Multistability of cognitive maps in the hippocampus of old rats

Hippocampal neurons provide a population code for location(1). In young rats, environments are reliably 'mapped' by groups of neurons that have firing locations ('place fields'(2)) that can be stable for several months(3). Old animals exhibit deficits in spatial memory, raising the question of whether the quality or stability of their hippocampal 'cognitive maps'(4) is altered. By recording from large groups of neurons, we observed the hippocampal spatial code to be multistable. In young rats, the place field maps were reliable both within and between episodes in a familiar environment. In old rats, place field maps were accurate and stable during an episode, but frequently exhibited complete rearrangements between episodes. In a spatial memory task, both young and old rats exhibited bimodal performance, consistent with map multistability early in training. However, the performance of young rats became almost unimodal with further training, whereas that of old rats remained markedly bimodal. The multistability of the hippocampal map provides an insight into the dynamics of neural coding in high-level cortical structures and their changes during ageing, and may provide an explanation for the frequent failure of place recognition in elderly humans.