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Research ArticleResearch Article: New Research, Development

Sex and Pubertal Differences in the Maturational Trajectories of Sleep Spindles in the Transition from Childhood to Adolescence: A Population-Based Study

Anna Ricci, Fan He, Susan L. Calhoun, Jidong Fang, Alexandros N. Vgontzas, Duanping Liao, Edward O. Bixler, Magdy Younes and Julio Fernandez-Mendoza
eNeuro 24 June 2021, 8 (4) ENEURO.0257-21.2021; https://doi.org/10.1523/ENEURO.0257-21.2021
Anna Ricci
1Sleep Research and Treatment Center, Department of Psychiatry and Behavioral Health, Penn State College of Medicine, Hershey, PA17033
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Fan He
2Department of Public Health Sciences, Penn State College of Medicine, Hershey, PA17033
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Susan L. Calhoun
1Sleep Research and Treatment Center, Department of Psychiatry and Behavioral Health, Penn State College of Medicine, Hershey, PA17033
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Jidong Fang
1Sleep Research and Treatment Center, Department of Psychiatry and Behavioral Health, Penn State College of Medicine, Hershey, PA17033
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Alexandros N. Vgontzas
1Sleep Research and Treatment Center, Department of Psychiatry and Behavioral Health, Penn State College of Medicine, Hershey, PA17033
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Duanping Liao
2Department of Public Health Sciences, Penn State College of Medicine, Hershey, PA17033
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Edward O. Bixler
1Sleep Research and Treatment Center, Department of Psychiatry and Behavioral Health, Penn State College of Medicine, Hershey, PA17033
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Magdy Younes
3Sleep Disorders Centre, University of Manitoba, Winnipeg, ManitobaR3M 0A7, Canada
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Julio Fernandez-Mendoza
1Sleep Research and Treatment Center, Department of Psychiatry and Behavioral Health, Penn State College of Medicine, Hershey, PA17033
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Article Figures & Data

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  • Figure 1.
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    Figure 1.

    Cross-sectional trajectories of sleep spindles and sigma power in 572 subjects aged 6–21. Data points are multivariable-adjusted means and their 95% CI and lines are multivariable-adjusted regression curves for sleep spindle and sigma activity. A, Spindle density (# of spindles/minute) overall. B, Spindle density stratified by sex. C, Spindle frequency (Hz) overall. D, Spindle frequency stratified by sex. E, Fast spindle percent (% of spindles in the 12–16 Hz range) overall. F, Fast spindle percent stratified by sex. G, Spindle power (μV2) overall. H, Spindle power stratified by sex. I, Sigma power (μV2) overall. J, Sigma power stratified by sex.

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    Figure 2.

    Sex (left column) and Tanner-related (right column) differences in the longitudinal trajectories of sleep spindles and sigma power in 332 subjects aged 5–12 at baseline followed-up at ages 12–22. Data are multivariable-adjusted percent change (95% CI) from baseline to follow-up in sleep spindle and sigma activity. Age groups represent transitions between baseline age (mean) 6.6 years to follow-up ages 12–14, from 8.7 years to ages 15–17, and from 10.3 years to ages 18–22. A, Spindle density stratified by sex. B, Spindle frequency stratified by sex. C, Fast spindle percent stratified by sex. D, Spindle power stratified by sex. E, σ power stratified by sex. F, Spindle density stratified by Tanner stage. G, Spindle frequency stratified by Tanner stage. H, Fast spindle percent stratified by Tanner stage. I, Spindle power stratified by Tanner stage. J, σ power stratified by Tanner stage. *p < 0.05, **p < 0.01.

