Emotion and personal space: Neural correlates of approach-avoidance tendencies to different facial expressions as a function of coldhearted psychopathic traits

Abstract

In social interactions, humans are expected to regulate interpersonal distance in response to the emotion displayed by others. Yet, the neural mechanisms implicated in approach-avoidance tendencies to distinct emotional expressions have not been fully described. Here, we investigated the neural systems implicated in regulating the distance to different emotions, and how they vary as a function of empathy. Twenty-three healthy participants assessed for psychopathic traits underwent fMRI scanning while they viewed approaching and withdrawing angry, fearful, happy, sad and neutral faces. Participants were also asked to set the distance to those faces on a computer screen, and to adjust the physical distance from the experimenter outside the scanner. Participants kept the greatest distances from angry faces, and shortest from happy expressions. This was accompanied by increased activation in the dorsomedial prefrontal and orbitofrontal cortices, inferior frontal gyrus, and temporoparietal junction for angry and happy expressions relative to the other emotions. Irrespective of emotion, longer distances were kept from approaching faces, which was associated with increased activation in the amygdala and insula, as well as parietal and prefrontal regions. Amygdala activation was positively correlated with greater preferred distances to angry, fearful and sad expressions. Moreover, participants scoring higher on coldhearted psychopathic traits (lower empathy) showed reduced amygdala activation to sad expressions. These findings elucidate the neural mechanisms underlying social approach-avoidance, and how they are related to variations in empathy. Hum Brain Mapp 38:1492-1506, 2017. © 2016 Wiley Periodicals, Inc.

Keywords: empathy; fMRI; facial expressions; interpersonal distance; psychopathic traits.

Figure 1

Schematic representation of the experimental tasks: imaging task (A), computerized interpersonal distance task (B) and “Stop‐distance” task (C). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Mean distances set to each emotional expression in the computerized task (A), and mean discomfort ratings during the scanning task (B). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Clusters showing a main effect of Direction in the 5 × 2 ANOVA, including the bilateral visual cortex, fusiform gyrus, right inferior (IPL) and superior parietal lobules (SPL), right amygdala, bilateral anterior insula (AI) and bilateral dorsolateral prefrontal cortex (dlPFC; FDR‐corrected P < 0.05). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

(A) Clusters showing a main effect of emotion in the 5 × 2 ANOVA, including the bilateral IFG right OFC, left IPL and left dorsomedial prefrontal cortex (dmPFC; FDR‐corrected P < 0.05). (B) Graphs depicting the percent signal change per facial expression in clusters showing a main effect of emotion (left dmPFC, right OFC, right IFG and right IPL). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 5

(A) Clusters showing a direction × emotion interaction in the 5 × 2 ANOVA, including the left IFG, right ventrolateral prefrontal cortex (vlPFC), left mid‐insula (MI) and right anterior insula (AI; FDR‐corrected P < 0.05). (B) Graphs depicting the percent signal change per facial expression and direction in clusters showing a significant interaction (left IFG, right vlPFC left MI and right AI) (*P < 0.05, ** P < 0.01, *** P < 0.001). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 6

Scatter plots depicting the association between right amygdala activation (24, 0, −14) and distance set to angry (top left), sad (top right) and fearful expressions (bottom left); scatter plot depicting the association between right amygdala activation to sad faces and Coldheartedness scores (bottom right). [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 7

Scatter plot depicting the association between activation to sad faces in the right amygdala ROI and Coldheartedness (FWE‐corrected P < 0.05). [Color figure can be viewed at http://wileyonlinelibrary.com]