Human social motivation is characterized by the pursuit of social reward and the avoidance of social punishment. The ventral striatum/nucleus accumbens (VS/Nacc), in particular, has been implicated in the reward component of social motivation, i.e., the ‘wanting’ of social incentives like approval. However, it is unclear to what extent the VS/Nacc is involved in avoiding social punishment like disapproval, an intrinsically pleasant outcome. Thus, we conducted an event-related functional magnetic resonance imaging (fMRI) study using a social incentive delay task with dynamic video stimuli instead of static pictures as social incentives in order to examine participants' motivation for social reward gain and social punishment avoidance. As predicted, the anticipation of avoidable social punishment (i.e., disapproval) recruited the VS/Nacc in a manner that was similar to VS/Nacc activation observed during the anticipation of social reward gain (i.e., approval). Stronger VS/Nacc activity was accompanied by faster reaction times of the participants to obtain those desired outcomes. This data support the assumption that dynamic social incentives elicit robust VS/Nacc activity, which likely reflects motivation to obtain social reward and to avoid social punishment. Clinical implications regarding the involvement of the VS/Nacc in social motivation dysfunction in autism and social phobia are discussed.

The amygdala is central to the pathophysiology of many psychiatric illnesses. An imprecise understanding of how the amygdala fits into the larger network organization of the human brain, however, limits our ability to create models of dysfunction in individual patients to guide personalized treatment. Therefore, we investigated the position of the amygdala and its functional subdivisions within the network organization of the brain in 10 highly sampled individuals (5 h of fMRI data per person). We characterized three functional subdivisions within the amygdala of each individual. We discovered that one subdivision is preferentially correlated with the default mode network; a second is preferentially correlated with the dorsal attention and fronto-parietal networks; and third subdivision does not have any networks to which it is preferentially correlated relative to the other two subdivisions. All three subdivisions are positively correlated with ventral attention and somatomotor networks and negatively correlated with salience and cingulo-opercular networks. These observations were replicated in an independent group dataset of 120 individuals. We also found substantial across-subject variation in the distribution and magnitude of amygdala functional connectivity with the cerebral cortex that related to individual differences in the stereotactic locations both of amygdala subdivisions and of cortical functional brain networks. Finally, using lag analyses, we found consistent temporal ordering of fMRI signals in the cortex relative to amygdala subdivisions. Altogether, this work provides a detailed framework of amygdala–cortical interactions that can be used as a foundation for models relating aberrations in amygdala connectivity to psychiatric symptoms in individual patients.

Decisions to trust people with whom we have no personal history can be based on their social reputation-a product of what we can observe about them (their appearance, social group membership, etc.)-and our own beliefs. The striatum and amygdala have been identified as regions of the brain involved in trust decisions and trustworthiness estimation, respectively. However, it is unknown whether social reputation based on group membership modulates the involvement of these regions during trust decisions. To investigate this, we examined blood-oxygenation-level-dependent (BOLD) activity while participants completed a series of single-shot trust game interactions with real partners of varying races. At the time of choice, baseline BOLD responses in the striatum correlated with individuals' trust bias-that is, the overall disparity in decisions to trust Black versus White partners. BOLD signal in the striatum was higher when deciding to trust partners from the race group that the individual participant considered less trustworthy overall. In contrast, activation of the amygdala showed greater BOLD responses to Black versus White partners that scaled with the amount invested. These results suggest that the amygdala may represent emotionally relevant social group information as a subset of the general detection function it serves, whereas the striatum is involved in representing race-based reputations that shape trust decisions.

Given the spike in risky behaviors that accompanies adolescence, the need to examine the processes and contextual factors that influence disinhibition for adolescents is of great import. Using an emotionally salient cognitive control task, we examined how socially appetitive and aversive cues differentially affect behavioral inhibition across development. In Study 1 (N = 94, ages 8-30 years), we found that socially appetitive cues were particularly detrimental to inhibition, a finding driven by our adolescent sample. In Study 2 (N = 35, ages 12-17 years), we sought to explore the neural processes implicated in suboptimal inhibition during adolescence. Replicating our behavioral findings from Study 1, socially appetitive cues again caused detriments to inhibition compared with socially aversive cues. At the neural level, increased activation in affective regions (amygdala and ventral striatum) while viewing socially appetitive relative to socially aversive cues was correlated with increases in disinhibition. Furthermore, both whole-brain and functional connectivity analyses suggest recruitment of affective and social-detection networks (fusiform, bilateral temporoparietal junction) may account for the increased focus on appetitive relative to aversive cues. Together, our findings suggest that adolescents show detriments in inhibition to socially appetitive contexts, which is related to increased recruitment of affective and social processing neural regions.