Amygdala–midbrain connectivity indicates a role for the mammalian parental care system in human altruism

Abstract

Costly altruism benefitting a stranger is a rare but evolutionarily conserved phenomenon. This behaviour may be supported by limbic and midbrain circuitry that supports mammalian caregiving. In rodents, reciprocal connections between the amygdala and the midbrain periaqueductal grey (PAG) are critical for generating protective responses toward vulnerable and distressed offspring. We used functional and structural magnetic resonance imaging to explore whether these regions play a role in supporting costly altruism in humans. We recruited a rare population of altruists, all of whom had donated a kidney to a stranger, and measured activity and functional connectivity of the amygdala and PAG as altruists and matched controls responded to care-eliciting scenarios. When these scenarios were coupled with pre-attentive distress cues, altruists' sympathy corresponded to greater activity in the left amygdala and PAG, and functional connectivity analyses revealed increased coupling between these regions in altruists during this epoch. We also found that altruists exhibited greater fractional anisotropy within the left amygdala–PAG white matter tract. These results, coupled with previous evidence of altruists' increased amygdala-linked sensitivity to distress, are consistent with costly altruism resulting from enhanced care-oriented responses to vulnerability and distress that are supported by recruitment of circuitry that supports mammalian parental care.