Human Replay Spontaneously Reorganizes Experience

Summary

Knowledge abstracted from previous experiences can be transferred to aid new learning. Here, we asked whether such abstract knowledge immediately guides the replay of new experiences. We first trained participants on a rule defining an ordering of objects and then presented a novel set of objects in a scrambled order. Across two studies, we observed that representations of these novel objects were reactivated during a subsequent rest. As in rodents, human “replay” events occurred in sequences accelerated in time, compared to actual experience, and reversed their direction after a reward. Notably, replay did not simply recapitulate visual experience, but followed instead a sequence implied by learned abstract knowledge. Furthermore, each replay contained more than sensory representations of the relevant objects. A sensory code of object representations was preceded 50 ms by a code factorized into sequence position and sequence identity. We argue that this factorized representation facilitates the generalization of a previously learned structure to new objects.

Graphical Abstract

Highlights

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  As in rodents, human replay occurs during rest and reverses direction after reward

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  As in rodents, human replay coincides with hippocampal sharp-wave ripples

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  Human replay spontaneously reorganizes experience based on learned structure

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  Human replay is factorized, allowing fast structural generalization

Abstract

In the human hippocampus, neural activity known as sequential replay includes both item-specific and generalizable abstract representations and spontaneously reorders sequences to integrate past knowledge with current experiences during rest.