Sleep spindle maturation enhances slow oscillation-spindle coupling

Abstract The synchronization of canonical fast sleep spindle activity (12.5-16 Hz) precisely during the slow oscillation up peak is considered an essential feature of adult non-rapid eye movement sleep. However, there is little knowledge on how this well-known coalescence between slow oscillations and sleep spindles develops. Leveraging individualized detection of single events, we first provide a detailed cross-sectional characterization of age-specific patterns of slow and fast sleep spindles, slow oscillations, and their coupling in children aged 5 to 6, 8 to 11, and 14 to 18 years. Critically, based on this, we then investigated how spindle and slow oscillation maturity substantiate age differences in their precise orchestration. While the predominant type of fast spindles was development-specific in that it was still nested in a frequency range below the canonical fast spindle range for the majority of children, the well-known slow oscillation-spindle coupling pattern was evident for sleep spindles in the canonical (adult-like) fast spindle range in all three age groups – but notably less precise in children. To corroborate these findings, we linked personalized measures of fast spindle maturity, which indicate the similarity between the prevailing development-specific and adult-like fast spindles, and slow oscillation maturity, which reflects the extent to which slow oscillations show frontal dominance, with individual slow oscillation-spindle coupling patterns. Importantly, we found that fast spindle maturity was uniquely associated with enhanced slow oscillation-spindle coupling strength and precision. Taken together, our results suggest that the increasing ability to generate canonical fast sleep spindles actuates precise slow oscillation-spindle coupling patterns across child and adolescent development.