Neural pathways of embarrassment and their modulation by social anxiety

Abstract

While being in the center of attention and exposed to other's evaluations humans are prone to experience embarrassment. To characterize the neural underpinnings of such aversive moments, we induced genuine experiences of embarrassment during person-group interactions in a functional neuroimaging study. Using a mock-up scenario with three confederates, we examined how the presence of an audience affected physiological and neural responses and the reported emotional experiences of failures and achievements. The results indicated that publicity induced activations in mentalizing areas and failures led to activations in arousal processing systems. Mentalizing activity as well as attention towards the audience were increased in socially anxious participants. The converging integration of information from mentalizing areas and arousal processing systems within the ventral anterior insula and amygdala forms the neural pathways of embarrassment. Targeting these neural markers of embarrassment in the (para-)limbic system provides new perspectives for developing treatment strategies for social anxiety disorders.

Keywords: Embarrassment; Limbic system; Mentalizing; Publicity; Social anxiety; Social immersion.

Figure 1

Experimental set-up and design. A Set-up of the fMRI experiment. During the pre-scanning phase (upper picture), the participant (red clothes) and the three confederates practice the cognitive estimation task while sitting in front of their notebooks in the preparation room adjacent to the scanner room. During scanning (lower picture), the participant lies in the MRI believing that the three confederates are completing the same task in the preparation room and are able to follow his/her performance on their notebook screens via cable connections. B Timing of the fMRI paradigm. Estimation questions are presented for 10 s followed by a fixation cross presented for 1.5 s and the feedback presented for 8 s. After an intertrial interval of 5 s, the next trial starts. C Design of the fMRI paradigm. There are six different conditions resulting from the PERFORMANCE (3) x PUBLICITY (2) levels. PERFORMANCE is either LOW, mediocre (NEUTRAL) or HIGH and is indicated by a line marking the exact percent value of the relative estimation performance (red frames). Half of the feedback is made PUBLIC and visible to the audience (green frames) and the other half is PRIVATE and only visible to the participant him- or herself (gray frames). For further details see also Movie A. 1.

Figure 2

FMRI results. A Pupil dilation as indicator of arousal. Increased activation of the ventral anterior insula (vAI) associated with increases in pupil dilation during individual feedback trials across all conditions (p < .05, whole-brain corrected). For further details see also Table A.4. B Audience effect. Increased activation of the medial prefrontal cortex (mPFC) and precuneus during public (PUB) compared to private (PRIV) performance averaged across PERFORMANCE levels was associated with mentalizing processes when thinking about others’ evaluations (p < .05, whole-brain corrected, see also Table A. 2) C Performance effect. Increased activation of the dorsal anterior insula (dAI) during LOW and HIGH compared to mediocre (NEUT) performance indicating increased processing of affective arousal (conjunction analysis LOW-NEUT∩HIGH-NEUT, p < .05, whole-brain corrected). For further results see also Fig. A.1 and Table A.1. D Increased functional connectivity during embarrassment. Psychophysiological interaction analyses revealed increased functional connectivity during LOW compared to HIGH performance (p < .05 uncorrected for display purposes, results survive correction within our amygdala and vAI search volumes). Seed regions are based on the arousal (left and right dAIs; results presented in red, for seed regions see Fig. 2c) and mentalizing (precuneus and mPFC; results presented in green, for seed regions see Fig. 2b) networks. Overlap is presented in yellow. Dashed lines illustrate the anatomically defined search volumes including the amygdalae (AAL; Tzourio-Mazoyer et al., 2002) and the functional vAI (Kelly et al., 2012).

Figure 3

Modulatory effects of social anxiety and self-reported embarrassment. β-values result from robust regression analyses using Huber’s M-estimators presented with one-tailed p-values. A Scatter plots of trait social anxiety and PUBLICITY effects for gaze dwell times and activation data. There was a positive correlation between social anxiety (mean SIAS scores) and differences in dwell time on the confederates’ faces between the public and private conditions (top). Participants with higher social anxiety scores also showed increased activation within the right fusiform face area (FFA, middle) and the mPFC (bottom) during PUB-PRIV (averaged parameter estimates within the FFA and mPFC clusters from the PUBLICITY effect, Fig. 2b). B Scatter plots of self-reports of embarrassment and PUBLICITY effects for gaze and activation data. The upper part shows a positive correlation between self-reports of embarrassment during LOW_PUB feedback and differences in dwell time of gaze on the confederates’ faces between the public and private conditions. Participants who reported experiencing stronger embarrassment during LOW_PUB feedback also showed increased activation within the right fusiform face area (FFA, middle) and the precuneus (bottom) during PUB-PRIV feedback.