UCSF

The hippocampus is essential for encoding new memories for space and events. In the rodent hippocampus, a result of this process is that individual neurons fire selectively when the animal is located in a particular subregion of its environment. We show that that hippocampal area CA1, but not upstream area CA3, emits twice as many spikes in novel as compared to familiar environments, and during the initial stages of novelty many CA1 neurons are active. The overall population rate and the number of active cells decreases as the environment becomes familiar, but the decline in rate is not uniform across neurons. Instead, the activity of cells with peak spatial rates above ~12 Hz is enhanced, while the activity of cells with lower peak rates is suppressed. The result is that, after several days of experience in the environment, the active CA1 population consists of a relatively small group of cells with strong spatial tuning. This process is not evident in CA3, suggesting that a region specific selection process operates in CA1 to create a sparse, spatially informative population of neurons. We also show that there is clear and long lasting replay of experiences from one place during waking behavior in subsequently experienced places. Surprisingly, this remote replay was most robust when the animal had recently been in motion as compared to during extended periods of immobility. These results indicate that waking and sleep replay both constitute a form of memory retrieval where past experiences can be reactivated, and that patterns of activity associated with memory consolidation continue unabated during both sleep and awake states.