Social Motivation, Reward and the Roots of Autism


Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. The manner in which neurons in three frontal cortical areas determine the outcomes of social decisions as monkeys performed a reward-allocation task was examined and it was discovered that neurons in the orbitofrontal cortex predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus signaled reward allocations to the other monkey or to no one. In this network of received orbitofrontal cortex and foregone anterior cingulate gyrus reward signaling, anterior cingulate gyrus emerged as an important link for the process of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas.

Social cohesion depends on vicarious identification with members of one’s group. In social situations, we are aware of our actions and their consequences, but also consider those of others, especially those with whom we might interact. We also estimate the internal states of others, perhaps by simulation, which in turn shapes our future actions. Social situations can drive observational learning, and other regarding preferences influence neural computations that ultimately result in cooperation, altruism or spite. Disruptions of neural circuits involved in other regarding processes may underlie social deficits attending neuropsychiatric conditions like autism. Human imaging and clinical studies have found critical links between social deficits and abnormal brain activity in frontal cortex and its subcortical targets.

The study implemented a reward-allocation task in pairs of rhesus macaques while recording from single neurons in three critical nodes in the decision-making network, namely the anterior cingulate gyrus, anterior cingulate sulcus and orbitofrontal cortex. The study capitalized on monkeys’ willingness to engage with a social partner via an interposed computer system while simultaneously controlling the sensory and reward environment. The study specifically matched choices for the reward outcomes directly received by the actor monkey (decision maker) and controlled for potential secondary acoustic reinforcement effects associated with delivering juice to the recipient monkey. In these conditions, study found regional biases in the encoding of social decision outcomes with respect to self and another individual. In this network of received orbitofrontal cortex and foregone anterior cingulate cortex reward signals, anterior cingulate gyrus emerged as an important link for the computation of shared experience and social reward.

 

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