Slow oscillation–spindle coupling strength predicts real-life gross-motor learning in adolescents and adults

Abstract

Previously, we demonstrated that precise temporal coordination between slow oscillations (SOs) and sleep spindles indexes declarative memory network development (Hahn et al., 2020). However, it is unclear whether these findings in the declarative memory domain also apply in the motor memory domain. Here, we compared adolescents and adults learning juggling, a real-life gross-motor task. Juggling performance was impacted by sleep and time of day effects. Critically, we found that improved task proficiency after sleep lead to an attenuation of the learning curve, suggesting a dynamic juggling learning process. We employed individualized cross-frequency coupling analyses to reduce inter- and intragroup variability of oscillatory features. Advancing our previous findings, we identified a more precise SO–spindle coupling in adults compared to adolescents. Importantly, coupling precision over motor areas predicted overnight changes in task proficiency and learning curve, indicating that SO–spindle coupling relates to the dynamic motor learning process. Our results provide first evidence that regionally specific, precisely coupled sleep oscillations support gross-motor learning.

An evolutionary conserved division-of-labor between hippocampal and neocortical sharp-wave ripples organizes information transfer during sleep

“…Slow wave detection. Slow waves were detected on scalp EEG following previously described criteria (Hahn et al, 2022;Hahn et al, 2020;Helfrich et al, 2019;Helfrich et al, 2018;Staresina et al, 2015). Data were high-pass filtered at .16 Hz and subsequently low-pass filtered at 1.25 Hz using a Butterworth IIR filter and filter orders of 2 and 6, respectively.…”

“…1g and h; Fig. 5d and e) was conducted in accordance with the analysis steps of previous studies (Hahn et al, 2022;Hahn et al, 2020;Helfrich et al, 2019;Staresina et al, 2015). Sharp-wave phase angles of the Hilbert transform were determined upon ripple troughs following z-normalization and band-pass filtering (.3 to 2 Hz).…”

Sleep EEG in young people with 22q11.2 deletion syndrome: A cross-sectional study of slow-waves, spindles and correlations with memory and neurodevelopmental symptoms

“…Spindle properties and spindle – SW relationships change across the lifespan ( Djonlagic et al, 2021 ; Hahn et al, 2020 ; Hahn et al, 2022 ; Purcell et al, 2017 ; Zhang et al, 2021 ): spindle density, power and frequency increases from childhood to adolescence alongside spindle-SW coupling, while power in lower frequency declines ( Hahn et al, 2020 ; Jenni and Carskadon, 2004 ; Tarokh and Carskadon, 2010 ). Our findings could therefore be interpreted in the context of alterations in developmental processes in 22q11.2DS: higher spindle amplitude, density, and frequency in young, at-risk populations for psychosis could mark an aberrant maturational state, which leads to reduced spindle activity in adulthood for individuals who go on to develop psychotic disorders, with higher symptom burden and illness duration linked to greater reductions in spindle activity.…”

Sleep EEG in young people with 22q11.2 deletion syndrome: a cross-sectional study of slow-waves, spindles and correlations with memory and neurodevelopmental symptoms

“…Spindle properties and spindle -SW relationships change across the lifespan (Djonlagic et al, 2020;Hahn et al, 2020Hahn et al, , 2022Purcell et al, 2017;Zhang et al, 2021): spindle density, power and frequency increases from childhood to adolescence alongside spindle-SW coupling, while power in lower frequency declines (Hahn et al, 2020;Jenni & Carskadon, 2004;Tarokh & Carskadon, 2010). Our findings could therefore be interpreted in the context of alterations in developmental processes in 22q11.2DS: higher spindle amplitude, density and frequency in young, at-risk populations for psychosis could mark an aberrant maturational state, which leads to reduced spindle activity in adulthood for individuals who go on to develop psychotic disorders, with higher symptom burden and illness duration linked to greater reductions in spindle activity.…”