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    Table 1

    Characteristics of the cross-sectional and longitudinal samples

    Cross-sectionalaLongitudinal (N = 332)b
    (N = 572)BaselineFollow-up
    Sex
     Male300 (52.4%)178 (53.6%)178 (53.6%)
     Female272 (47.6%)154 (46.4%)154 (46.4%)
    Race/ethnicity
     Non-Hispanic White424 (74.1%)252 (75.9%)252 (75.9%)
     Racial/ethnic minority148 (25.9%)80 (24.1%)80 (24.1%)
    Age
     52 (0.3%)6 (1.8%)
     632 (5.6%)35 (10.5%)
     738 (6.6%)53 (16.0%)
     848 (8.4%)51 (15.4%)
     932 (5.6%)72 (21.7%)
     1036 (6.3%)57 (17.2%)
     1128 (4.9%)51 (15.4%)
     1213 (2.3%)7 (2.1%)8 (2.4%)
     1327 (4.7%)27 (8.1%)
     1440 (7.0%)40 (12.0%)
     1550 (8.7%)51 (15.4%)
     1659 (10.3%)58 (17.5%)
     1753 (9.3%)51 (15.4%)
     1846 (8.0%)45 (13.6%)
     1931 (5.4%)27 (8.1%)
     2021 (3.7%)15 (4.5%)
     218 (1.4%)7 (2.1%)
     22
     23
    7 (1.2%)
    1 (0.2%)
    3 (0.9%)
    BMI percentile
     Normal weight373 (65.2%)232 (69.9%)225 (67.8%)
     Overweight113 (19.8%)36 (10.8%)61 (18.4%)
     Obese86 (15.0%)64 (19.3%)46 (13.9%)
    Behavioral disorders
     None449 (78.5%)274 (82.5%)248 (74.7%)
     Yes123 (21.5%)58 (17.5%)84 (25.3%)
    Neurobehavioral measures
     Attention problems, score54.6 (6.6)54.3 (6.4)54.8 (6.6)
     Thought problems, score55.1 (6.6)55.4 (6.9)54.5 (5.8)
     Internalizing problems, score50.5 (10.7)50.6 (10.7)50.4 (10.0)
     Externalizing problems, score48.1 (10.8)48.3 (11.0)48.2 (10.0)
     Verbal IQ, score105.8 (13.2)107.0 (13.2)102.0 (10.4)
     Non-verbal IQ, score106.4 (15.5)108.1 (15.5)106.1 (11.6)
     Coding, scaled score10.3 (3.2)10.6 (3.3)9.8 (2.6)
     Digit span backward, raw score4.5 (1.7)4.6 (1.6)6.9 (2.4)
    PSG
     SOL, min27.4 (22.2)26.8 (22.3)25.0 (20.0)
     WASO, min61.6 (41.0)43.9 (32.9)69.2 (41.1)
     TST, min448.6 (51.3)461.3 (44.3)448.0 (49.8)
     SE, %83.6 (9.3)86.7 (7.6)82.9 (9.1)
     N1, %2.0 (2.7)3.5 (2.6)0.9 (1.1)
     N2, %51.1 (10.9)46.7 (10.8)53.2 (9.4)
     N3, %27.9 (10.1)29.9 (10.5)27.1 (9.0)
     R, %19.0 (5.2)20.1 (5.3)18.8 (4.7)
    AHI, events/h1.9 (4.7)0.8 (1.1)2.5 (5.7)
    • ↵a Data for 572 subjects in cross-sectional analyses.

    • ↵b Data for 332 subjects in longitudinal analyses, including baseline and follow-up.

    • Data are means (SD) and number of cases (percentage) for continuous and categorical/ordinal variables, respectively. AHI = apnea/hypopnea index; BMI = body mass index; N1 = epochs scored as NREM stage 1; N2 = epochs scored as NREM stage 2; N3 = epochs scored as NREM stages 3 or 4; R = epochs scored as REM sleep; SE = sleep efficiency; SOL = sleep onset latency; TST = total sleep time; WASO = wake after sleep onset.

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    Table 2

    Correlation coefficients for sleep spindle/σ activity in the cross-sectional sample (above diagonal) and the longitudinal sample (below diagonal)

    Spindle densitySpindle frequencyFast spindle percentSpindle powerσ power
    Spindle density---0.2050.2630.5530.311
    Spindle frequency0.286---0.931−0.120−0.104
    Fast spindle percent0.3490.564---−0.061−0.106
    Spindle power0.4710.1910.248---0.628
    σ power0.5530.2620.2250.671---
    • Data are Pearson correlation coefficients. For the cross-sectional sample, the correlation coefficients for spindle density (#/min), spindle frequency (Hz), fast spindle percent (%), and spindle and σ power (μV2) were determined. For the longitudinal sample, the correlation coefficients for the percent change in each spindle metric from baseline (ages 5–12) to follow-up (ages 12–22) were calculated.

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Sex and Pubertal Differences in the Maturational Trajectories of Sleep Spindles in the Transition from Childhood to Adolescence: A Population-Based Study
Anna Ricci, Fan He, Susan L. Calhoun, Jidong Fang, Alexandros N. Vgontzas, Duanping Liao, Edward O. Bixler, Magdy Younes, Julio Fernandez-Mendoza
eNeuro 24 June 2021, 8 (4) ENEURO.0257-21.2021; DOI: 10.1523/ENEURO.0257-21.2021

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Sex and Pubertal Differences in the Maturational Trajectories of Sleep Spindles in the Transition from Childhood to Adolescence: A Population-Based Study
Anna Ricci, Fan He, Susan L. Calhoun, Jidong Fang, Alexandros N. Vgontzas, Duanping Liao, Edward O. Bixler, Magdy Younes, Julio Fernandez-Mendoza
eNeuro 24 June 2021, 8 (4) ENEURO.0257-21.2021; DOI: 10.1523/ENEURO.0257-21.2021
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Keywords

  • adolescence
  • brain maturation
  • childhood
  • developmental biology
  • puberty
  • sleep spindles

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