HIPPOCAMPUS AND VISUAL CORTEX REACTIVATE COHERENT CONTEXTUAL INFORMATION DURING SLEEP

Memory consolidation depends on coordinated communication between the hippocampus and neocortex during sleep. Hippocampal sharp-wave ripples (SWRs) are synchronous population events that are believed to drive reactivation of relevant information in cortical regions. Cortical oscillations during sleep, including spindles and slow-oscillations, are thought to provide windows of elevated cortical excitability to communicate with the hippocampus. However, when multiple memories compete for consolidation, how do cortex and hippocampus reactivate distinct experiences? Is reactivation content modulated by cortical oscillations?

To address this, we used Neuropixel probes to simultaneously record bilaterally from primary visual cortices (V1) and hippocampi (HPC) in head-fixed mice navigating two virtual linear tracks, followed by sleep. Each track was restricted to one visual hemifield, such that a track is biased to be represented in one V1 hemisphere. We calculated the relative likelihood of tracks being reactivated during individual SWR events in HPC and V1, based on population decoding.

We found that hippocampal and V1 populations tend to coherently reactivate the same context during SWRs, especially during high-power SWR events. The reactivation coherence was higher for SWRs occurring during periods of high spindle power and during the slow-oscillations trough phase. Interestingly, cortical activity preceding SWRs predicted the subsequent hippocampal reactivation content, especially when the slow-oscillations trough phase was unique to the context-matching V1 hemisphere, possibly reflecting a bias in the pre-SWR cortical input into HPC.

These results reveal how ongoing cortical oscillations shape reactivation content across the hippocampus and V1, providing a mechanistic insight into selective memory consolidation.