Selective engram coreactivation in idling brain inspires implicit learning

Abstract

Passive priming of prior knowledge to assimilate ongoing experiences underlies advanced cognitive processing. However, the necessary neural dynamics of memory assimilation remains elusive. Uninstructed brain could also show boosted creativity, particularly after idling states, yet it remains unclear whether the idling brain can spontaneously spark relevant knowledge assimilations. We established a paradigm that links/separates context-dependent memories according to geometrical similarities. Mice exploring one of four contexts 1 d before undergoing contextual fear conditioning in a square context showed a gradual fear transfer to preexposed geometrically relevant contexts the next day, but not after 15 min. Anterior cingulate cortex neurons representing relevant, rather than distinct, memories were significantly coreactivated during postconditioning sleep only, before their selective integration the next day during testing. Disrupting sleep coreactivations prevented assimilation while preserving recent memory consolidation. Thus, assimilating pertinent memories during sleep through coreactivation of their respective engrams represents the neural underpinnings of sleep-triggered implicit cortical learning.