Summary Theories of associative memory suggest that successful memory storage and recall depends 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 the first 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.

The hippocampus receives its major cortical input from the medial entorhinal cortex (MEC) and the lateral entorhinal cortex (LEC). It is commonly believed that the MEC provides spatial input to the hippocampus, whereas the LEC provides non-spatial input. We review new data which suggest that this simple dichotomy between ‘where’ versus ‘what’ needs revision. We propose a refinement of this model, which is more complex than the simple spatial–non-spatial dichotomy. MEC is proposed to be involved in path integration computations based on a global frame of reference, primarily using internally generated, self-motion cues and external input about environmental boundaries and scenes; it provides the hippocampus with a coordinate system that underlies the spatial context of an experience. LEC is proposed to process information about individual items and locations based on a local frame of reference, primarily using external sensory input; it provides the hippocampus with information about the content of an experience.