In a Temporally Segmented Experience Hippocampal Neurons Represent Temporally Drifting Context But Not Discrete Segments.

Abstract

There is widespread agreement that episodic memory is organized into a timeline of past experiences. Recent work suggests that the hippocampus may 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 male Long-Evans rats performed 6 blocks of an object discrimination task in sets of 15 trials. Each block was separated by removal from the testing chamber for a delay to enable segmentation. The reward contingency reversed from one block to the next to incentivize segmentation. We expected animals to hold two distinct, recurring representations of context to match the two distinct rule contingencies. Instead, we found that overtrained rats began each block neither above nor below chance but by guessing randomly. While many units had clear firing fields selective to the conjunction of objects in places, a significant population also reflected a continuously drifting code both within block and across blocks. Despite clear boundaries between blocks, we saw no neural evidence for event segmentation in this experiment. Rather, the hippocampal ensemble drifted continuously across time. This continuous drift in the neural representation was consistent with the lack of segmentation observed in behavior.SIGNIFICANCE STATEMENT The neuroscience literature yet to reach consensus on how the hippocampus supports the organization of events across time in episodic memory. Initial studies reported stable hippocampal maps segmented by remapping events. However, it remains unclear whether segmentation is an artifact of cue responsivity. Recently, research has shown that the hippocampal code exhibits continuous drift. Drift may represent a continually evolving context; however, it is unclear whether this is an artifact of changing experiences. We recorded dCA1 in rats performing an object discrimination task designed to segment time. Overtrained rats could not anticipate upcoming context switches but used context boundaries to their advantage. Hippocampal ensembles showed neither evidence of alternating between stable contexts nor sensitivity to boundaries, but showed robust temporal drift.