Ongoing brain state dynamics shape spontaneous awake reactivation and its relationship with memory

Abstract

Memory reactivation is thought to support memory consolidation, but how ongoing brain states shape awake reactivation and its relationship to memory remain poorly understood. Here, we asked whether spontaneous hippocampal-cortical reactivation during awake rest is embedded in ongoing brain state dynamics by examining its coupling with whole-brain activity patterns and infra-slow global signal (GS) fluctuations, and whether these dynamics shape its relationship to memory retention. Reactivation preferentially occurred during an internally oriented brain state characterized by default mode network activation and dorsal attention network suppression, as well as states that reinstated encoding-related visual activity. Reactivation also clustered around the peak of infra-slow GS fluctuations and in high GS amplitude time windows, features previously associated with lower arousal. Importantly, the relationship between reactivation and memory depended on the ongoing brain state: distinct whole-brain activity patterns expressed during reactivation were associated with opposing memory outcomes, while reactivation during high GS amplitude windows was positively associated with retention. Together, these findings show that awake memory reactivation is embedded in dynamic whole-brain states that may influence its memory outcome, suggesting that recurring brain states may provide favorable windows for awake memory consolidation.