Orbitofrontal state representations are related to choice adaptations and reward predictions

Abstract

Animals can categorize the environment into “states,” defined by unique sets of available action-outcome contingencies in different contexts. Doing so helps them choose appropriate actions and make accurate outcome predictions when in each given state. State maps have been hypothesized to be held in the orbitofrontal cortex (OFC), an area implicated in decision making and encoding information about outcome predictions. Here we recorded neural activity in OFC in six male rats to test state representations. Rats were trained on an odor-guided choice task consisting of five trial blocks containing distinct sets of action-outcome contingencies, constituting states, with unsignaled transitions between them. OFC neural ensembles were analyzed using decoding algorithms. Results indicate that the vast majority of OFC neurons contributed to representations of the current state at any point in time, independent of odor cues and reward delivery, even at the level of individual neurons. Across state transitions, these representations gradually integrated evidence for the new state; the rate at which this integration happened in the pre-choice part of the trial was related to how quickly the rats’ choices adapted to the new state. Finally, OFC representations of outcome predictions, often thought to be the primary function of OFC, were dependent on the accuracy of OFC state representations.

SIGNIFICANCE STATEMENT: A prominent hypothesis proposes that orbitofrontal cortex (OFC) tracks current location in a “cognitive map” of state space. Here we tested this idea in detail by analyzing neural activity recorded in OFC of rats performing a task consisting of a series of states, each defined by a set of available action-outcome contingencies. Results show that most OFC neurons contribute to state representations and that these representations are related to the rats’ decision making and OFC reward predictions. These findings suggest new interpretations of emotional dysregulation in pathologies such as addiction, which have long been known to be related to OFC dysfunction.