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.\n\nSignificance StatementThe neuroscience literature yet to reach consensus as to how hippocampal firing fields support the organizing of events across time in episodic memory. Initial reports of hippocampal activity focused on discrete episodes within which representations were stable, and across which representations remapped. However, it remains unclear whether this segmentation of representations is merely an artifact of cue responsivity. More recently, research has shown that a proportion of the population codes for temporal aspects of context by exhibiting varying degrees of drift in their firing fields. Drift is hypothesized to represent a continually evolving temporal context, however it is unclear whether this drift is continuous or is also a mere artifact of changing experiences. We recorded from the dorsal hippocampus of rats performing an object discrimination task that involved contexts that were segmented in time. Overtrained rats were unable to anticipate the identity of the upcoming context, but may have used context boundaries to their advantage. Event segmentation theory predicts that hippocampal ensembles would alternate between behaviorally-relevant segments. Contrary to these predictions, animals showed weak evidence of context segmentation, even across blocks with different reward contingencies. Hippocampal ensembles showed neither evidence of alternating between stable contexts nor sensitivity to context boundaries, but did show robust temporal drift.