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

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.

DOI: http://dx.doi.org/10.7554/eLife.08105.001

eLife digest

Place cells are neurons that respond to a particular location in the physical world. For example, as a rat runs around a maze, some place cells will become active when the rat reaches one corner. When the rat moves on towards a different corner, other place cells activate instead. The real-time activity of these place cells helps the rat to work out where it is in the maze. This activity also contains information about what the rat is doing.

In addition to their real-time activity, place cells also help previous events to be ‘replayed’ mentally, which is important for making decisions. Previous studies have shown that when a rat pauses during a task, place cell replays allow it to mentally map out the route it needs to take. However, it is less clear whether these replays also provide information about what the rat needs to do.

Takahashi gave rats a number of tasks to perform inside a figure of eight maze. In one of these tasks, the rat had to assess which one of two lights was lit up, and run towards it. In the other two tasks, the rat had to remember the direction it took on the previous occasion, and go in the opposite direction. During these tasks, the rat would occasionally pause to replay information about the task.

Takahashi recorded what the rats' place cells were doing during these pauses, and found that the place cell replays contained information about both the path the rat needed to take (‘where and when’ information), and which task it needed to carry out (‘what’ information). This suggests that replays are important for the ability to recall information about specific events, which is known as episodic memory. Takahashi's results may therefore also help us to learn more about this “mental time travel” and human conditions that damage episodic memory, such as Alzheimer's disease.

DOI: http://dx.doi.org/10.7554/eLife.08105.002