David Dupret, Joe O'Neill, Barty Pleydell-Bouverie, and Jozsef Csicsvari

The hippocampus is a key brain region for spatial memory. This has been related to the fact that hippocampal principal cells fire in relation to space and these "place cells" collectively provide a map-like representation of the environment, which can be used for solving spatial problems. In order to examine how place cell representations might enable solving spatial memory tasks, we recorded place cell activity in behaving rats during a matching-to-multiple-places task that requires frequent updating of memories for goal locations. The task took place on a cheeseboard maze where rats had to find a set of rewarded wells whose locations changed from day-to-day but stayed fixed within successive learning trials on each day. On each day, rats covered longer distances before finding the rewards during the first trial than in subsequent trials suggesting that rats search for the baited wells on the first trial, while they rapidly encode and remember locations for the remaining trials. The place-related firing patterns in CA1 region reorganised to over-represent the learnt goal locations whereas such reorganisation did not take place in CA3. Moreover the learning-related CA1 population firing patterns representing learnt locations predict memory performances in subsequent memory retention tests. During learning, place cells that encoded goal locations exhibited a higher sharp-wave/ripple associated firing response compared to those place cells that did not encode goal locations. During the post-learning sleep period, the firing patterns of goal-centric cells exhibited stronger reactivation than other place cells and their reactivation predicted subsequent memory performances. Altogether, these results suggest that reorganisation and reactivation of goal-related population firing patterns sustain spatial learning and memory retention abilities.