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Newly discovered neurons predict the cooperative behavior of others

Cell Press

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IMAGE: Cells in the cingulate cortex of primates are able to anticipate the unknown intentions or state of mind of other individuals and have critical importance in enacting cooperative social behavior, a framework that might be... view more

Credit: Katie Ris-Vicari/Cell 2015

Social interactions rely on the ability to anticipate others' intentions and actions, and identifying neurons that reflect another individual's so-called "state of mind" has been a long-sought goal in neuroscience. A study published February 26th in the journal Cell reveals that a newly discovered set of neurons in a frontal brain region called the anterior cingulate is used in primates to predict whether or not an opponent will cooperate in a strategic decision-making task, providing information about the inherently unobservable and unknown decisions of others. By shedding light on the neuronal basis of cooperative interactions, the study paves the way for the targeted treatment of social behavioral disorders such as autism spectrum disorders.

"Many conflicts or adversarial interactions arise from an inability to accurately read another's intentions or hidden state of mind," says lead author Keren Haroush, MD, a postdoctoral fellow at the Massachusetts General Hospital-Harvard Medical School Center for Nervous System Repair. "Therefore, understanding where and how these computations are performed within the brain may help us better understand how such complex social interactions occur."

Previous studies had shown that brain cells called mirror neurons reflect the known and observable actions of oneself and others. But these neurons do not represent another's imminent decisions or intentions. While neurons that predict another's intended actions have been widely hypothesized and are a cornerstone of many theories on social behavior, their existence had never before been demonstrated. Moreover, past research on the neural basis of social behavior has focused on competitive interactions, leaving it unclear how the brain allows us to interact in mutually beneficial ways.

To address these gaps in knowledge, Haroush and senior study author Massachusetts General Hospital neurosurgeon Ziv Williams, MD, studied mutual decisions in macaque monkeys while recording from neurons at the back of the anterior cingulate, which is involved in learning social information and is connected with other brain regions that play a role in interactive behavior. In successive trials of the classical prisoner's dilemma game, a joint-decision task, two monkeys sitting side by side simultaneously chose whether to cooperate or defect by moving a joystick to select different options shown on a screen in front of them. A monkey received the largest juice reward when it decided to defect while the opponent chose to cooperate, whereas both monkeys received a lower reward for mutual cooperation and the lowest reward for mutual defection.

The activity of about one-quarter of the anterior cingulate neurons reflected the monkey's own decision on a given trial. However, the opponent's yet-unknown upcoming choice affected the activity of about one-third of largely non-overlapping neurons. Moreover, neural population activity in the dorsal anterior cingulate cortex accurately predicted the monkey's own choices in 66% of the trials and the opponent's yet unknown choices in 79% of the trials. When the researchers used electrical stimulation to disrupt the activity of neurons at the back of the anterior cingulate cortex, the monkey was less likely to cooperate after the opponent had cooperated on the preceding trial. This finding suggests that these neurons play a critical role in incorporating recent positive interactions to make mutually beneficial decisions.

Moving forward, the authors will continue to explore how complex interactions are encoded in the brain, with the goal of developing new treatments for social behavioral disorders. "The electrical stimulation technique we used is very similar to what is currently used with deep brain stimulation for treating disorders such as depression and obsessive-compulsive disorder," Williams says. "This study may therefore help guide the future treatment of medically intractable disorders such as autism and antisocial personality disorder, which are often characterized by difficulty with social interactions."

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Cell, Haroush et al.: "Neuronal prediction of opponent's behavior during cooperative social interchange in primates"

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