Reward vs. Retaliation-the Role of the Mesocorticolimbic Salience Network in Human Reactive Aggression

Abstract

The propensity for reactive aggression (RA) which occurs in response to provocation has been linked to hyperresponsivity of the mesocorticolimbic reward network in healthy adults. Here, we aim to elucidate the role of the mesocorticolimbic network in clinically significant RA for two competing motivated behaviors, reward-seeking vs. retaliation. 18 male participants performed a variant of the Point-Subtraction Aggression Paradigm (PSAP) during functional magnetic resonance imaging (fMRI). We examined whether RA participants compared with non-aggressive controls would choose to obtain a monetary reward over the opportunity to retaliate against a fictitious opponent, who provoked the participant by randomly stealing money from his earnings. Across all fMRI-PSAP runs, RA individuals vs. controls chose to work harder to earn money but not to retaliate. When engaging in such reward-seeking behavior vs. retaliation in a single fMRI-PSAP run, RA individuals exhibited increased activation in the insular-striatal part of the mesocorticolimbic salience network, and decreased precuneus and ventromedial prefrontal cortex activation compared to controls. Enhanced overall reward-seeking behavior along with an up-regulation of the mesocorticolimbic salience network and a down-regulation of the default-mode network in RA individuals indicate that RA individuals are willing to work more for monetary reward than for retaliation when presented with a choice. Our findings may suggest that the use of positive reinforcement might represent an efficacious intervention approach for the potential reduction of retaliatory behavior in clinically significant RA.

Keywords: intermittent explosive disorder; mesocorticolimbic network; point-subtraction aggression paradigm; reactive aggression; reward; salience.

Figure 1

(A) In each fMRI-PSAP trial, participants could choose between increasing their earnings by $0.4 (option “A”) and retaliating by subtracting $1 from their opponent's earnings (option “B,” no monetary gain to participant). (B) Events and earnings/losses are displayed for each trial type. Each trial lasted for 18 s. Within a trial participants could not switch between the monetary and retaliatory option. However, they could complete multiple monetary (=50 button presses) or retaliatory ratios (=40 button presses) if they were fast enough. There was a 2-s interval between trials (Inter-trial-interval) in which a blank screen was presented.

Figure 2

Retaliatory and monetary reward-seeking responses displayed for reactive aggressive participants (RA) and controls for the single fMRI run for which brain responses have been analyzed (left), and mean responses across the four fMRI PSAP runs (right; responses were collapsed across runs as there was no effect of run and run x group interaction on behavioral responses). There were no significant differences between groups for the single fMRI run. Averaged across the four fMRI runs, RA individuals worked significantly more than controls to earn money, but not to retaliate. Abbreviations: fMRI, functional-magnetic resonance imaging; n.s., not significant; PSAP, Point-subtraction aggression paradigm. ^*p < 0.05.

Figure 3

Group effects on brain activity during sustained button pressing to gain money (reward) compared to achieving retaliation for a single fMRI-PSAP run (see Methods, fMRI preprocessing for reasons for including only one out of four fMRI-PSAP run into analysis). (A) RA individuals relative to controls exhibited increased activation within brain areas of the mesocorticolimbic salience network including the bilateral anterior insula and putamen, when working to obtain a reward vs. achieving retaliation (RA>controls; warm color scale). (B) RA individuals relative controls exhibited decreased activation within brain areas of the default-mode network, the bilateral vmPFC, and the Precuneus, when working to obtain a reward vs. achieving retaliation (RA<Controls, blue color scale). In the bar plots, the yellow upward pointing arrow indicates that brain responses were increased for reward vs. retaliation, and the blue downward pointing arrow indicates that brain responses were decreased for reward vs. retaliation. Whole-brain results are significant at a corrected cluster-threshold of p < 0.05 with at least 86 connected voxels (initial uncorrected height threshold: p < 0.005). Abbreviations: < 0.001, ^*p < 0.05, Ins, insula; L, Left; n.s., not significant; Precun, precuneus; Put, putamen; r, Spearman's correlation coefficient; R, Right; RA, reactive aggressive group; vmPFC, ventromedial PFC.

Figure 4

Whole-brain-behavior correlations: brain reactivity in the left ventral/dorsal striatum, and the left anterior prefrontal cortex (PFC) to reward vs. retaliation in the single fMRI run was positively correlated with reward-seeking behavior (i.e., monetary responses) across all fMRI runs, which was significantly increased in the RA group (warm color scale). The more pronounced the brain response to reward relative to retaliation within these mesocorticolimbic areas, the more increased the overall reward-seeking behavior. Whole-brain results are significant at a corrected cluster-threshold of p < 0.05 with at least 86 connected voxels (initial uncorrected height threshold: p < 0.005).