In a temporally segmented experience hippocampal neurons represent temporally drifting context but not discrete segments

Abstract There is widespread agreement that episodic memory depends on a representation of spatiotemporal context. Recent work suggests that people parse the flow of experience into discrete episodes separated by event boundaries. A complementary body of work suggests that context changes gradually as experience unfolds. We recorded from hippocampal neurons as rats performed 6 blocks of an object discrimination task in sets of 15 trials. Each block was separated by a one-minute delay to enable segmentation. The reward contingency reversed from one block to the next to incentivize segmentation. If animals segmented the blocks and learned the reversal contingency, we would expect the animal’s choice to switch with the beginning of each block. Similarly, hippocampal ensembles should reflect the discrete alternating block structure. If the delay between blocks had no effect on memory, one would expect the animals to perseverate, starting each block by repeating the choice from the previous block. We observed neither of these patterns of results. Animals started each new block at chance as if they relied on a recency-weighted average of the reward experience. Hippocampal ensembles showed continuous contextual drift both within block and across blocks and showed no evidence of sensitivity to the alternating block structure. Despite clear boundaries between blocks, we saw no behavioral or neural evidence for event segmentation in this experiment. Rather, the hippocampal ensemble drifted continuously. This continuous drift was consistent with the recency weighted averaging seen in the behavioral results.