Integrative Processing of Touch and Affect in Social Perception: An fMRI Study

Abstract

Social perception commonly employs multiple sources of information. The present study aimed at investigating the integrative processing of affective social signals. Task-related and task-free functional magnetic resonance imaging was performed in 26 healthy adult participants during a social perception task concerning dynamic visual stimuli simultaneously depicting facial expressions of emotion and tactile sensations that could be either congruent or incongruent. Confounding effects due to affective valence, inhibitory top-down influences, cross-modal integration, and conflict processing were minimized. The results showed that the perception of congruent, compared to incongruent stimuli, elicited enhanced neural activity in a set of brain regions including left amygdala, bilateral posterior cingulate cortex (PCC), and left superior parietal cortex. These congruency effects did not differ as a function of emotion or sensation. A complementary task-related functional interaction analysis preliminarily suggested that amygdala activity depended on previous processing stages in fusiform gyrus and PCC. The findings provide support for the integrative processing of social information about others' feelings from manifold bodily sources (sensory-affective information) in amygdala and PCC. Given that the congruent stimuli were also judged as being more self-related and more familiar in terms of personal experience in an independent sample of participants, we speculate that such integrative processing might be mediated by the linking of external stimuli with self-experience. Finally, the prediction of task-related responses in amygdala by intrinsic functional connectivity between amygdala and PCC during a task-free state implies a neuro-functional basis for an individual predisposition for the integrative processing of social stimulus content.

Keywords: emotion; fMRI; facial expression; social perception; somatosensory; tactile sensation.

FIGURE 1

Visualization of the experimental stimuli and procedure.

FIGURE 2

Voxel clusters (thresholded at p < 0.05 corrected; k > 10) characterized by a significant interaction effect “facial expression × tactile sensation.” BOLD responses in these clusters were stronger during the congruent conditions, compared to the incongruent conditions. L: left; R: right; A: anterior; P: posterior.

FIGURE 3

Graphs showing average beta values and standard errors for the experimental conditions regarding voxels clusters characterized by a significant facial expression × tactile sensation interaction effect, and the absence of significant effects due tactile sensation or facial expression separately. Graphs on the left show beta values for the four conditions (CA-PL: caress-pleasure; HI-PA: hit-pain; CA-PA: caress-pain; HI-PL: hit-pleasure) indicating stronger responses for congruent compared to incongruent stimuli. Graphs on the right show average beta values for caress versus hit stimuli, and pleasure versus pain stimuli, illustrating the absence of differences between the observation of distinct tactile sensations or distinct facial expressions in these regions. ^∗, statistically significant difference p < 0.05.

FIGURE 4

Group statistical maps (F-statistics) showing voxels characterized by a significant effect of the facial expression factor (thresholded at p < 0.05 corrected; k > 10). L: left; R: right; A: anterior; P: posterior.

FIGURE 5

Group statistical maps (F-statistics) showing voxels characterized by a significant effect of the tactile sensation expression factor (thresholded at p < 0.05 corrected; k > 10). L: left; R: right; A: anterior; P: posterior.

FIGURE 6

Group statistical maps (conjunction thresholded at p < 0.05 corrected; k > 10) showing overlapping modulation by the observation of different tactile sensations as well as by different facial expressions. L: left; R: right; A: anterior; P: posterior.

FIGURE 7

Model of directional effects (indicating standardized path coefficients) between posterior cingulate cortex, fusiform gyrus, and amygdala obtained by SEM for the differentiation between congruent and incongruent stimuli, and a recapitulation of the task-related fMRI results concerning the encoding of socio-emotional stimulus congruence within the network.

FIGURE 8

Relationship (r = -0.58) between differential BOLD responses in left amygdala for congruent and incongruent stimuli, and its intrinsic functional connectivity with left dorsal posterior cingulate cortex (axes indicating natural log values).