Model of Balance of Excitation and Inhibition in Hippocampal Sharp Wave Replays and Application to Spatial Remapping

In a recent experimental paper, D.J.Foster and M.A.Wilson (2006) report reverse replay of recent behavioural sequences in rat Hippocampal CA3 place cells during the awake state immediately after spatial experience at the reward location. The replay is associated with a fast oscillation known as a dendritic sharp wave, which occurs as a ripple in the electroencephalogram (EEG). Here we propose a very simple dynamical firing rate neural model of this phenomenon based on balance of multiplicative feedback inhibition between the pyramidal cells and basket cells in the CA3 region of the hippocampus. This model accounts for the reverseness of the replayed re-activations as well as for some characteristics of the ripple oscillation. Furthermore we suggest the function of the replay itself is to perform a spatial remapping and therefore to form a cognitive map of the experienced environment. We illustrate this idea with the creation of a map where the place cell firing rate depends on distance to the replay location and which can therefore be used in spatial navigation to follow the shortest experienced path to a goal. As a second illustration we show how the model naturally accounts for splitter cells, which are cells whose response varies on the central arm of successive trials of an alternation task despite the fact that the environmental input is the same.