Interplay of sleep neural oscillations enhances coordinated memory reactivation between cortex and hippocampus

Abstract

Memory consolidation during sleep requires coordinated reactivation of specific experiences across hippocampus and cortex. This process occurs with synchronized neural oscillations including cortical slow waves, thalamocortical spindles, and hippocampal sharp-wave ripples. While temporal coupling of these rhythms is implicated in consolidation, a fundamental question remains: do oscillations reflect a general increase in communication, or do they selectively coordinate which memories are reactivated together across regions? Here we segregated competing memory representations in primary visual cortex by training mice on two visually distinct virtual reality tracks, each restricted to one visual hemifield, rendering their representations lateralized in cortex. Using large-scale electrophysiology, we demonstrate that hippocampus and cortex coherently reactivate the same memories. Temporally, the cortical memory trace active before and after a ripple is coherent with the memory hippocampus reactivates. Crucially, this reactivation coherence is maximally enhanced by high hippocampal ripple power in concert with high cortical spindle-band power and slow oscillation trough phase localized to the dominant memory trace reactivating. Our findings establish that sleep oscillations coordinate content-specific cortico-hippocampal reactivation necessary for consolidation.