Evidence for lateralized functional connectivity patterns at rest related to the tendency of externalizing or internalizing anger

Abstract

Previous electroencephalographic and brain stimulation studies have shown that anger responses may be differently lateralized in the prefrontal cortex, with outward-oriented responses (externalized anger) linked to left prefrontal activity, and inward-oriented responses (internalized anger) linked to right prefrontal activity. However, the specific neural structures involved in this asymmetry, and how they interact to produce individual differences, remain unexplored. Furthermore, it is unclear whether such asymmetry may be explained by general behavioral tendencies, known as Behavioral Activation and Behavioral Inhibition Systems (BIS/BAS). Therefore, we analyzed the tendency of externalizing and internalizing anger, respectively measured by the Anger-Out and Anger-In subscales of the State-Trait Anger Expression Inventory, with the patterns of functional connectivity at rest of 71 participants. A left, prefrontal, resting-state, functional connectivity pattern was found for externalizing anger (Anger-Out), including the left inferior frontal gyrus and the left frontal eye fields. By contrast, a right, prefrontal, resting-state, functional connectivity pattern was found for internalizing anger (Anger-In), including the rostral and lateral prefrontal cortex, the orbitofrontal cortex, the frontal pole, the superior, middle and inferior frontal gyri, and the anterior cingulate. Notably, these patterns were not associated with the BIS/BAS scores. In this study, for the first time, we provide evidence using fMRI functional connectivity for two specific lateralized circuits contributing to individual differences in externalizing and internalizing anger. These results confirm and extend the asymmetry hypothesis for anger and have notable implications in the treatment of anger-related problems.

Individual differences in the expression and control of anger are encoded in the same fronto-temporal GM-WM network

“…The involvement in the anterior cingulate in rumination and internalization of anger may appear contradictory to our findings, which show a positive association between the cingulate and externalization. However, in our study, the cingulate area was more centrally located and posterior compared to the anterior cingulate observed in previous studies on rumination and internalization (Denson et al 2009; Consolini et al 2022).…”

“…Another important region in our study was the Cingulate cortex. The cingulate, especially the anterior part, as well as the medial prefrontal area, have been associated to angry rumination (Denson et al 2009), which characterizes the internalization of anger (Consolini et al 2022). Indeed, in one study, authors found that after the presentation of angry faces, the negative connectivity of the ventral anterior cingulate cortex with the amygdala was reduced in individuals with high appetitive motivation (associated with aggression) (Passamonti et al 2008).…”

“…Another important region in our study was the Cingulate cortex. The cingulate, especially the anterior part, as well as the medial prefrontal area, have been associated to angry rumination (Denson et al 2009), which characterizes the internalization of anger (Consolini et al 2022).…”

“…Additionally, trait impulsivity that may be related with externalizing anger, was linked to prefrontal, temporal, and parietal cortices (Pan N., Wang S., 2021). From a structural point of view, a recent study used supervised machine learning to identify grey matter features related to the individual differences in externalizing anger (Consolini et al, 2022) revealing that the medial, lateral, and orbito-frontal regions, the temporal and parietal regions (temporal poles, insula, fusiform and angular gyrus, posterior cingulate), the basal ganglia, and parts of the cerebellum were found to be involved in the structural network that predicted anger externalisation.…”