Empathy for social exclusion involves the sensory-discriminative component of pain: a within-subject fMRI study

Abstract

Recent research has shown that experiencing events that represent a significant threat to social bonds activates a network of brain areas associated with the sensory-discriminative aspects of pain. In the present study, we investigated whether the same brain areas are involved when witnessing social exclusion threats experienced by others. Using a within-subject design, we show that an ecologically valid experience of social exclusion recruits areas coding the somatosensory components of physical pain (posterior insular cortex and secondary somatosensory cortex). Furthermore, we show that this pattern of activation not only holds for directly experienced social pain, but also during empathy for social pain. Finally, we report that subgenual cingulate cortex is the only brain area conjointly active during empathy for physical and social pain. This supports recent theories that affective processing and homeostatic regulation are at the core of empathic responses.

Keywords: empathy; fMRI; physical pain; social exclusion; somatosensory cortex.

Fig. 1

fMRI design for the physical pain task. In each trial, participants were first presented with colored arrows as cues indicating the target, either the participant (self) or the confederate (other) and the intensity (painful or non-painful) of the incoming stimulation. Specifically, dark colors indicated a painful stimulus, whereas light colors were paired with non-painful stimuli (in the figure only dark-colored cues are shown). The actual delivery of the stimulus was signaled by a dot of the same color of the arrow, appearing after 2500 ms. Participants judged their own emotion on a 9-points Likert scale, displayed for 4000 ms, immediately after the stimulation period (1000 ms). Interstimulus interval was randomly jittered (1000–3000 ms).

Fig. 2

fMRI design for the social pain task. During each trial, participants could receive (or observe receiving for the ‘other’ condition) the ball from the other two players and decide to whom to throw the ball by pressing the left or the right key on the pad. Each round ended after 12 throws of the ball. Immediately after, they were asked to judge their own emotion on a 9-points Likert scale, displayed for 4000 ms. Interstimulus interval was randomly jittered (1000–3000 ms). On the right, the number of passes received by the player (either the participant or the confederate) in each of the 10 rounds is indicated. Inclusion rounds are depicted in white, exclusion rounds in gray.

Fig. 3

Emotional ratings for the physical pain (A) and social pain (B) tasks. Graphs represent means and standard errors.

Fig. 4

Top part: neural activations for the first person experience of physical pain (contrast: self (pain > no-pain)). Bottom part: neural activations for the first person experience of social exclusion (contrast: self (exclusion > inclusion)). Statistical maps are superimposed on a standard inflated surface (medial and lateral views are showed for each hemisphere). Maps are thresholded at P < 0.005 uncorrected, for illustrative purposes.

Fig. 5

Top part: neural activations for empathy for physical pain (contrast: self ⋂ other (pain > no-pain)). Bottom part: neural activations for empathy for social exclusion (contrast: Self ⋂ Other (exclusion > inclusion)). Statistical maps are superimposed on a standard inflated surface (medial and lateral views are showed for each hemisphere). Maps are thresholded at P < 0.005 uncorrected, for illustrative purposes.

Fig. 6

Top part: common neural activations for physical and social pain (contrast: self (pain > no-pain) ⋂ self (exclusion > inclusion)). Bottom part: common neural activations for empathy for physical and social pain (contrast: self (main effect pain > no-pain and exclusion > inclusion) ⋂ other (main effect pain > no-pain and exclusion > inclusion)). Statistical maps are superimposed on a standard inflated surface (medial and lateral views are showed for each hemisphere). Maps are thresholded at P < 0.005 uncorrected, for illustrative purposes.

Fig. 7

Difference in neural activation between physical and social pain for the empathy condition. Top part: brain areas more active during the witnessing of the other person suffering from physical pain than from social pain (contrast: other (pain > no-pain) > other (exclusion > inclusion)). Bottom part: brain areas more active during the witnessing of the other person suffering from social pain than from physical pain (contrast: other (exclusion > inclusion) > other (pain > no-pain)). Statistical maps are superimposed on a standard inflated surface (medial and lateral views are showed for each hemisphere). Maps are thresholded at P < 0.005 uncorrected, for illustrative purposes.