Activity of striatal neurons reflects social action and own reward

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 110; no. 41; pp. 16634 - 16639
• Main Authors: Báez-Mendoza, Raymundo, Harris, Christopher J., Schultz, Wolfram
• Format: Journal Article
• Language: English
• Published: Washington, DC National Academy of Sciences 08-10-2013; NATIONAL ACADEMY OF SCIENCES; National Acad Sciences
• Subjects: Acting; Analysis of Variance; Animals; Behavioral neuroscience; Biological and medical sciences; Biological Sciences; Brain; Corpus Striatum - cytology; Discounting; Discrimination, Psychological - physiology; Eye movements; Eye Movements - physiology; Fundamental and applied biological sciences. Psychology; Linear Models; Macaca mulatta; Macaca mulatta - physiology; Male; Monkeys & apes; Neurons; Neurons - metabolism; Neuropsychology; Primates; Reward; ROC Curve; Social Behavior; Social interaction; Social movements; Vertebrates: nervous system and sense organs; Basal ganglion; Corpus striatum; Neuron; Reward; Central nervous system; Encephalon
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1211342110

Social interactions provide agents with the opportunity to earn higher benefits than when acting alone and contribute to evolutionary stable strategies. A basic requirement for engaging in beneficial social interactions is to recognize the actor whose movement results in reward. Despite the recent interest in the neural basis of social interactions, the neurophysiological mechanisms identifying the actor in social reward situations are unknown. A brain structure well suited for exploring this issue is the striatum, which plays a role in movement, reward, and goal-directed behavior. In humans, the striatum is involved in social processes related to reward inequity, donations to charity, and observational learning. We studied the neurophysiology of social action for reward in rhesus monkeys performing a reward-giving task. The behavioral data showed that the animals distinguished between their own and the conspecific’s reward and knew which individual acted. Striatal neurons coded primarily own reward but rarely other's reward. Importantly, the activations occurred preferentially, and in approximately similar fractions, when either the own or the conspecific's action was followed by own reward. Other striatal neurons showed social action coding without reward. Some of the social action coding disappeared when the conspecific's role was simulated by a computer, confirming a social rather than observational relationship. These findings demonstrate a role of striatal neurons in identifying the social actor and own reward in a social setting. These processes may provide basic building blocks underlying the brain's function in social interactions.