Humans exhibit considerable variation in how they value their own interest relative to the interests of others. Deciphering the neural codes representing potential rewards for self and others is crucial for understanding social decision-making. Here we integrate computational modeling with fMRI to investigate the neural representation of social value and the modulation by oxytocin, a nine-amino acid neuropeptide, in participants evaluating monetary allocations to self and other (self-other allocations). We found that an individual's preferred self-other allocation serves as a reference-point for computing the value of potential self-other allocations. In more-prosocial participants, amygdala activity encoded a social-value-distance signal, i.e. the value dissimilarity between potential and preferred allocations. Intranasal oxytocin administration amplified this amygdala representation and increased prosocial behavior in more-individualist participants but not in more-prosocial ones. Our results reveal a neurocomputational mechanism underlying social-value representations and suggest that oxytocin may promote prosociality by modulating social-value representations in the amygdala.

The hypothalamic peptide oxytocin (OT) is crucial in social adaptation and used to treat emotional and social deficits. Here, we conducted a systematic, quantitative meta-analysis of functional-MRI studies intranasally administering OT (IN-OT) to uncover neural substrates underlying the IN-OT effects and to elucidate differential IN-OT effects between healthy and clinical populations. Meta-analyses were conducted on 66 IN-OT fMRI studies, stratified by psychopathology, valence and sex. IN-OT increased bilateral amygdala, caudate head, and superior temporal activity in healthy individuals and increased dorsal anterior cingulate activity in patients. Moreover, IN-OT decreased amygdala activity in both patients and healthy individuals but did so to a greater degree in patients than healthy individuals. The OT-increased amygdala activity was only found on the negative social and affective processes, whereas the OT-decreased amygdala activity was mainly contributed by contrasts on negative-valenced processes. IN-OT increased parahippocampal activity and decreased amygdala activity during negative socio-affective processing. During positive socio-affective processes, IN-OT increased caudate head activity. This study indicates convergent neural substrates and the underlying neuropsychological mechanisms for IN-OT effects on social and affective processes. The common and different effects of IN-OT on patients and healthy individuals and the modulation of OT effects by valence have critical implications.

Humans update their beliefs upon feedback and, accordingly, modify their behaviors to adapt to the complex, changing social environment. However, people tend to incorporate desirable (better than expected) feedback into their beliefs but to discount undesirable (worse than expected) feedback. Such optimistic updating has evolved as an advantageous mechanism for social adaptation. Here, we examine the role of oxytocin (OT)-an evolutionary ancient neuropeptide pivotal for social adaptation-in belief updating upon desirable and undesirable feedback in three studies (n = 320). Using a double-blind, placebo-controlled between-subjects design, we show that intranasally administered OT (IN-OT) augments optimistic belief updating by facilitating updates of desirable feedback but impairing updates of undesirable feedback. The IN-OT-induced impairment in belief updating upon undesirable feedback is more salient in individuals with high, rather than with low, depression or anxiety traits. IN-OT selectively enhances learning rate (the strength of association between estimation error and subsequent update) of desirable feedback. IN-OT also increases participants' confidence in their estimates after receiving desirable but not undesirable feedback, and the OT effect on confidence updating upon desirable feedback mediates the effect of IN-OT on optimistic belief updating. Our findings reveal distinct functional roles of OT in updating the first-order estimation and second-order confidence judgment in response to desirable and undesirable feedback, suggesting a molecular substrate for optimistic belief updating.oxytocin | social adaptation | confidence | belief updating | optimism