Hippocampal Replay Is Not a Simple Function of Experience

Replay of behavioral sequences in the hippocampus during sharp wave ripple complexes (SWRs) provides a potential mechanism for memory consolidation and the learning of knowledge structures. Current hypotheses imply that replay should straightforwardly reflect recent experience. However, we find these hypotheses to be incompatible with the content of replay on a task with two distinct behavioral sequences (A and B). We observed forward and backward replay of B even when rats had been performing A for >10 min. Furthermore, replay of nonlocal sequence B occurred more often when B was infrequently experienced. Neither forward nor backward sequences preferentially represented highly experienced trajectories within a session. Additionally, we observed the construction of never-experienced novel-path sequences. These observations challenge the idea that sequence activation during SWRs is a simple replay of recent experience. Instead, replay reflected all physically available trajectories within the environment, suggesting a potential role in active learning and maintenance of the cognitive map.

Anoopum S. Gupta, Matthijs A.A. van der Meer, David S. Touretzky, A. David Redish. Hippocampal Replay Is Not a Simple Function of Experience. Neuron, Volume 65, Issue 5, 695-705, 11 March 2010

And here’s an interesting detail from the discussion section of the paper:

Furthermore, during left-only and right-only half-
sessions, trajectories along the nonrecent (opposite-side) loop
were replayed with a similar frequency to trajectories on the
recent (same-side) loop. This observation was in contrast to
alternation half-sessions in which opposite-side loops were re-
played less frequently. These observations indicate that current
proposals for potential mechanisms of replay that rely on
recency or frequency of experience are inadequate.

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