Dataset Information

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.

SUBMITTER: Sharp DJ

PROVIDER: S-EPMC2851908 | biostudies-other | 2010 Mar

REPOSITORIES: biostudies-other

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

Sharp D J DJ Bonnelle V V De Boissezon X X Beckmann C F CF James S G SG Patel M C MC Mehta M A MA

Proceedings of the National Academy of Sciences of the United States of America 20100310 13

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, ...[more]

PMID: 20220100

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Project description:Inhibitory control relies on attention, inhibition, and other functions that are integrated across neural networks in an interactive manner. Functional MRI studies have provided excellent spatial mapping of the involved regions. However, finer temporal resolution is needed to capture the underlying neural dynamics and the pattern of their functional contributions. Here, we used anatomically-constrained magnetoencephalography (aMEG) which combines MEG with structural MRI to examine how the spatial ("where") and temporal ("when") processing stages and interregional co-oscillations unfold in real time to contribute to inhibitory control. Healthy participants completed a modified Go/NoGo paradigm in which a subset of stimuli was modified to be visually salient (SAL). Compared to the non-modified condition, the SAL manipulation facilitated response withholding on NoGo trials and hindered responding to Go stimuli, reflecting attentional capture effectuated by an orienting response to SAL stimuli. aMEG source estimates indicate SAL stimuli elicited the attentional "circuit breaker" effect through early activity within a right-lateralized network centered around the lateral temporal cortex with additional activity in the pre-supplementary motor area (preSMA) and anterior insula (aINS/FO). Activity of the bilateral inferior frontal cortex responded specifically to inhibitory demands and was generally unaffected by the attentional manipulation. In contrast, early aINS/FO activity was sensitive to stimulus salience while subsequent activity was specific to inhibitory control. Activity estimated to the medial prefrontal cortex including the dorsal anterior cingulate cortex and preSMA reflected an integrative role that was sensitive to both inhibitory and attentional stimulus properties. At the level of neurofunctional networks, neural synchrony in the theta band (4-7 Hz) revealed interactions between principal cortical regions subserving attentional and inhibitory processes. Together, these results underscore the dynamic, integrative processing stages underlying inhibitory control.

Project description:Microsaccades exhibit systematic oscillations in direction after spatial cueing, and these oscillations correlate with facilitatory and inhibitory changes in behavioral performance in the same tasks. However, independent of cueing, facilitatory and inhibitory changes in visual sensitivity also arise pre-microsaccadically. Given such pre-microsaccadic modulation, an imperative question to ask becomes: how much of task performance in spatial cueing may be attributable to these peri-movement changes in visual sensitivity? To investigate this question, we adopted a theoretical approach. We developed a minimalist model in which: (1) microsaccades are repetitively generated using a rise-to-threshold mechanism, and (2) pre-microsaccadic target onset is associated with direction-dependent modulation of visual sensitivity, as found experimentally. We asked whether such a model alone is sufficient to account for performance dynamics in spatial cueing. Our model not only explained fine-scale microsaccade frequency and direction modulations after spatial cueing, but it also generated classic facilitatory (i.e., attentional capture) and inhibitory [i.e., inhibition of return (IOR)] effects of the cue on behavioral performance. According to the model, cues reflexively reset the oculomotor system, which unmasks oscillatory processes underlying microsaccade generation; once these oscillatory processes are unmasked, "attentional capture" and "IOR" become direct outcomes of pre-microsaccadic enhancement or suppression, respectively. Interestingly, our model predicted that facilitatory and inhibitory effects on behavior should appear as a function of target onset relative to microsaccades even without prior cues. We experimentally validated this prediction for both saccadic and manual responses. We also established a potential causal mechanism for the microsaccadic oscillatory processes hypothesized by our model. We used retinal-image stabilization to experimentally control instantaneous foveal motor error during the presentation of peripheral cues, and we found that post-cue microsaccadic oscillations were severely disrupted. This suggests that microsaccades in spatial cueing tasks reflect active oculomotor correction of foveal motor error, rather than presumed oscillatory covert attentional processes. Taken together, our results demonstrate that peri-microsaccadic changes in vision can go a long way in accounting for some classic behavioral phenomena.

Dataset Information

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

Publications

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

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