Emotional reactivity to threat modulates activity in mentalizing network during aggression

Abstract

Aggression is a common response to provocation, albeit with considerable interindividual differences. In this fMRI study, we investigated emotional reactivity to threat as possible link between provocation and aggression, as well as the neural correlates of this relationship. We hypothesized that emotional reactivity, measured as fear potentiation (FP) of the startle response, would be negatively associated with aggressive behavior and would modulate neural activity during an aggressive interaction. In 30 healthy female participants, FP was measured as the difference between blink amplitudes while watching threatening vs neutral pictures. Participants subsequently engaged in a variant of the Taylor Aggression Paradigm (TAP), while being scanned. During the TAP, participants selected a punishment level for either a highly provoking or a nonprovoking opponent. There was no difference in aggressive behavior between participants high and low in FP. However, we found a negative correlation between FP and the neural provocation effect in several regions of a network previously associated with mentalizing including the medial prefrontal cortex, precuneus and the temporo-parietal junction. Independently of the FP variability, aggressive behavior correlated with the provocation effect on activity in the caudate nucleus. Our results indicate that during a provocative confrontation, high emotional reactivity to threat suppresses recruitment of the mentalizing network.

Keywords: aggression; empathy; fMRI; startle reaction; theory of mind.

Fig. 1

Paradigm. Figure shows the time course for one trial of the TAP.

Fig. 2

Behavioral results. Mean standardized startle amplitudes are given for neutral and threatening trials (A). (B) depicts mean noise level selected for the nonprovocative and highly provocative opponent. (C) Mean standardized RTs for the punishment selections for the nonprovocative and highly provocative opponent are given separately for participants low and high in behavioral provocation effect.

Fig. 3

Decision phase. Displayed is the region of interest defined for the correlation of provocation effect in the nucleus caudatus and the behavioral provocation effect (A); (B) shows the correlation map for the behavioral provocation effect and the high > low provocation contrast value for the bilateral caudate ROI.

Fig. 4

Regression analysis. Figure shows contrast images for the negatively weighted regression FP × high > low provocation for the decision phase (A; displayed at P < 0.001 uncorr., corresponding to q < 0.02 FDR corrected, clustering threshold 20 voxels). MFG = middle frontal gyrus; IFG = inferior frontal gyrus. (B) For visualization purposes, scatter diagrams are shown for the relationship between FP and high > low provocation contrast values averaged across the precuneus and TPJ clusters.

Fig. 5

ROI values. Shown are the contrast values for ROI derived from the regression FP × high > low provocation for the decision phase, displayed for high and low provocation in participants high and low in FP.

Fig. 6

Outcome phase. Figure shows the contrast images for win>lose (A; displayed at P < 0.001 uncorr., corresponding to q < 0.005 FDR corrected, clustering threshold 20 voxels) and lose > win (B; displayed at P < 0.001 uncorr., corresponding to q < 0.05 FDR corrected, clustering threshold 20 voxels).