Trait self-consciousness predicts amygdala activation and its functional brain connectivity during emotional suppression: an fMRI analysis

Abstract

The present functional magnetic resonance imaging study investigated how trait neuroticism and its heterogeneous subdimensions are related to the emotional consequences and neural underpinnings of emotion regulation. Two levels of neuroticism assessments were conducted with 47 female subjects, who were required to attend to, suppress emotion displays to, or cognitively reappraise the meanings of negative images. The results showed reduced emotional experience and bilateral amygdala activation during reappraisal, and this regulation effect is unaffected by individual differences in neuroticism and its subdimensions. By contrast, the emotion downregulation effect of suppression in the right amygdala is compromised with increasing self-consciousness but not overall neuroticism dimension. This association holds robust after controlling the potential contribution of habitual suppression. Moreover, the psychophysiological interaction (PPI) analysis revealed that self-consciousness predicts weaker functional coupling of the right amygdala to supplementary motor area and putamen during expressive suppression, two regions mediating the control and execution of motor actions. These findings suggest that self-consciousness predicts increased difficulty in emotional regulation using expressive suppression; and that the heterogeneous nature of trait neuroticism needs to be considered in exploring the association of neuroticism and emotion regulation.

Figure 1

Mean negative emotion ratings during emotion induction and regulation sessions. Error bars = SEM.

Figure 2

(a) Amygdala responses to negative stimuli. From the one-sample t-test across all 48 subjects for the contrast watch-negative > watch-neutral. The display threshold was FWE-corrected p < 0.001 with an extent of ten voxels. Peak of amygdala activation was centered at (t = 9.29, x = 27, y = −3, z = −18) in the right and (t = 10.98, x = −21, y = 0, z = −12) in the left. (b) Left amygdala responses during the instructed emotion regulation. (c) Right amygdala responses during the instructed emotion regulation. Error bars = SEM.

Figure 3

Scatterplot of self-consciousness and the emotion regulation effects of suppression (suppression-watching contrast) in the right amygdala (RA).

Figure 4

(a) The bar graph showing areas that exhibit significant task-dependent (Suppression vs. Watching contrast) coupling with the right amygdala: bilateral middle cingulum cortex (MCC), superior occipital cortex (SOC), lingual cortex, supplementary motor area (SMA), insula, putamen and rolandic operculum. (b) Partial correlations between self-consciousness and amygdala-SMA (left: r = −0.253, p = 0.049) and amygdala-putamen (right: r = −0.266, p = 0.041) PPI beta after isolating the effect of trait anxiety, depression and the habitual use of expressive suppression.