Origin, synchronization, and propagation of sleep slow waves in children

by Anna Castelnovo, Althea Lividini, Brady A. Riedner, Giulia Avvenuti, Stephanie G. Jones, Silvia Miano, Giulio Tononi, Mauro Manconi and Giulio Bernardi
Abstract:
Study Objectives Sleep slow wave activity, as measured using EEG delta power (<4 Hz), undergoes significant changes throughout development, mirroring changes in brain function and anatomy. Yet, age-dependent variations in the characteristics of individual slow waves have not been thoroughly investigated. Here we aimed at characterizing individual slow wave properties such as origin, synchronization, and cortical propagation at the transition between childhood and adulthood. Methods We analyzed overnight high-density (256 electrodes) EEG recordings of healthy typically developing children (N = 21, 10.3 ± 1.5 years old) and young healthy adults (N = 18, 31.1 ± 4.4 years old). All recordings were preprocessed to reduce artifacts, and NREM slow waves were detected and characterized using validated algorithms. The threshold for statistical significance was set at p = 0.05. Results The slow waves of children were larger and steeper, but less widespread than those of adults. Moreover, they tended to mainly originate from and spread over more posterior brain areas. Relative to those of adults, the slow waves of children also displayed a tendency to more strongly involve and originate from the right than the left hemisphere. The separate analysis of slow waves characterized by high and low synchronization efficiency showed that these waves undergo partially distinct maturation patterns, consistent with their possible dependence on different generation and synchronization mechanisms. Conclusions Changes in slow wave origin, synchronization, and propagation at the transition between childhood and adulthood are consistent with known modifications in cortico-cortical and subcortico-cortical brain connectivity. In this light, changes in slow-wave properties may provide a valuable yardstick to assess, track, and interpret physiological and pathological development.
Reference:
Origin, synchronization, and propagation of sleep slow waves in children (Anna Castelnovo, Althea Lividini, Brady A. Riedner, Giulia Avvenuti, Stephanie G. Jones, Silvia Miano, Giulio Tononi, Mauro Manconi and Giulio Bernardi), In NeuroImage, volume 274, 2023.
Bibtex Entry:
@article{CASTELNOVO2023120133,
    title = {Origin, synchronization, and propagation of sleep slow waves in children},
    journal = {NeuroImage},
    volume = {274},
    pages = {120133},
    year = {2023},
    issn = {1053-8119},
    doi = {https://doi.org/10.1016/j.neuroimage.2023.120133},
    url = {https://www.sciencedirect.com/science/article/pii/S1053811923002847},
    pdf = {file:///Users/jonathanlang/Downloads/1-s2.0-S1053811923002847-main.pdf},
    author = {Anna Castelnovo and Althea Lividini and Brady A. Riedner and Giulia Avvenuti and Stephanie G. Jones and Silvia Miano and Giulio Tononi and Mauro Manconi and Giulio Bernardi},
    keywords = {Development, Maturation, Slow wave activity, SWA, Traveling},
    abstract = {Study Objectives
    Sleep slow wave activity, as measured using EEG delta power (<4 Hz), undergoes significant changes throughout development, mirroring changes in brain function and anatomy. Yet, age-dependent variations in the characteristics of individual slow waves have not been thoroughly investigated. Here we aimed at characterizing individual slow wave properties such as origin, synchronization, and cortical propagation at the transition between childhood and adulthood.
    Methods
    We analyzed overnight high-density (256 electrodes) EEG recordings of healthy typically developing children (N = 21, 10.3 ± 1.5 years old) and young healthy adults (N = 18, 31.1 ± 4.4 years old). All recordings were preprocessed to reduce artifacts, and NREM slow waves were detected and characterized using validated algorithms. The threshold for statistical significance was set at p = 0.05.
    Results
    The slow waves of children were larger and steeper, but less widespread than those of adults. Moreover, they tended to mainly originate from and spread over more posterior brain areas. Relative to those of adults, the slow waves of children also displayed a tendency to more strongly involve and originate from the right than the left hemisphere. The separate analysis of slow waves characterized by high and low synchronization efficiency showed that these waves undergo partially distinct maturation patterns, consistent with their possible dependence on different generation and synchronization mechanisms.
    Conclusions
    Changes in slow wave origin, synchronization, and propagation at the transition between childhood and adulthood are consistent with known modifications in cortico-cortical and subcortico-cortical brain connectivity. In this light, changes in slow-wave properties may provide a valuable yardstick to assess, track, and interpret physiological and pathological development.}
    }