Meta-analytic evidence for a joint neural mechanism underlying response inhibition and state anger

Abstract

Although anger may weaken response inhibition (RI) by allowing outbursts to bypass deliberate processing, it is equally likely that RI deficits precipitate a state of anger (SA). In adolescents, for instance, anger occurs more frequently and often leads to escalating aggressive behaviors. Even though RI is considered a key component in explaining individual differences in SA expression, the neural overlap between SA and RI remains elusive. Here, we aimed to meta-analytically revisit and update the neural correlates of motor RI, to determine a consistent neural architecture of SA, and to identify their joint neural network. Considering that inhibitory abilities follow a protracted maturation until early adulthood, we additionally computed RI meta-analyses in youths and adults. Using activation likelihood estimation, we calculated twelve meta-analyses across 157 RI and 39 SA experiments on healthy individuals. Consistent with previous findings, RI was associated with a broad frontoparietal network including the anterior insula/inferior frontal gyrus (aI/IFG), premotor and midcingulate cortices, extending into right temporoparietal areas. Youths showed convergent activity in right midcingulate and medial prefrontal areas, left aI/IFG, and the temporal poles. SA, on the other hand, reliably recruited the right aI/IFG and anterior cingulate cortex. Conjunction analyses between RI and SA yielded a single convergence cluster in the right aI/IFG. While frontoparietal networks and bilateral aI are ubiquitously recruited during RI, the right aI/IFG cluster likely represents a node in a dynamically-adjusting monitoring network that integrates salient information thereby facilitating the execution of goal-directed behaviors under highly unpredictable scenarios.

Keywords: activation likelihood meta-analysis; anterior insula, inferior frontal gyrus; frontoparietal; monitoring network; response inhibition; state anger; temporoparietal.

FIGURE 1

Flowchart of the different meta‐analytic steps (cf., PRISMA). In total, 12 meta‐analyses including 157 response inhibition and 39 state anger experiments were calculated. * indicates the meta‐analysis fell short of the recommended experiment sample size for detecting true effects. ALE, activation likelihood estimation; RI, response inhibition; ROI, region of interest; SA, state anger

FIGURE 2

Convergent response inhibition clusters across subjects and tasks (collapsed across go‐no/go and stop‐signal tasks). The overall ALE analysis (red) shows a broad frontoparietal network extending into temporo‐occipital areas that serves successful response inhibition. Sub‐analyses in youths (green) showed convergent activity in midcingulate and medial prefrontal areas, left aI/ IFG, and the temporal poles, while adults (magenta) rely on a distributed frontoparietal network responsible for adequate inhibitory control. Results survived cluster level FWE correction for multiple comparisons (p < .05, cluster forming threshold at voxel level p < .001 using 5,000 permutations; ALE scores ranged from a minimum value of 0.022–0.051). ALE, activation likelihood estimation; FWE, family‐wise error (correction)

FIGURE 3

(a) Main effect of state anger. Meta‐analyzing state anger experiments yielded two clusters of convergent activity in the anterior cingulate cortex and the right aI/IFG. (b) Conjunction analysis between successful response inhibition and state anger. The right aI/IFG was the only ensuing cluster following response inhibition— state anger conjunction analyses. Results survived a cluster‐level p < .05 family‐wise error‐corrected for multiple comparisons, cluster‐forming threshold p < .001 at voxel level. aI, anterior insula; IFG, inferior frontal gyrus