Effects of Novelty and Temporal Distance on Postexperience Spike Patterns of Hippocampal Place Cells Encoding Multiple Environments

Abstract

The hippocampus plays a crucial role in consolidating episodic memories from diverse experiences that encompass spatial, temporal, and novel information. This study analyzed the spike patterns of hippocampal place cells in the CA3 and CA1 areas of male rats that sequentially foraged in five rooms, including familiar and novel rooms, followed by a rest period. Across the five rooms, both CA3 and CA1 place cells showed overlapping spatial representations. In a postexperience rest period, both CA3 and CA1 place cells increased baseline spike rates depending on the temporal distance from when the cells had place fields. In addition, CA3 place cells that encoded novel environments showed stronger sharp-wave ripple (SWR) reactivation. Coordinated reactivation of CA1 place cell ensembles that encoded temporally distant environments was eliminated. These results suggest that, following sequential experiences in multiple environments, increases in SWR-induced spikes of hippocampal neurons more specifically process novelty-related aspects of memory, while global increases in baseline spike rates process temporal distance-related aspects.