CA3 circuit model compressing sequential information in theta oscillation and replay

Abstract

The hippocampus compresses the sequential information in a theta oscillation cycle and short-term sequential activities during sharp-wave ripple while sleeping or resting; these processes are known as theta sequence and replay, respectively. The theta sequence is based on theta phase precession patterns of individual neurons. However, how these sequential neuronal activities are generated and how they store information about the outside environment remains unknown. We developed a hippocampal cornu ammonis (CA)3 computational model based on the biological CA3 circuits anatomical and electrophysiological evidence to address these. The model comprises theta rhythm inhibition, place input, and CA3-CA3 plastic recurrent connection. The model could compress the sequence of the external inputs and reproduce theta phase precession and replay, learn additional sequences, and reorganize previously learned sequences. A gradual increase in synaptic inputs, controlled by interactions between theta-paced inhibition and place inputs, explained the mechanism for sequence acquisition. This model highlights the crucial role of plasticity in the CA3 recurrent connection and theta oscillational dynamics, and hypothesizes how the CA3 circuit acquires, compresses, and replays sequential information.