Empathy for the social suffering of friends and strangers recruits distinct patterns of brain activation

Abstract

Humans observe various peoples' social suffering throughout their lives, but it is unknown whether the same brain mechanisms respond to people we are close to and strangers' social suffering. To address this question, we had participant's complete functional magnetic resonance imaging (fMRI) while observing a friend and stranger experience social exclusion. Observing a friend's exclusion activated affective pain regions associated with the direct (i.e. firsthand) experience of exclusion [dorsal anterior cingulate cortex (dACC) and insula], and this activation correlated with self-reported self-other overlap with the friend. Alternatively, observing a stranger's exclusion activated regions associated with thinking about the traits, mental states and intentions of others ['mentalizing'; dorsal medial prefrontal cortex (DMPFC), precuneus, and temporal pole]. Comparing activation from observing friend's vs stranger's exclusion showed increased activation in brain regions associated with the firsthand experience of exclusion (dACC and anterior insula) and with thinking about the self [medial prefrontal cortex (MPFC)]. Finally, functional connectivity analyses demonstrated that MPFC and affective pain regions activated in concert during empathy for friends, but not strangers. These results suggest empathy for friends' social suffering relies on emotion sharing and self-processing mechanisms, whereas empathy for strangers' social suffering may rely more heavily on mentalizing systems.

Fig. 1

Pictorial representation of Cyberball task for observing a (A) stranger’s Cyberball game and (B) friend’s Cyberball game. Actual Cyberball games were video recordings, not static images.

Fig. 2

Main effects of observing a friend and stranger’s social exclusion. Regions associated with empathizing for a friend and stranger’s social exclusion. T-values are represented by the intensity of the activation, with lighter activations representing larger t-values. Coordinates shown demonstrate the extent of activation for friend: dACC: 11 24 33; Insula: −40 0 16; MPFC: −6 45 0 and stranger: DMPFC: −16 35 36; precuneus: −1 −46 36; TP: −50 −6 −26.

Fig. 3

Brain regions during a friend’s exclusion predicted by self-other overlap scores. (A) Affective pain regions (coordinates shown demonstrate the extent of activation for dACC: 4 18 27 and anterior insula: 42 6 −3) observed in the contrast regressing self-other overlap scores with the friend’s exclusion contrast. T-values are represented by the intensity of the activation, with lighter activations representing larger t-values. (B) Mean parameter estimates of most significant voxels (sphere centered around peak voxel with 3 mm extent) in these regions are plotted on the y-axis of the graphs and self-other overlap scores are plotted on the x-axis.

Fig. 4

Brain regions significantly active in the interaction contrast comparing a friend’s exclusion > inclusion to a stranger’s exclusion > inclusion. (A) Brain activations during the observation of a friend compared to stranger’s social exclusion. Coordinates shown demonstrate the extent of activation for MPFC: −10 63 3; dACC: 12 22 34; and Insula: 33 5 14. T-values are represented by the intensity of the activation, with lighter activations representing larger t-values. (B) Mean parameter estimates of most significant voxels (sphere centered around peak voxel with 3 mm extent) in the dACC, insula and MPFC.

Fig. 5

Brain regions showing functional connectivity with MPFC for the friend’s exclusion and the friend’s exclusion compared to stranger’s exclusion. (A) Affective pain regions (Coordinates shown demonstrate the extent of activation for dACC: 5 18 26; bilateral anterior insula: L −38 17 0; R 40 14 0) that showed increased functional connectivity with the MPFC during observation of a friend’s exclusion. T-values are represented by the intensity of the activation, with lighter activations representing larger t-values. (B) Comparing the functional connectivity activation with the MPFC seed for the friend’s exclusion and the stranger’s exclusion showed significantly more connectivity with the dACC (coordinate showing extent of activation: 7 17 26) and anterior insula (coordinate showing extent of activation: L −36 1 31) for the friend’s exclusion relative to the stranger’s exclusion.