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

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.attention | functional MRI | presupplementary motor area | stop signal task | stopping T he control of voluntary action depends critically upon the ability to inhibit unwanted responses. This process has been extensively studied using the Stop Signal Task (SST) (1). Previous work with this task provides evidence that both medial frontal regions, including the presupplementary motor area (pre-SMA), and more lateral regions, including the right inferior frontal gyrus (IFG; rIFG) and insula (Ins), are involved in stopping. However, the specific contributions of these regions to motor control are unresolved (2-4). Many functional imaging studies have demonstrated activation of right inferior frontal regions during stopping (2, 5-8) and individual differences in response inhibition correlate with the magnitude of the IFG/Ins activation during the SST (5). Activation of medial prefrontal regions are also observed during stopping (2, 5). Pre-SMA activation is correlated with the efficiency of inhibitory processing (2), and work in nonhuman primates supports a role for the medial prefrontal regions in behavioral inhibition (9, 10). Neuropsychological studies provide discrepant results, with correlations between the extent of damage and impairments of inhibitory function reported for both the right lateral and medial frontal regions (3, 4).A limitation of much of the previous neuroimaging literature is that "stop trials" conflate p...

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