Large-scale functional neural network correlates of response inhibition: an fMRI meta-analysis

Abstract

An influential hypothesis from the last decade proposed that regions within the right inferior frontal cortex of the human brain were dedicated to supporting response inhibition. There is growing evidence, however, to support an alternative model, which proposes that neural areas associated with specific inhibitory control tasks co-exist as common network mechanisms, supporting diverse cognitive processes. This meta-analysis of 225 studies comprising 323 experiments examined the common and distinct neural correlates of cognitive processes for response inhibition, namely interference resolution, action withholding, and action cancellation. Activation coordinates for each subcategory were extracted using multilevel kernel density analysis (MKDA). The extracted activity patterns were then mapped onto the brain functional network atlas to derive the common (i.e., process-general) and distinct (i.e., domain-oriented) neural network correlates of these processes. Independent of the task types, activation of the right hemispheric regions (inferior frontal gyrus, insula, median cingulate, and paracingulate gyri) and superior parietal gyrus was common across the cognitive processes studied. Mapping the activation patterns to a brain functional network atlas revealed that the fronto-parietal and ventral attention networks were the core neural systems that were commonly engaged in different processes of response inhibition. Subtraction analyses elucidated the distinct neural substrates of interference resolution, action withholding, and action cancellation, revealing stronger activation in the ventral attention network for interference resolution than action inhibition. On the other hand, action withholding/cancellation primarily engaged the fronto-striatal circuit. Overall, our results suggest that response inhibition is a multidimensional cognitive process involving multiple neural regions and networks for coordinating optimal performance. This finding has significant implications for the understanding and assessment of response inhibition.

Keywords: Action restrain; Interference resolution; Meta-analysis; Multilevel kernel density analysis; fMRI.

Fig. 1

Number of studies investigating the neural correlates of response inhibition using fMRI over the last 15 years (1 Jan. 2001–31 Dec. 2015). Two databases—PubMed and Web of Science—were searched using the keywords “response inhibition” and “fMRI”

Fig. 2

Flowchart of searching and selection of literature in response inhibition

Fig. 3

Concordance of brain activation from the MKDA analyses. a Brain areas activated by all contrasts. Brain areas activated in b interference resolution, c action withholding, and d action cancellation. The color bar represents the proportion of studies exhibiting the effect at the peak density weighted by sample size (P)

Fig. 4

Network distribution of concordance of brain activation from the MKDA analyses. a Brain networks activated by all contrasts. Brain networks activated in b interference resolution, c action withholding, and d action cancellation. Of note, the relative distribution (relative) was estimated by the proportion of activated voxels of specific networks versus overall activated voxels; absolute distribution (absolute) was estimated by the proportion of activated voxels of specific networks versus voxels of each template network. FPN fronto-parietal network; DAN dorsal attention network; VAN ventral attention network; SMN somatomotor network; VN visual network; AFN affective network; DMN default mode network

Fig. 5

Common areas among different classifications of response inhibition. IFG.R, right inferior frontal gyrus, MCG.R, right median cingulate and paracingulate gyri

Fig. 6

Direct contrasts of brain activations among the different classifications of response inhibition. a and c Different regions (neural network correlates) of interference resolution (IR) contrasted with action withholding (AW). b and d Different regions (neural network correlates) for interference resolution (IR) contrasted with action cancellation (AC). e and f Different regions (neural network correlates) for action withholding (AW) in contrast with action cancellation (AC). Regions showing differences between each category were listed in the left panel, and the corresponding neural network correlates of regions which showed differences were arranged in the right panel. FPN fronto-parietal network; DAN dorsal attention network; VAN ventral attention network; SMN somatomotor network; VN visual network; AFN affective network; DMN default mode network