Enhanced bodily states of fear facilitates bias perception of fearful faces

Abstract

We investigated whether enhanced interoceptive bodily states of fear would facilitate recognition of the fearful faces. Participants performed an emotional judgment task after a bodily imagery task inside a functional magnetic resonance imaging scanner. In the bodily imagery task, participants were instructed to imagine feeling the bodily sensations of two specific somatotopic patterns: a fear-associated bodily sensation (FBS) or a disgust-associated bodily sensation (DBS). They were shown faces expressing various levels of fearfulness and disgust and instructed to classify the facial expression as fear or disgust. We found a stronger bias favoring the "fearful face" under the congruent FBS condition than under the incongruent DBS condition. The brain response to fearful versus intermediate faces increased in the fronto-insular-temporal network under the FBS condition, but not the DBS condition. The fearful face elicited activity in the anterior cingulate cortex and extrastriate body area under the FBS condition relative to the DBS condition. Furthermore, functional connectivity between the anterior cingulate cortex/extrastriate body area and the fronto-insular-temporal network was modulated according to the specific bodily sensation. Our findings suggest that somatotopic patterns of bodily sensation provide informative access to the collective visceral state in the fear processing via the fronto-insular-temporal network.

Keywords: Anterior cingulate cortex; Emotional face; Extrastriate body area; Fear; Interoception.

Fig. 1

Experimental procedure during fMRI scanning. Inside the fMRI scanner, the bodily imagery task required participants to view a somatotopic map that flickered twice during an 8-s period with a 4-s cycle. Participants were instructed to imagine the bodily sensation depicted by the somatotopic pattern. The somatotopic maps were representative sensation maps for fear or disgust generated by averaging the sensation patterns recorded in subjects after watching video clips containing fearful or disgusting stimuli in our previous study. After the bodily imagery task, a face with a morphed facial expression between fear and disgust appeared for 2 s. In this two-alternative forced-choice task, participants were given 4 s to classify the expression as fearful or disgusted

Fig. 2

Self-reported bodily sensations according to intensity and spatial pattern and percentage of decisions favoring fearful face under congruent bodily sensation pattern. a Fear/disgust-associated bodily sensation (intensity). The intensity of the bodily sensations did not significantly differ between the conditions (t = 1.16, p = 0.264). The statistical parametric maps of bodily sensations induced in the bodily imagery task under each condition were visualized on a body template (FBS on the left side and DBS on the right side). b Fear/disgust-associated bodily sensation (spatial patterns). The location of each self-reported bodily sensation was well matched with the patterns presented in the bodily imagery task. c Emotional judgment task. The group-level classification ratio for each morphed face under the FBS (red) and DBS (blue) conditions. The psychometric curves fitted to the classification results are shown in the corresponding colors. The two-way repeated-measures ANOVA revealed a main effect of somatotopic pattern on the classification pattern of the emotional faces (F [1, 16] = 5.191; p = 0.0242). Tukey’s HSD post hoc analyses indicated that the emotional recognition bias favoring the “fearful face” was more pronounced under the FBS condition than under the DBS condition

Fig. 3

Brain responses to emotional faces according to somatotopic information (FBS and DBS). A: BOLD response to emotional face after bodily imagery task. Brain activity in response to the fearful face (fearful face > intermediate face) under the FBS condition was found in the bilateral regions of the anterior insula and dorsolateral prefrontal and inferior frontal cortices and in the right posterior insula, secondary somatosensory cortex, middle temporal gyrus (extrastriate body area), and middle occipital gyrus (p < 0.05; cluster-wise corrected). In contrast, the fearful face did not evoke significant brain activity under the DBS condition. Moreover, the disgusted face did not evoke a significant brain response (disgusted face > intermediate face) under the FBS or DBS condition. a Beta estimates for insula and amygdala (ROIs). b The ROI analysis of the bilateral amygdala and insula revealed that the FBS condition enhanced the brain response to fearful faces

Fig. 4

a Brain responses to the fearful face according to somatotopic condition. Comparison of the brain response to the fearful face under the FBS and DBS conditions revealed enhanced activity in the bilateral regions of the anterior cingulate cortex (ACC, Brodmann area 32) and the right region of middle temporal gyrus (Brodmann area 37) under the FBS condition (p < 0.05; cluster-wise corrected). b Functional connectivity of the anterior cingulate cortex (ACC) and extrastriate body area (EBA) according to somatotopic condition. The ACC and EBA, which encode different bodily sensations, were used as seed regions in the functional connectivity analysis. The dorsolateral prefrontal cortex (dlPFC), insula, operculum, fusiform gyrus, cerebellum, and extrastriate cortex (V4) showed somatotopic pattern-dependent connectivity modulation with the ACC (top). The amygdala (basolateral amygdala; BLA), insula, dlPFC, supramarginal gyrus, and left MTG showed somatotopic pattern-dependent connectivity modulation with the right EBA (p < 0.05; cluster-wise corrected, bottom)