Preplay of future place cell sequences by hippocampal cellular assemblies

Abstract

During spatial exploration, hippocampal neurons show a sequential firing pattern in which individual neurons fire specifically at particular locations along the animal’s trajectory (place cells1, 2). According to the dominant model of hippocampal cell assembly activity, place cell firing order is established for the first time during exploration, to encode the spatial experience, and is subsequently replayed during rest3, 4, 5, 6 or slow-wave sleep7, 8, 9, 10 for consolidation of the encoded experience11, 12. Here we report that temporal sequences of firing of place cells expressed during a novel spatial experience occurred on a significant number of occasions during the resting or sleeping period preceding the experience. This phenomenon, which is called preplay, occurred in disjunction with sequences of replay of a familiar experience. These results suggest that internal neuronal dynamics during resting or sleep organize hippocampal cellular assemblies13, 14, 15 into temporal sequences that contribute to the encoding of a related novel experience occurring in the future.