A temporal mechanism for generating the phase precession of hippocampal place cells

The phase relationship between the activity of hippocampal place cells and the hippocampal theta rhythm systematically precesses as the animal runs th rough the region in an environment called the place field of the cell. We p resent a minimal biophysical model of the phase precession of place cells i n region CA3 of the hippocampus. The model describes the dynamics of two co upled point neurons-namely, a pyramidal cell and an interneuron, the latter of which is driven by a pacemaker input. Outside of the place field, the n etwork displays a stable, background firing pattern that is locked to the t heta rhythm. The pacemaker input drives the interneuron, which in turn acti vates the pyramidal cell. A single stimulus to the pyramidal cell from the dentate gyrus, simulating entrance into the place field, reorganizes the fu nctional roles of the cells in the network for a number of cycles of the th eta rhythm. In the reorganized network, the pyramidal cell drives the inter neuron at a higher frequency than the theta frequency, thus causing a syste matic precession relative to the theta input. The frequency of the pyramida l cell can vary to account for changes in the animal's running speed. The t ransient dynamics end after up to 360 degrees of phase precession when the pacemaker input to the interneuron occurs at a phase to return the network to the stable background firing pattern, thus signaling the end of the plac e field. Our model, in contrast to others, reports that phase precession is a temporally, and not spatially, controlled process. We also predict that like pyramidal cells, interneurons phase precess. Our model provides a mech anism for shutting off place cell firing after the animal has crossed the p lace field, and it explains the observed nearly 360 degrees of phase preces sion. We also describe how this model is consistent with a proposed autoass ociative memory role of the CA3 region.