Neuronal Circuits for Social Decision-Making and Their Clinical Implications

Abstract

Social living facilitates individual access to rewards, cognitive resources, and objects that would not be otherwise accessible. There are, however, some drawbacks to social living, particularly when competing for scarce resources. Furthermore, variability in our ability to make social decisions can be associated with neuropsychiatric disorders. The neuronal mechanisms underlying social decision-making are beginning to be understood. The momentum to study this phenomenon has been partially carried over by the study of economic decision-making. Yet, because of the similarities between these different types of decision-making, it is unclear what is a social decision. Here, we propose a definition of social decision-making as choices taken in a context where one or more conspecifics are involved in the decision or the consequences of it. Social decisions can be conceptualized as complex economic decisions since they are based on the subjective preferences between different goods. During social decisions, individuals choose based on their internal value estimate of the different alternatives. These are complex decisions given that conspecifics beliefs or actions could modify the subject's internal valuations at every choice. Here, we first review recent developments in our collective understanding of the neuronal mechanisms and circuits of social decision-making in primates. We then review literature characterizing populations with neuropsychiatric disorders showing deficits in social decision-making and the underlying neuronal circuitries associated with these deficits.

Keywords: decision making; mental health; neuroeconomics; neurophysiology; primates; psychiatry; social cognition; translational neuroscience.

FIGURE 1

Schema of Value-based social decision-making. Under this model, the value of each good is computed by integrating multiple types of information or determinants, some of which are external social & non-social determinants, while others are social & non-social determinants computed internally. The values of different goods are computed independently of each other and are compared to decide. The decision outcome guides an action plan through a good-to-action transformation. Values and choice outcomes inform future value computations through observational learning, emotion, and observed movements. Based on Padoa-Schioppa (2011).

FIGURE 2

Brain regions that comprise the social information processing network. The face-processing network includes the face patch areas along the superior temporal sulcus (STS), the temporal pole (TP), and the amygdala (Amy) within the temporal lobe, the lateral orbitofrontal cortex (OFC) and the dorsolateral prefrontal cortex (dlPFC) in the frontal lobe. Biological motion is encoded by neurons in the superior temporal sulcus (STS). Bidirectional arrows indicate the interdependence of these processes on acquiring social information. The areas are illustrated on a side view of a Rhesus brain.

FIGURE 3

The social valuation network comprises several cortical areas, including: the anterior cingulate cortex (ACC), medial prefrontal cortex (mPFC), medial orbitofrontal cortex (OFC), insula (Ins); and subcortical nuclei including: the anterior striatum, amygdala (Amy), and substantia nigra pars compacta (SNc). Each one of these regions plays a specialized role during distinct cognitive processes of social decision making. Bidirectional arrows indicate the interdependence of these processes on social decisions. All brain regions are illustrated on a sagittal view of a Rhesus brain.

FIGURE 4

Experimental games used to probe social decision-making. (A) Dictator Game. In the Dictator Game the person playing as dictator receives an initial financial endowment and decides to give an amount of the endowment to a receiver. The neoclassical assumption of rational behavior predicts that dictators will not give away anything of their payoff; however, dictators usually give away between 5 and 25% of their initial endowment (Forsythe et al., 1994). It is assumed that the proportion of money given to the receiver is a measure of the disutility for the dictator of having more than the other (Gibbons, 1992; Camerer et al., 2004). (B) Ultimatum Game. In this game, the proposer receives an endowment and proposes a split to the responder, just as in the Dictator Game. The responder then either rejects the split, thereby forgoing all monies, or accepts it. Neoclassical economic models predict that the responder will accept any split that results in him having more than nothing. However, responders tend to only accept splits where they obtain more than 30% of the initial endowment (Güth et al., 1982). The responder’s minimum acceptable offer is the percentage of the initial endowment that he is willing to accept 50% of the time (Camerer et al., 2004). This last parameter is directly proportional to the degree of disadvantageous inequality aversion. Some have suggested, instead, that rejecting an offer is a form of altruistic punishment that can foment future cooperation (e.g., Sanfey et al., 2003). (C) Prisoner’s Dilemma. In this game, two players choose between cooperation or defection. Mutual cooperation results in a medium-size reward for both players, while mutual defection results in a small reward. But if one of them defects then they receive the highest reward, the tempting reward, while the other receives the lowest, or sucker’s, payoff. The game tests the ability of both players to cooperate and trust others.

FIGURE 5

Location of differential brain activity during social decision making associated with different psychiatric conditions. Brain regions are illustrated on a lateral (left) or sagittal (right) view of the human brain.