CA3 Retrieves Coherent Representations from Degraded Input: Direct Evidence for CA3 Pattern Completion and Dentate Gyrus Pattern Separation

Theories of associative memory suggest that successful memory storage and recall depend on a balance between two complementary processes: pattern separation (to minimize interference) and pattern completion (to retrieve a memory when presented with partial or degraded input cues). Putative attractor circuitry in the hippocampal CA3 region is thought to be the final arbiter between these two processes. Here we present direct, quantitative evidence that CA3 produces an output pattern closer to the originally stored representation than its degraded input patterns from the dentate gyrus (DG). We simultaneously recorded activity from CA3 and DG of behaving rats when local and global reference frames were placed in conflict. CA3 showed a coherent population response to the conflict (pattern completion), even though its DG inputs were severely disrupted (pattern separation). The results thus confirm the hallmark predictions of a longstanding computational model of hippocampal memory processing.