When shared concept cells support associations: Theory of overlapping memory engrams

Author summaryExperimental evidence suggests that associations between concepts are encoded in the hippocampus by cells shared between neuronal assemblies ("overlap" of concepts). What is the necessary overlap that ensures a reliable encoding of associations? Under which conditions can associations induce a simultaneous or a chain-like activation of concepts? Our theoretical model shows that the ideal overlap presents a tradeoff: the overlap should be larger than a minimum value in order to reliably encode associations, but lower than a maximum value to prevent loss of individual memories. Our theory explains experimental data from human Medial Temporal Lobe and provides a mechanism for chain-like recall in presence of inhibition, while still allowing for simultaneous recall if inhibition is weak. Assemblies of neurons, called concepts cells, encode acquired concepts in human Medial Temporal Lobe. Those concept cells that are shared between two assemblies have been hypothesized to encode associations between concepts. Here we test this hypothesis in a computational model of attractor neural networks. We find that for concepts encoded in sparse neural assemblies there is a minimal fraction c(min) of neurons shared between assemblies below which associations cannot be reliably implemented; and a maximal fraction c(max) of shared neurons above which single concepts can no longer be retrieved. In the presence of a periodically modulated background signal, such as hippocampal oscillations, recall takes the form of association chains reminiscent of those postulated by theories of free recall of words. Predictions of an iterative overlap-generating model match experimental data on the number of concepts to which a neuron responds.