Oscillatory and Non-Oscillatory Emergence of Cell Assemblies

Timing of spikes within the theta cycle has been shown to reflect the spatial position of the animal (“phase precession”). The phase of spikes correlates more strongly with distance than with the time elapsed from the point the rat enters the place field. We show here that at faster running speeds place cells are active for fewer theta cycles but oscillate at a higher frequency and emit more spikes per cycle. As a result, the phase shift of spikes from cycle to cycle (i.e., temporal precession slope) is faster. Interneurons also show transient phase precession and contribute to the formation of coherently precessing assemblies. Thus, the speed-correlated increase of place cell oscillation is responsible for the phase-distance invariance of hippocampal place cells.We report that temporal spike sequences from hippocampal “place” neurons on an elevated track recur in reverse order at the end of a run but in forward order in anticipation of the run, coinciding with sharp waves. Vector distances between the place fields are reflected in the temporal structure of these sequences. This bidirectional reenactment of temporal sequences may contribute to the establishment of higher order associations in episodic memory.