Memory-Guided Learning: CA1 and CA3 Neuronal Ensembles Differentially Encode the Commonalities and Differences between Situations

Memory influences learning, but how neural signals support such transfer are unknown. To investigate these mechanisms, we trained rats to perform a standard spatial memory task in a plus maze and tested how training affected learning and neural coding in two new task variants. A switch task exchanged the start and goal locations in the same environment, whereas, an altered environment task contained unfamiliar local and distal cues. Learning was facilitated in both variants compared with the acquisition of the standard task. In the switch task, performance was largely maintained, and was accompanied by immediate and stable place-field remapping. Place-field maps in CA1 were anticorrelated in the standard and switch sessions, and the anticorrelation covaried with switch performance. Simultaneously, CA3 maps were uncorrelated overall in the standard and switch, though many CA3 cells had fields in shifted locations in the same maze arms. In the altered environment, performance was initially impaired, and place fields changed dynamically. CA1 fields were initially unstable, and their stabilization correlated with improving performance. Most CA3 cells, however, stopped firing on the maze in the altered environment, even as the same cells maintained prominent fields in standard sessions recorded before and after. CA1 and CA3 place fields thus revealed different coding dynamics that correlated with both learning and memory performance. Together, CA1 and CA3 ensembles represented the similarities and differences between new and familiar situations through concurrent rate and place remapping.