Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network

Abstract

The CA3 network in the hippocampus may operate as an autoassociator, in which declarative memories, known to be dependent on hippocampal processing, could be stored, and subsequently retrieved, using modifiable synaptic efficacies in the CA3 recurrent collateral system. On the basis of this hypothesis, the authors explore the computational relevance of the extrinsic afferents to the CA3 network. A quantitative statistical analysis of the information that may be relayed by such afferent connections reveals the need for two distinct systems of input synapses. The synapses of the first system need to be strong (but not associatively modifiable) in order to force, during learning, the CA3 cells into a pattern of activity relatively independent of any inputs being received from the recurrent collaterals, and which thus reflects sizable amounts of new information. It is proposed that the mossy fiber system performs this function. A second system, with a large number of associatively modifiable synapses on each receiving cell, is needed in order to relay a signal specific enough to initiate the retrieval process. This may be identified, we propose, with the perforant path input to CA3.