Asymmetry of the temporal code for space by hippocampal place cells

Hippocampal place cells convey spatial information through spike frequency (\"rate coding\") and spike timing relative to the theta phase (\"temporal coding\"). Whether rate and temporal coding are due to independent or related mechanisms has been the subject of wide debate. Here we show that the spike timing of place cells couples to theta phase before major increases in firing rate, anticipating the animals entrance into the classical, rate-based place field. In contrast, spikes rapidly decouple from theta as the animal leaves the place field and firing rate decreases. Therefore, temporal coding has strong asymmetry around the place field center. We further show that the dynamics of temporal coding along space evolves in three stages: phase coupling, phase precession and phase decoupling. These results suggest that place cells represent more future than past locations through their spike timing and that independent mechanisms govern rate and temporal coding.