Hippocampal signals modify orbitofrontal representations to learn new paths

We often remember the consequences of past choices to adapt to changing circumstances. Recalling past events requires the hippocampus (HPC), and using stimuli to anticipate outcome values requires the orbitofrontal cortex (OFC).(1-3) Spatial reversal tasks require both structures to navigate newly rewarded paths.(4,5) Both HPC place (6) and OFC value cells(7,8) fire in phase with theta (4-12 Hz) oscillations. Both structures are described as cognitive maps: HPC maps space(9) and OFC maps task states.(10) These similarities imply that OFC-HPC interactions are crucial for using memory to predict outcomes when circumstances change, but the mechanisms remain largely unknown. To investigate possible interactions, we simultaneously recorded ensembles in OFC and CA1 as rats learned spatial reversals in a plus maze. Striking interactions occurred only while rats learned their first reversal: CA1 population vectors predicted changes in OFC activity but not vice versa, OFC spikes phase locked to hippocampal theta oscillations, mixed pairs of CA1 and OFC neurons fired together within single theta cycles, and CA1 led OFC spikes by similar to 30 ms. After the new contingency became familiar, CA1 ensembles stably represented distinct spatial paths, whereas OFC ensembles developed more generalized goal arm representations in different paths to identical rewards. These frontotemporal interactions, engaged selectively when new task features inform decision-making, suggest a mechanism for linking novel episodes with expected outcomes, when HPC signals trigger ``cognitive remapping'' by OFC.(11)

Automated summary

This study investigates the interaction between the OFC and HPC during the learning of spatial reversal tasks. The results reveal significant interactions between the activity of the OFC and CA1 during the first reversal, but their activity shows different characteristics once the task becomes familiar. These frontotemporal interactions occur selectively when new task features inform decision-making and provide a mechanism for linking novel episodes with expected outcomes.