UC San Diego

Memories for autobiographical events contain information not only about what happened, but also about when and where. The hippocampus is known to be critical for organizing autobiographical memories, yet little is known about how the temporal context of a memory is represented there, especially on the timescale of hours to days. We sought to elucidate the coding mechanisms used by the hippocampus to represent the spatio-temporal context of events. In our experimental paradigm, rats performed random foraging tasks twice a day for several days, as we conducted electrophysiological recordings in three subregions of the hippocampus, CA1, CA2, and CA3. By recording from the same cells for 30 or more hours, we were able to evaluate the impact of passing time on the representation of identical events in each of these subregions. We performed these experiments within two distinct arenas, allowing us to explore coding for spatial context in addition to temporal context. We found that the population of cells in CA3 showed robust coding for spatial context that was very stable for a period of at least 30 hours. Conversely, neuronal ensembles in CA2 were highly variable on the time scale of hours to days, with the change in time overshadowing change with spatial context. Finally, CA1, which receives input from each of these regions, showed a gradual change with time while also coding strongly for spatial context. These findings correspond well with theoretical predictions that time- stamped memories may be generated by combining a stable content signal with a time-varying temporal context signal. We thus propose that CA2 provides temporal context information to CA1, while CA3 provides stable information about space and spatial context, allowing CA1 to represent both types of information simultaneously