Dissociable brain mechanisms for processing social exclusion and rule violation

Abstract

Social exclusion inherently involves an element of expectancy violation, in that we expect other people to follow the unwritten rule to include us in social interactions. In this functional magnetic resonance imaging (fMRI) study, we employed a unique modification of an interactive virtual ball-tossing game called "Cyberball" (Williams et al., 2000) and a novel paradigm called "Cybershape," in which rules are broken in the absence of social exclusion, to dissociate brain regions that process social exclusion from rule violations more generally. Our Cyberball game employed an alternating block design and removed evoked responses to events when the participant was throwing the ball in inclusion to make this condition comparable to exclusion, where participants did not throw. With these modifications, we replicated prior findings of ventral anterior cingulate cortex (vACC), insula, and posterior cingulate cortex activity evoked by social exclusion relative to inclusion. We also identified exclusion-evoked activity in the hippocampi, left ventrolateral prefrontal cortex, and left middle temporal gyrus. Comparing social exclusion and rule violation revealed a functional dissociation in the active neural systems as well as differential functional connectivity with vACC. Some overlap was observed in regions differentially modulated by social exclusion and rule violation, including the vACC and lateral parietal cortex. These overlapping brain regions showed different activation during social exclusion compared to rule violation, each relative to fair play. Comparing activation patterns to social exclusion and rule violation allowed for the dissociation of brain regions involved in the experience of exclusion versus expectancy violation.

Figure 1

Cyberball and Cybershape game screens. Above: Image of the game screen in Cyberball. The participant (bottom center glove) currently has the ball and can choose to throw the ball to either of the other players. Below: Image of the game screen in Cybershape. In this game the participant chose the red square as their shape. The participant currently has the ball in his/her glove, which is in the shape of a green diamond, indicating that the participant must throw to the player on the right with the matching green diamond next to his glove. When that player receives the green diamond it will change to a different shape (either a red square or a blue circle) dictating the next appropriate throw. Player pictures displayed in the figure were not used in the actual paradigm, as those pictures were not consented for publication.

Figure 2

Left column: whole-brain comparison of social exclusion and fair play. Regions in orange showed greater activation in social exclusion compared to fair play. Regions in blue showed greater activation in fair play compared to social exclusion (p < .05, cluster threshold of 35 contiguous voxels). Right Column: whole-brain comparison of rule violation and fair play. Regions in orange showed greater activation in rule violation compared to fair play. Regions in blue showed greater activation in fair play compared to rule violation (p < .05, cluster threshold of 35 contiguous voxels).

Figure 3

Between game comparison of differential activation in Cyberball and Cybershape, using a paired samples t-test of social exclusion – fair play and rule violation –fair play. Regions in orange showed greater activation in the Cyberball contrast (social exclusion – fair play), while regions in blue showed greater activation in the rule violation contrast (rule violation – fair play) (p < .01, cluster threshold of 9 contiguous voxels). All contrasts were performed after the removal of activation modeled from events when the participant was throwing the ball. Activations are displayed on a Talairach-transformed template brain in radiological orientation.

Figure 4

Structural Region of Interest (ROI) analysis of the vACC. A structural ROI (shown in purple) was used to compare vACC activity between the two games. Average contrast beta values for this ROI in each game were calculated for each participant using (social exclusion – fair play, rule violation – fair play). These average beta values are shown in the bar graph, with error bars depicting standard error.

Figure 5

PPI analysis of differential connectivity to vACC in Cyberball (left) and Cybershape (right). In both connectivity analyses the seed region used was functionally defined by greater activation in Cyberball social exclusion compared to fair play (3189 voxels, shown in green). In Cyberball (left), areas of activation in orange are regions that showed more functional connectivity to the seed region in social exclusion compared to fair play (p < .05, cluster threshold of 34 contiguous voxels). In Cybershape (right), areas of activation in orange are regions that showed more functional connectivity to the seed region in rule violation compared to fair play (p < .05, cluster threshold of 34 contiguous voxels). Activations are displayed on a Talairach-transformed template brain in radiological orientation.