The formation of an expanding memory representation in the hippocampus

Abstract

AbstractHow episodic memories are stored within brains is poorly understood. While certain memory-retaining neurons have been potentially identified1–3, it is unclear if they retain learned information4,5. Further, there is considerable evidence that neuronal activity is unstable and may require additional mechanisms to support robust memory6–11. To examine these issues, we recorded the activity of a hippocampal CA1 neuronal population for 7 days as mice learned cued reward locations. These data and modelling results suggest that two place cell (PC) pools, distinguished by place field (PF) stability, are formed each day (transient: ~1.5 days; sustained: ~2 weeks)8. Notably, the proportions of these pools changed across the week as unstable transient PCs were progressively replaced by sustained PCs, markedly enhancing the stability of the total representation. This growing stable representation contained behaviorally relevant information and sustained PCs became active immediately at the start of each session. Finally, the initial formation of sustained PCs was associated with a higher rate and efficacy of behavioral timescale synaptic plasticity (BTSP) and these PCs showed elevated and more reliable activity. It, therefore, appears that BTSP stabilizes particularly informative PCs, incorporating them into an expanding and readily retrievable representation that displays hallmarks of a long-lasting memory.