Neural signatures underlying the effect of social structure on empathy and altruistic behaviors

Abstract

Humans inhabit complex social networks, monitoring social structures that encompass both direct and indirect relationships. However, previous research primarily focused on direct relationships, leaving the neural basis of how social structure influences socioemotional processes understudied. This study addressed this gap by investigating the neural pathways underlying the influence of social structure on empathy and altruistic behaviors. During fMRI scanning, participants viewed painful or non-painful stimulation to innocent strangers who shared preferences with targets who had either treated participants fairly or unfairly. Afterwards, participants rated the pain experienced by these innocents and shared money with other innocents. Participants showed reduced empathic and altruistic responses toward innocents resembling unfair (vs. fair) targets, accompanied by heightened activation in regions crucial for emotion regulation and mentalizing, such as the lateral and medial prefrontal cortex. Furthermore, whole-brain and local neural patterns in the anterior insula and premotor cortex robustly discriminated painful (but not non-painful) stimulation of different innocents, suggesting that social structure altered emotional and sensorimotor aspects of empathy. These alterations might be driven by top-down regulation, as indicated by heightened functional connectivity between the lateral prefrontal cortex and sensorimotor areas, as well as between the anterior insula and subgenual anterior cingulate cortex when witnessing the pain of innocents resembling fair (vs. unfair) targets. Together, our work is the first to uncover the neural underpinnings through which human empathy and altruistic behaviors are shaped by social structure beyond direct self-other relationships.