The orbitofrontal cortex as part of a hierarchical neural system mediating choice between two good options

Animals rely on environmental cues to identify potential rewards and select the best reward available. The orbitofrontal cortex (OFC) is proposed to encode sensory-specific representations of expected outcome. However, its contribution to the selection of a preferred outcome among different reward options is still unclear. We investigated the effect of transient OFC inactivation (achieved by presession injection of muscimol and baclofen) in a novel two-reward choice task. In discrete trials, rats could choose between a solution of polycose and an equally caloric, but highly preferred, solution of sucrose by visiting one of two liquid dispensers after the presentation of a specific cue signaling the availability of one or both of the solutions. We found that OFC inactivation did not affect outcome preference: rats maintained high preference for sucrose and adapted their behavioral responding when the cue-outcome contingencies were reversed. However, when rats were tested drug-free 24 h after OFC inactivation and reversal learning, memory for the newly learned contingencies was poor. These results suggest a potential conflict between OFC (encoding pre-reversal contingencies) and other brain circuits (encoding the new contingencies). Remarkably, repeating the OFC inactivation before the reversal memory test restored normal behavior, confirming the hypothesis of a dominant impact of OFC on other decision-making circuits. These results indicate that the representations encoded in the OFC, while not essential to the expression of outcome preference, exert hierarchical control on downstream decision-making circuits.