Mature amygdala-prefrontal circuitry regulates affect in adulthood, but shows protracted development. In (semi-)altricial species, caregivers provide potent affect regulation when mature neurocircuitry is absent. This investigation examined a potential mechanism through which caregivers provide regulatory influences in childhood. Children, but not adolescents, showed evidence of maternal buffering, such that maternal stimuli suppressed amygdala reactivity. In the absence of maternal stimuli, children exhibited immature amygdala-prefrontal connectivity. However, in the presence of maternal stimuli, children displayed mature-like connectivity that resembled adolescents’ connectivity. Children showed improved affect-related regulation in the presence of their mother. Individual differences emerged, with maternal influence on amygdalaprefrontal circuitry associated with stronger mother-child relationships and maternal modulation of behavioral regulation. These findings suggest a neural mechanism through which caregivers modulate children's regulatory behavior by inducing mature-like connectivity and buffering against heightened reactivity. Maternal buffering in childhood, but not adolescence, suggests that childhood may be a sensitive period for amygdala-prefrontal development.

Decisions to engage in collaborative interactions require enduring considerable risk, yet provide the foundation for building and maintaining relationships. Here, we investigate the mechanisms underlying this process and test a computational model of social value to predict collaborative decision making. Twenty-six participants played an iterated trust game and chose to invest more frequently with their friends compared with a confederate or computer despite equal reinforcement rates. This behavior was predicted by our model, which posits that people receive a social value reward signal from reciprocation of collaborative decisions conditional on the closeness of the relationship. This social value signal was associated with increased activity in the ventral striatum and medial prefrontal cortex, which significantly predicted the reward parameters from the social value model. Therefore, we demonstrate that the computation of social value drives collaborative behavior in repeated interactions and provide a mechanistic account of reward circuit function instantiating this process.

Everyday goals and experiences are often shared with others who may hold different places within our social networks. We investigated whether the experience of sharing a reward differs with respect to social network. Twenty human participants played a card guessing game for shared monetary outcomes with three partners: a computer, a confederate (out-of-network), and a friend (in-network). Participants subjectively rated the experience of sharing a reward more positively with their friend than the other partners. Neuroimaging results support participants’ subjective reports, as ventral striatal BOLD responses were more robust when sharing monetary gains with a friend, as compared to with the confederate or computer, suggesting a higher value for sharing with an in-network partner. Interestingly, ratings of social closeness co-varied with this activity, resulting in a significant partner × closeness interaction: exploratory analysis showed that only participants reporting higher levels of closeness demonstrated partner-related differences in striatal BOLD response. These results suggest that reward valuation in social contexts is sensitive to distinctions of social network, such that sharing positive experiences with in-network others may carry higher value.

The human striatum is integral for reward-processing and supports learning by linking experienced outcomes with prior expectations. Recent endeavors implicate the striatum in processing outcomes of social interactions, such as social approval/rejection, as well as in learning reputations of others. Interestingly, social impressions often influence our behavior with others during interactions. Information about an interaction partner’s moral character acquired from biographical information hinders updating of expectations after interactions via top down modulation of reward circuitry. An outstanding question is whether initial impressions formed through experience similarly modulate the ability to update social impressions at the behavioral and neural level. We investigated the role of experienced social information on trust behavior and reward-related BOLD activity. Participants played a computerized ball-tossing game with three fictional partners manipulated to be perceived as good, bad, or neutral. Participants then played an iterated trust game as investors with these same partners while undergoing fMRI. Unbeknownst to participants, partner behavior in the trust game was random and unrelated to their ball-tossing behavior. Participants’ trust decisions were influenced by their prior experience in the ball-tossing game, investing less often with the bad partner compared to the good and neutral. Reinforcement learning models revealed that participants were more sensitive to updating their beliefs about good and bad partners when experiencing outcomes consistent with initial experience. Increased striatal and anterior cingulate BOLD activity for positive versus negative trust game outcomes emerged, which further correlated with model-derived prediction error learning signals. These results suggest that initial impressions formed from direct social experience can be continually shaped by consistent information through reward learning mechanisms.

Early institutional care can be profoundly stressful for the human infant, and, as such, can lead to significant alterations in brain development. In animal models, similar variants of early adversity have been shown to modify amygdala-hippocampal-prefrontal cortex development and associated aversive learning. The current study examined this rearing aberration in human development. Eighty-nine children and adolescents who were either previously institutionalized (PI youth; N ϭ 46; 33 females and 13 males; age range, 7-16 years) or were raised by their biological parents from birth (N ϭ 43; 22 females and 21 males; age range, 7-16 years) completed an aversive-learning paradigm while undergoing functional neuroimaging, wherein visual cues were paired with either an aversive sound (CSϩ) or no sound (CSϪ). For the PI youth, better aversive learning was associated with higher concurrent trait anxiety. Both groups showed robust learning and amygdala activation for CSϩ versus CSϪ trials. However, PI youth also exhibited broader recruitment of several regions and increased hippocampal connectivity with prefrontal cortex. Stronger connectivity between the hippocampus and ventromedial PFC predicted significant improvements in future anxiety (measured 2 years later), and this was particularly true within the PI group. These results suggest that for humans as well as for other species, early adversity alters the neurobiology of aversive learning by engaging a broader prefrontal-subcortical circuit than same-aged peers. These differences are interpreted as ontogenetic adaptations and potential sources of resilience.