Spatiotemporal dynamics of sleep spindles form spiral waves that predict overnight memory consolidation and age-related memory decline

A growing body of evidence has demonstrated that sleep spindles occurring during stage 2 non-rapid-eye-movement (N2) sleep often organize into travelling waves, but the spatiotemporal dynamics of these waves and their functional significance remain unclear. Using high-density electroencephalogram recordings in humans, we demonstrate that N2 sleep spindles frequently form travelling spiral waves, primarily concentrated in the frontoparietal cortices and symmetrically distributed across hemispheres. These spiral waves display rich spatiotemporal dynamics, rotating around phase singularity centers while propagating across the cortex. We find that the propagation trajectories of these spiral waves exhibit two distinct types of behaviour: while some spirals undergo long-range propagation, traversing considerable distances across the cortex, others remain confined to local regions. We illustrate remarkable consistency in the distribution of these trajectories, which repeat across N2 epochs in hours-long recording sessions and remain consistent over a three-month period. Crucially, the consistency of these trajectories can reliably predict subjects' overnight memory retention performance in a word-pair association task, with greater consistency predicting better performance. Additionally, we find a progressive decrease in trajectory consistency with age, proposing these spiral waves as a potential biomarker for aging. Together, our findings indicate that spiral waves are a defining spatiotemporal feature of N2 sleep and play a crucial role in memory consolidation, offering a promising avenue for further research into sleep-dependent memory processing.