Hippocampal State Transitions at the Boundaries between Trial Epochs

Abstract

The hippocampus encodes distinct environmental and behavioral contexts with unique patterns of activity. Representational shifts with changes in the context, referred to as remapping, have been extensively studied. However, less is known about the nature of transitions between representations. In this study, we leverage a large dataset of 2056 neurons recorded while rats performed an olfactory memory task with a predictable temporal structure involving trials and inter-trial intervals, separated by salient boundaries at the trial start and trial end. We found that trial epochs were associated with stable hippocampal population representations, despite moment to moment variability in stimuli and behavior. Representations of trial and inter-trial interval epochs were far more distinct than spatial factors would predict and the transitions between the two were abrupt, with a sharp boundary suggestive of a dynamic shift in the representational state. This boundary was associated with a large spike in multi-unit activity, with many individual cells specifically active at the start or end of each trial. Both epochs and boundaries were encoded by hippocampal populations, and these representations carried information on orthogonal axes readily identified using principal component analysis. We suggest that the activity spike at trial boundaries might serve to drive hippocampal activity from one stable state to another, and may play a role in segmenting continuous experience into discrete episodic memories.