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A quantitative computational theory of the operation of the hippocampal CA3 system as an autoassociation or attractor network used in episodic memory system is described. In this theory, the CA3 system operates as a single attractor or autoassociation network to enable rapid, one-trial, associations between any spatial location (place in rodents, or spatial view in primates) and an object or reward, and to provide for completion of the whole memory during recall from any part. The theory is extended to associations between time and object or reward to implement temporal order memory, also important in episodic memory. The dentate gyrus (DG) performs pattern separation by competitive learning to produce sparse representations suitable for setting up new representations in CA3 during learning, producing for example neurons with place-like fields from entorhinal cortex grid cells. The dentate granule cells produce by the very small number of mossy fiber (MF) connections to CA3 a randomizing pattern separation effect important during learning but not recall that separates out the patterns represented by CA3 firing to be very different from each other, which is optimal for an unstructured episodic memory system in which each memory must be kept distinct from other memories. The direct perforant path (pp) input to CA3 is quantitatively appropriate to provide the cue for recall in CA3, but not for learning. Tests of the theory including hippocampal subregion analyses and hippocampal NMDA receptor knockouts are described, and support the theory.

A quantitative theory of the functions of the hippocampal CA3 network in memory