Hippocampal Consolidation Hypothesis

I sketched a theory in Section 4.13 of my 1996 thesis of what I think the hippocampus might be doing. In that sketch, shown animated below [note: four trials of the same input (to EC) are shown], a cortical code at time T begets a DG/CA3 code, which begets a CA1/Subic. code. This last code sends a wave of synaptic signals that would arrive back at cortex contemporaneously with intra-cortical signals propagating via the local intrinsic (horizontal) L2/3 matrix, which were also begotten by the original time T cortical code. That original code might not have yet changed [due to assumed longer persistence of EC codes (e.g., persistence = 4 time steps)] or if it has changed, then the updated EC code will be determininstically related, through perhaps several intermediate EC codes, to the original time T cortical code.

If we assume that the synapses impinging or internal to the hippocampus are updated in all-or-none (binary) fashion (heavy arrows), then the rapidly (e.g., single-trial) learned hippocampal trace, can function to assist the more gradual strengthening of intra-cortical weights (i.e., consolidation) (visually suggested here by the gradually thickening intra-cortical arrows) on successive trials. Note: although this animation suggests multiple trials orginating in the environment, the basic concept can accommodate a scheme in which the "repeated trials" actually arise from within the hippocampus itself, consistent with studies showing recapitulation of traces in sleep periods following training experience, e.g., Ji & Wilson (2007) and many others.

So, this model predicts that the spatiotemporal trace (i.e., phase sequence of cell assemblies) laid down in cortex during the initial experience is stable from that initial occurrence. However, initially it is stable only with the assist from the spatiotemporal hippocampal trace that will also have been laid down during that initial occurrence. As the intra-cortical associations strengthen, the purely cortical trace of the experience becomes independent of the hippocampus. Once the intra-cortical pathways are firmly entrenched, the intra-hippocampal pathways that aided consolidation are no longer needed and are free to be overwritten by newly experienced associations. Thus, the weights in the hippocampal path can have much faster forgetting rates than the strictly cortical weights. Thus, while the hippocampus is small compared to the cortex, such a faster forgetting rate protects it from becoming oversaturated, which would lead to information loss due to crosstalk interference. Further protection from interference is likely also conferred by the neurogenesis that has been found to occur in the hippocampus throughout the lifespan.

The animation below provides additional intuition as to the proposed scheme. It suggests that the hippocampus, being at the apex of the cortical hierarchy, essentially provides: a) a complex infrastucture for organizing top-down (recurrent) feedback at the scale of the whole hierarchy, which augments and perhaps provides meta control for the local top-down recurrence between adjacent cortical regions; and b) a subcircuit that has evolved to specifically assist with learning/handling temporal/sequential relations.

Beyond the hippocampus's role in consolidation, the scheme described here also effectively increases the (horizontal) connectivity rate of the entorhinal cortex. It does this by allowing associations to be formed via multi-step mappings. That is, reliable connections between cells separated by more than one synapse can be embedded. This should generally allow richer, more multimodal concepts to be learned.