EXPERIENCE-DEPENDENT ALTERATIONS OF HIPPOCAMPAL-NEOCORTICAL DIALOGUE

During sleep, the brain autonomously restructures network connectivity to support the consolidation of new memories. Current models of systems consolidation hypothesize that newly acquired experiences are encoded by co-active ensembles in the hippocampus during wake and later reactivated during high-frequency hippocampal network oscillations known as sharp wave ripples (SPW-Rs). However, the mechanistic details of how the hippocampus and cortex jointly coordinate systems-wide reactivations during sleep are not yet known. Here, we combined CA1 silicon probe recordings with widefield calcium imaging across the dorsal cortex in sleeping mice to show that SPW-Rs are associated with transient learning-dependent segregation of neocortical functional networks. We identified two dominant cortical domains corresponding to default mode and somatomotor networks. SPW-R-centered analyses revealed increased default-mode activity and rapid reorganization of functional connectivity, characterized by strengthened within-network correlations and reduced cross-network coupling. Following acquisition of a novel spatial task, ripple-associated network segregation was significantly enhanced, producing stronger reductions in between-network coupling during post-learning sleep. Together, these data suggest that SPW-Rs create privileged time windows for the broadcast of behaviorally relevant hippocampal content to cortical memory networks engaged in default mode dynamics during consolidation. From a complementary learning systems perspective, transient network segregation may protect against catastrophic interference by restricting when and where hippocampal information is broadcast to the cortex. By limiting cross-network coupling during early consolidation, SPW-Rs could enable gradual integration of new traces without disrupting established cortical representations.