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

Gabriela Gan,Rita Z Goldstein,Thomas Maloney,Nelly Alia-Klein,Joel L Steinberg,Muhammad A Parvaz,Scott J Moeller,Scott D Lane,Rebecca N Preston-Campbell

doi:10.3389/fnbeh.2016.00179

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.

Highlights

Reactive aggression (RA) is an approach-related impulsive response committed in anger-provoking or threatening social situations (Carver and Harmon-Jones, 2009; Blair, 2012)
Across all 4 runs, the 4 × 2 repeated-measures ANOVAs revealed that RA participants pressed significantly more buttons for the monetary reward than controls [main effect of group, F(1, 15) = 7.62, p = 0.015, partial η2 = 0.34], but the number of retaliatory button presses did not differ between groups [F(1, 15) = 0.15, p = 0.701, partial η2 = 0.01; Figure 2 right]
We demonstrate for the first time that an upregulation of the mesocorticolimbic salience system along with increased monetary reward-seeking behavior might play a role in clinical human RA, exemplified by the psychiatric condition of intermittent explosive disorder (IED) and high trait anger

Summary

Introduction

Reactive aggression (RA) is an approach-related impulsive response committed in anger-provoking or threatening social situations (Carver and Harmon-Jones, 2009; Blair, 2012). Neurobiological models suggest that RA in IED is mediated by a functional imbalance between prefrontal cortical “control” areas and mesolimbic “emotion” areas (Coccaro et al, 2007; Siever, 2008) In this model, there is increased reactivity of the bottom-up “drives” in mesolimbic regions including the amygdala and the insula to arousing emotional events, and impaired functioning of top-down “brakes” in regions including the anterior cingulate cortex (ACC), and the lateral and medial sections of the prefrontal cortex (PFC), areas implicated in anger regulation and impulse control (Davidson et al, 2000; Siever, 2008). This imbalance in the functioning of mesolimbicprefrontal circuits can manifest as a failure of integration of social cues and self-regulation (Heatherton and Wagner, 2011), precipitating disproportionate RA (Buckholtz and MeyerLindenberg, 2008; Siever, 2008; Coccaro, 2012)

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