Neural mechanisms of social decision-making in the primate amygdala

Abstract

Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions.amygdala | social decision | value mirroring | oxytocin | hierarchical modeling H ow we treat others impacts not only their well-being but our own. Human society depends on cooperation, charity, and altruism, as well as institutions to regulate selfish biases. In humans, these behaviors involve perspective-taking, empathy, and theory of mind (1, 2), and the rudiments of these capacities appear to mediate complex social behavior in animals (3). Recent research has sketched a rough outline of the neural circuits that contribute to complex social behavior (4, 5). These comprise a set of domaingeneral brain areas, including the ventromedial prefrontal cortex and ventral striatum, that process information about reward and punishment and contribute to decision-making, and a set of specialized areas, including the temporoparietal junction and medial prefrontal cortex, that process specifically social information (4, 6). How social and nonsocial signals in these circuits are integrated to mediate decisions with respect to others remains imperfectly understood, in part, due to the indirect nature of hemodynamic signals measured in human neuroimaging experiments that constitute the bulk of this research. Recent advances in the development of neurophysiological and neuropharmacological models of social decision-making, however, permit more direct inquiry into the neural mechanisms mediating other-regarding behavior (7-11).The amygdala, especially the basolateral division (BLA), has been implicated in both decision-making and social perception, inviting the possibility that it contributes to decision-making with respect to others (12)(13)(14)(15)(16)(17). This set of nuclei is well known for contributions to emotional experience and expression, especia...

The roots of empathy: Through the lens of rodent models

“…It has been recently shown that in the basolateral amygdala of monkeys there are neurons that mirror value of rewards delivered to self and others (Chang et al, 2015), suggesting a possible role of such neurons in vicarious experience of emotions. However mirror mechanism is not the only possible explanation of vicarious emotions.…”

Endocannabinoid Signaling in the Control of Social Behavior

“…Hypothalamic neurons that release the neuropeptide oxytocin respond selectively to social information, and oxytocin plays a central role in the regulation of social behaviors, such as maternal care, attachment, and social memory [55,114,124–128]. Importantly, specific neural circuitry likely mediate these effects [55,127,129–131]. Studies have validated the prosocial effects of oxytocin in humans [132–134] and elaborated its role in more complex, human-level behaviors such as trust and empathy [135,136].…”

Social Decision-Making and the Brain: A Comparative Perspective

“…This sensitivity decreased proportionally with social distance between the two monkeys as measured in their home environment, and was correlated with the amount of mutual gaze and mutual eye blinking observed between partners [66]. In a similar experiment, researchers trained rhesus macaques to play a modified version of the classic dictator game while recording from single neurons in the basolateral amygdala [67]. They identified neurons that signaled the value of rewards for both self and for a social partner when dictators made overt decisions to give or withhold reward but not when the computer made the decisions, suggesting an active role for these neurons in social decision making.…”