Distinct frontal systems for response inhibition, attentional capture, and error processing
Open accessAbstract
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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The right IFG facilitates infrequent action-related events by activating nondominant but relevant responses while inhibiting automatic but irrelevant actions at the same time.
“The right IFG, besides detecting changes in stimulus features (Sharp et al. 2010; Dodds et al. 2010), facilitates infrequent action-related events by activating nondominant but relevant responses while inhibiting automatic but irrelevant actions at the same time.”
From Large-scale functional neural network correlates of response inhibition: an fMRI meta-analysis (2017) · cites this paper as Sharp et al. 2010
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Self-citation
- Authors
- Sharp, D. J., Bonnelle, V., De Boissezon, X., Beckmann, C. F., James, S. G., Patel, M. C., & Mehta, M. A.
- Affiliations
- Imperial College London (GB)
- INSERM–Imagerie cérébrale et handicaps neurologiques UMR 825, F-31059 Toulouse, France;
- University of Oxford (GB)
- University of Surrey (GB)
- Charing Cross Hospital (GB)
- King's College London (GB)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-03-10
- Volume
- 107
- Issue
- 13
- Pages
- 6106-6111
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2851908
- OpenAlex
- W1967711862
- Cited by
- 535
- References
- 37
- Citations by year
- 2026: 21 · 2025: 13 · 2024: 20 · 2023: 22 · 2022: 31 · 2021: 34 · 2020: 41 · 2019: 33 · 2018: 34 · 2017: 22 · 2016: 33 · 2015: 39 · 2014: 44 · 2013: 47 · 2012: 50
- FWCI
- 28.05
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
- Keywords
- response inhibition, attentional capture, error processing, stop-signal task, pre-supplementary motor area, right inferior frontal gyrus, anterior cingulate cortex, medial frontal cortex, action stopping, frontal cortex
- MeSH terms
- Adult, Attention, Female, Frontal Lobe, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Models, Neurological, Motor Activity, Motor Cortex, Photic Stimulation, Task Performance and Analysis, Young Adult
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