhibitory control is cued by the stop signal, proactive inhibitory control is triggered by information stored in working memory (Aron, 2011). Indeed, it has been suggested that the right IFG could be involved in the detection of novel stimuli (i.e., stop signal; Erika-Florence, Leech, & Hampshire, 2014; Hampshire, Chamberlain, Monti, Duncan, & Owen, 2010; Sharp et al., 2010; Chikazoe, Jimura, Asari, et al., 2009) and right IFG stimulation could facilitate response inhibition by increasing the arousal and motivation . This is consistent with previous findings of the right IFG's role in the detection of changes in response contingency (Xue et al., 2013; Mullette-Gillman & Huettel, 2009). "
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    ABSTRACT: 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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