Social risk coding by amygdala activity and connectivity with dorsal anterior cingulate cortex.

Abstract

Risk is a fundamental factor affecting individual and social economic decisions, but its neural correlates are largely unexplored in the social domain. The amygdala, together with the dorsal anterior cingulate cortex (dACC), is thought to play a central role in risk taking. Here, we investigated in human volunteers (n=20; 11 females) how risk (defined as variance of reward probability distributions) in a social situation affects decisions and concomitant neural activity as measured with fMRI. We found separate variance-risk signals for social and non-social outcomes in the amygdala. Specifically, amygdala activity increased parametrically with social reward variance of presented choice options and on separate trials with non-social reward variance. Behaviorally, 75% of participants were averse to social risk as estimated in a Becker-DeGroot-Marschak auction-like procedure. The stronger this aversion, the more negative was the coupling between risk-related amygdala regions and dACC. This negative relation was significant for social risk attitude but not for the attitude towards variance-risk in juice outcomes. Our results indicate that the amygdala and its coupling with dACC process objective and subjectively evaluated social risk. Moreover, while social risk can be captured with a framework originally established by finance theory for non-social risk, the amygdala appears to processes social risk largely separately from non-social risk.Significance statement Risk-the uncertainty of outcomes-has profound effects on decision-making and behavior. In social situations, uncertainty about others' behavior ('social risk') similarly guides our decisions and can contribute to social anxiety. Surprisingly little is known about the neural mechanisms processing social risk. Here we investigated neural activity when humans evaluated social risk derived from the uncertainty of personal compliments received from social partners. Activity in the amygdala, a brain structure implicated in emotion and social behavior, reflected social risk levels. Amygdala functional connectivity to the anterior cingulate cortex reflected individuals' aversion to social risk. Our findings extend risk evaluation into the social domain and pave the way for investigating social risk attitude in mental-health impairments, including social anxiety.