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Meta-Analysis
. 2020 Aug 1;41(11):3147-3160.
doi: 10.1002/hbm.25004. Epub 2020 Apr 21.

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

Andrei A Puiu  1   2   3 , Olga Wudarczyk  3   4 , Gregor Kohls  1 , Danilo Bzdok  3   5   6   7   8 , Beate Herpertz-Dahlmann  9 , Kerstin Konrad  1   10
Affiliations
Meta-Analysis

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

Andrei A Puiu et al. Hum Brain Mapp. .

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.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

FIGURE 1
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
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
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
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