Exploration Disrupts Choice-Predictive Signals and Alters Dynamics in Prefrontal Cortex

In uncertain environments, decision-makers must balance two goals: they must “exploit” rewarding options but also “explore” in order to discover rewarding alternatives. Exploring and exploiting necessarily change how the brain responds to identical stimuli, but little is known about how these states, and transitions between them, change how the brain transforms sensory information into action. To address this question, we recorded neural activity in a prefrontal sensorimotor area while monkeys naturally switched between exploring and exploiting rewarding options. We found that exploration profoundly reduced spatially selective, choice-predictive activity in single neurons and delayed choice-predictive population dynamics. At the same time, reward learning was increased in brain and behavior. These results indicate that exploration is related to sudden disruptions in prefrontal sensorimotor control and rapid, reward-dependent reorganization of control dynamics. This may facilitate discovery through trial and error. •Monkeys transition between exploratory and exploitative goal states•During exploration, prefrontal choice-predictive activity is virtually absent•Prefrontal dynamics are disrupted during exploration both within and across trials•Exploration enhances reward-dependent learning in brain and behavior Exploratory choices permit the discovery of new rewarding options. Ebitz et al. report that spatially selective, choice-predictive neurons in the prefrontal cortex do not predict choice before exploratory decisions. Reduced prefrontal control may underlie flexible decision-making and trial-and-error discovery.