Predictions about reward outcomes in rhesus monkeys

Human infants and nonhuman animals respond to surprising events by looking longer at unexpected-than-expected situations. These looking responses provide core cognitive evidence that nonverbal minds make predictions about possible outcomes and detect when these predictions fail to match reality. We propose that this phenomenon has crucial parallels with the processes of reward prediction error, indexing the difference between expected and actual reward outcomes. Most work on reward prediction errors to date involves neurobiological techniques that cannot be implemented in many relevant populations, so we developed a novel behavioral task to assess monkeys’ predictions about reward outcomes using looking time responses. In Study 1, we tested how semi-free-ranging monkeys (n = 210) responded to positive error (more rewards than expected), negative error (less rewards than expected), and number control. We found that monkeys looked longer at a given reward when it was unexpectedly large or small, compared to when the same quantity was expected. In Study 2, we compared responses in the positive error condition in monkeys ranging from infancy to old age (n = 363), to assess lifespan changes in sensitivity to reward predictions. We found that adolescent monkeys showed heightened responses to unexpected rewards, similar to patterns seen in humans, but showed no changes during aging. These results suggest that monkeys’ looking responses can be used to track their predictions about rewards and that monkeys share some developmental signatures of reward sensitivity with humans, providing a new approach to accessing cognitive processes underlying reward-based decision-making. Methods See methods in the manuscript for all details.