POPULATION-DYNAMICS AND THETA-RHYTHM PHASE PRECESSION OF HIPPOCAMPAL PLACE CELL FIRING - A SPIKING NEURON MODEL

O'Keefe and Recce ([1993] Hippocampus 68:317-330) have observed that t he spatially selective firing of pyramidal cells in the CA1 field of t he rat hippocampus tends to advance to earlier phases of the electroen cephalogram theta rhythm as a rat passes through the place field of a cell. We present here a neural network model based on integrate-and-fi re neurons that accounts for this effect. In this model, place selecti vity in the hippocampus is a consequence of synaptic interactions betw een pyramidal neurons together with weakly selective external input. T he phase shift of neuronal spiking arises in the model as a result of asymmetric spread of activation through the network, caused by asymmet ry in the synaptic interactions. Several experimentally observed prope rties of the phase shift effect follow naturally from the model, inclu ding 1) the observation that the first spikes a cell fires appear near the theta phase corresponding to minimal population activity, 2) the overall advance is less than 360 degrees, and 3) the location of the r at within the place field of the cell is the primary correlate of the firing phase, not the time the rat has been in the field. The model ma kes several predictions concerning the emergence of place fields durin g the earliest stages of exploration in a novel environment. It also s uggests new experiments that could provide further constraints on a po ssible explanation of the phase precession effect. (C) 1996 Wiley-Liss , Inc.