The evolving view of replay and its functions in wake and sleep

The term hippocampal replay originally referred to the temporally compressed reinstantiation, during rest, of sequential neural activity observed during prior active wake. Since its description in the 1990s, hippocampal replay has often been viewed as the key mechanism by which a memory trace is repeatedly rehearsed at high speeds during sleep and gradually transferred to neocortical circuits. However, the methods used to measure the occurrence of replay remain debated, and it is now clear that the underlying neural events are considerably more complicated than the traditional narratives had suggested. “Replay-like” activity happens during wake, can play out in reverse order, may represent trajectories never taken by the animal, and may have additional functions beyond memory consolidation, from learning values and solving the problem of credit assignment to decision-making and planning. Still, we know little about the role of replay in cognition, and to what extent it differs between wake and sleep. This may soon change, however, because decades-long efforts to explain replay in terms of reinforcement learning (RL) have started to yield testable predictions and possible explanations for a diverse set of observations. Here, we (1) survey the diverse features of replay, focusing especially on the latest findings; (2) discuss recent attempts at unifying disparate experimental results and putatively different cognitive functions under the banner of RL; (3) discuss methodological issues and theoretical biases that impede progress or may warrant a partial revaluation of the current literature, and finally; (4) highlight areas of considerable uncertainty and promising avenues of inquiry.