Orbitofrontal-hippocampal state coding dynamics during reversal learning

Abstract

To build an understanding of our world, we make inferences about the connections between our actions, experiences, and the environment. This process, state inference, requires an agent to guess the current state of the world given a set of observations. During value-based decision-making, a growing body of evidence implicates the orbitofrontal cortex (OFC) and the hippocampus (HPC) in the process of contextualizing information and identifying links between stimuli, actions, and outcomes. However, the neural mechanisms driving these processes in primates remain unknown. To investigate how OFC and HPC contribute to state inference, we recorded simultaneously from both regions while two male monkeys (Macaca mulatta) performed a probabilistic reversal learning task, where reward contingencies could be captured by two task states. Using population-level decoding, we found neural representations of task state in both OFC and HPC that remained stable within each trial but strengthened with learning as monkeys adapted to reversals. Subjects also appeared to use their understanding of task structure to anticipate reversals, evidenced by anticipatory neural representations of the upcoming task state.

Significance Statement During value-based decision-making, a growing body of evidence implicates the orbitofrontal cortex (OFC) and the hippocampus (HPC) in the process of contextualizing information and identifying links between stimuli, actions, and outcomes. However, limited work has been done in nonhuman primates to bridge the gap between rodent and human models. In this study, we show that task state is represented in both OFC and HPC in nonhuman primates. These representations remain stable within each trial, but evolve with learning and anticipate upcoming task changes, equipping subjects to adapt their choice preferences to reversals in reward contingencies. Our results support the theory that OFC-HPC interactions are important for flexible, goal-directed decision making, and provide insight into how the OFC and HPC participate in decision making when information is not explicitly provided, but must instead be inferred.