Experience reorganizes content-specific memory traces in macaques

Abstract

Memory formation relies on the reorganization of neural activity patterns during experience that persist in subsequent sleep. How these processes promote learning while preserving established memories remains unclear. We recorded neural ensemble activity from hippocampal and associated regions in freely moving macaques as they recalled item sequences presented that day ("new"), one day prior ("recent"), or over two weeks prior ("old"). Cell assemblies biased for old sequences showed less drift, greater network connectivity, and stronger sleep reactivation than new-biased assemblies. Pairs of old and recent assemblies formed persistent task-to-sleep coupling ("metassemblies"), unlike new assembly pairs. In the hippocampus, the propensity for superficial and deep CA1 pyramidal cells to form integrated assemblies increased with memory age. These findings reveal rapid organization and stabilization of neural activity in the primate brain, suggesting potential mechanisms for balancing learning with memory linking and durability.