Across-night dynamics in traveling sleep slow waves throughout childhood

Abstract

Study objectives: Sleep slow waves behave like traveling waves and are thus a marker for brain connectivity. Across a night of sleep in adults, wave propagation is scaled down, becoming more local. Yet, it is unknown whether slow wave propagation undergoes similar across-night dynamics in childhood-a period of extensive cortical rewiring.

Methods: High-density electroencephalography (EEG; 128 channels) was recorded during sleep in three groups of healthy children: 2.0-4.9 years (n = 11), 5.0-8.9 years (n = 9) and 9.0-16.9 years (n = 9). Slow wave propagation speed, distance, and cortical involvement were quantified. To characterize across-night dynamics, the 20% most pronounced (highest amplitude) slow waves were subdivided into five time-based quintiles.

Results: We found indications that slow wave propagation distance decreased across a night of sleep. We observed an interesting interaction of across-night slow wave propagation dynamics with age (p < 0.05). When comparing the first and last quintiles, there was a trend level difference between age groups: 2- to 4.9-year-old children showed an 11.9% across-night decrease in slow wave propagation distance, which was not observed in the older two age groups. Regardless of age, cortical involvement decreased by 10.4%-23.7% across a night of sleep. No across-night changes were observed in slow wave speed.

Conclusions: Findings provide evidence that signatures of brain connectivity undergo across-night dynamics specific to maturational periods. These results suggest that across-night dynamics in slow wave propagation distance reflect heightened plasticity in underlying cerebral networks specific to developmental periods.

Figure 1.

Slow wave propagation metrics. Slow wave propagation was quantified with three key metrics: slow wave distance, slow wave speed and cortical involvement.

Figure 2.

Number of slow waves detected in each age group: between 813 and 7281 waves were detected (813–4845 excluding the outlier). 9- to 16.9-year-olds exhibited significantly more slow waves compared to 2- to 4.9-year-olds or 5- to 8.9-year-old children (p = 0.02). *p < 0.05; **p < 0.01; N = 29; “ns” not significant, N=29.

Figure 3.

Across-night changes in slow wave propagation. (A) Slow wave distance decreased from the first to the last quintile in 2- to 4.9-year-old children (by 11.9%) but not in 5- to 8.9-year-old children and 9- to 16.9-year-olds. (B) Across-night decreased in cortical involvement across the night independent of age. (C) Across-night dynamics in slow wave speed. There was a trend for an age × quintile interaction; however, no group differences were found in changes from the first to the last quintile. The shaded area represents the SEM. *p < 0.05; n = 29.

Figure 4.

Slow wave whole night mean data. (A) 9- to 16.9-year-olds exhibited significantly longer slow wave propagation distance than 2- to 4.9-year-old children. (B) No significant difference was apparent between age groups in slow wave cortical involvement, yet a trend was observed for increased cortical involvement in 9- to 16.9-year-olds compared to 5- to 8.9-year-old children. (C) Slow wave speed differed between 2- to 4.9-year-olds and 5- to 8.9-year-old children at trend level. Mean ± SEM is shown. *p = 0.05; **p < 0.01; N = 29.