Differential Reactivation of Task-Demand-Associated Firing Patterns in Subicular and CA1 Place Cells during a Hippocampal Memory Task

Abstract

Reactivation of place cells during sharp-wave ripples (SWRs) in the hippocampus is pivotal for memory consolidation, yet differences in SWR dynamics between the hippocampus and its neighboring subiculum remain underexplored. We examined the differential reactivations of task-demand-associated representations during SWR events in the subiculum and CA1 during a visual scene memory task in rats. In the task, the spiking activity of place cell ensembles was reactivated during a SWR event according to task demands. These reactivations were more frequent and were associated with more heterogeneous task-demand types in the subiculum compared with the CA1. Neural manifold analysis showed that the neural states of the reactivated ensemble were more clearly clustered into distinct states during subicular SWRs according to the task-demand-associated variables. These subicular characteristics were driven by multiple subfields of the subicular place field, parcellated by the theta phase precession cycle. In contrast, CA1 exhibited a higher incidence of spatial replay than the subiculum. These findings indicate that the subiculum plays a key role in transmitting task-specific variables from the hippocampus to other brain regions.