Cortical–hippocampal coupling during manifold exploration in motor cortex

Systems consolidation—a process for long-term memory stabilization—has been hypothesized to occur in two stages(1–4). Whereas new memories require the hippocampus(5–9), they become integrated into cortical networks over time(10–12), making them independent of the hippocampus. How hippocampal–cortical dialogue precisely evolves during this and how cortical representations change in concert is unknown. Here, we use a skill learning task(13,14) to monitor the dynamics of cross-area coupling during non-rapid eye movement sleep along with changes in primary motor cortex (M1) representational stability. Our results indicate that precise cross-area coupling between hippocampus, prefrontal cortex and M1 can demarcate two distinct stages of processing. We specifically find that each animal demonstrates a sharp increase in prefrontal cortex and M1 sleep slow oscillation coupling with stabilization of performance. This sharp increase then predicts a drop in hippocampal sharp-wave ripple (SWR)–M1 slow oscillation coupling—suggesting feedback to inform hippocampal disengagement and transition to a second stage. Notably, the first stage shows significant increases in hippocampal SWR–M1 slow oscillation coupling in the post-training sleep and is closely associated with rapid learning and variability of the M1 low-dimensional manifold. Strikingly, even after consolidation, inducing new manifold exploration by changing task parameters re-engages hippocampal–M1 coupling. We thus find evidence for dynamic hippocampal–cortical dialogue associated with manifold exploration during learning and adaptation.