Episodic-like memory trace in awake replay of hippocampal place cell activity sequences.

Susumu Takahashi

doi:10.7554/elife.08105

Abstract

Episodic memory retrieval of events at a specific place and time is effective for future planning. Sequential reactivation of the hippocampal place cells along familiar paths while the animal pauses is well suited to such a memory retrieval process. It is, however, unknown whether this awake replay represents events occurring along the path. Using a subtask switching protocol in which the animal experienced three subtasks as 'what' information in a maze, I here show that the replay represents a trial type, consisting of path and subtask, in terms of neuronal firing timings and rates. The actual trial type to be rewarded could only be reliably predicted from replays that occurred at the decision point. This trial-type representation implies that not only 'where and when' but also 'what' information is contained in the replay. This result supports the view that awake replay is an episodic-like memory retrieval process.

Highlights

One of the most important aspects of episodic memory is the mental retrieval of personal recollections of what happened “where” and “when”, referred to as “mental time travel” (Tulving, 1983)
According to the subtask switching protocol, four rats were trained for about one hour in a specific sequence—visually guided discrimination (VD) (20 laps), non-delayed spatial alternation (NA) (20 laps), VD (10 laps), delayed spatial alternation (DA) (20 laps), VD (20 laps), NA (20 laps), VD (10 laps), and DA (20 laps)—and were rewarded each time they arrived at the reward zone at the correct return rail
The replay can represent the actual trial type accurately when the trial type can be identified, but otherwise it evenly represents all trial types previously experienced along the reactivated path

Summary

Introduction

One of the most important aspects of episodic memory is the mental retrieval of personal recollections of what happened “where” and “when”, referred to as “mental time travel” (Tulving, 1983). The hippocampus is critically involved in episodic memory retrieval, and within this structure reside place cells—principal cells exhibiting place-specific firing patterns in particular locations. The presence of such cells has led to the hypothesis that the hippocampus is the locus of the “where” element of episodic memory (O’Keefe and Dostrovsky, 1971). Following on from this seminal finding, more recent studies have demonstrated that hippocampal place cell activity simultaneously represents a broad range of aspects of memory, including odors and their match/non-match status in a particular location, called the “place field”, as well as elapsed time (Otto and Eichenbaum, 1992; Sakurai, 1996; Wood et al, 1999; Pastalkova et al, 2008; MacDonald et al, 2011). Place cell activity sequences in rodents convey information on both familiar paths and accompanying subtasks (Allen et al, 2012; Takahashi, 2013)

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