Electroencephalographic sleep macrostructure and sleep spindles in early infancy

Soraia Ventura, Sean R Mathieson, John M O'Toole, Vicki Livingstone, Mary-Anne Ryan, Geraldine B Boylan, Soraia Ventura, Sean R Mathieson, John M O'Toole, Vicki Livingstone, Mary-Anne Ryan, Geraldine B Boylan

Abstract

Study objectives: Sleep features in infancy are potential biomarkers for brain maturation but poorly characterized. We describe normative values for sleep macrostructure and sleep spindles at 4-5 months of age.

Methods: Healthy term infants were recruited at birth and had daytime sleep electroencephalograms (EEGs) at 4-5 months. Sleep staging was performed and five features were analyzed. Sleep spindles were annotated and seven quantitative features were extracted. Features were analyzed across sex, recording time (am/pm), infant age, and from first to second sleep cycles.

Results: We analyzed sleep recordings from 91 infants, 41% females. Median (interquartile range [IQR]) macrostructure results: sleep duration 49.0 (37.8-72.0) min (n = 77); first sleep cycle duration 42.8 (37.0-51.4) min; rapid eye movement (REM) percentage 17.4 (9.5-27.7)% (n = 68); latency to REM 36.0 (30.5-41.1) min (n = 66). First cycle median (IQR) values for spindle features: number 241.0 (193.0-286.5), density 6.6 (5.7-8.0) spindles/min (n = 77); mean frequency 13.0 (12.8-13.3) Hz, mean duration 2.9 (2.6-3.6) s, spectral power 7.8 (4.7-11.4) µV2, brain symmetry index 0.20 (0.16-0.29), synchrony 59.5 (53.2-63.8)% (n = 91). In males, spindle spectral power (µV2) was 24.5% lower (p = .032) and brain symmetry index 24.2% higher than females (p = .011) when controlling for gestational and postnatal age and timing of the nap. We found no other significant associations between studied sleep features and sex, recording time (am/pm), or age. Spectral power decreased (p < .001) on the second cycle.

Conclusion: This normative data may be useful for comparison with future studies of sleep dysfunction and atypical neurodevelopment in infancy. Clinical Trial Registration: BABY SMART (Study of Massage Therapy, Sleep And neurodevelopMenT) (BabySMART)URL: https://ichgcp.net/clinical-trials-registry/NCT03381027?view=results.ClinicalTrials.gov Identifier: NCT03381027.

Keywords: EEG; NREM; REM; infant; macrostructure; nap; neurodevelopment; sleep; spindles.

© Sleep Research Society 2021. Published by Oxford University Press on behalf of the Sleep Research Society.

Figures

Figure 1.
Figure 1.
Flow diagram detailing numbers of participants in analysis.
Figure 2.
Figure 2.
N1 sleep stage with its characteristic relative low amplitude and mixed frequencies and slow eye movement (intrusion of frontal activity is present on the EOG channels). Incipient vertex sharp waves are present in the central regions. Gridlines represent 10 s-intervals. Power spectrum density (PSD) window on top of the EEG represent spectral power of frequencies from 0.5 to 30 Hz (y axis) across the approximately 1 h of recording (x axis). Red colors represent the highest spectral power for a particular frequency and time on the spectrum; colors close to dark blue represent the lower spectral power.
Figure 3.
Figure 3.
N2 sleep stage. Sleep spindles marked the onset of this epoch. Top EEG: timebase = 1.5 cm/s, gridlines correspond to 10 s intervals. Bottom EEG: detail of the previous page to evidence spindles, timebase = 3cm/s, gridlines correspond to 1 s intervals. Right and left fronto-central sleep spindles in yellow.
Figure 4.
Figure 4.
N3 sleep stage. High amplitude slow waves are a hallmark of this stage (intrusions of frontal high amplitude activity present on the EOG channels). Top EEG: timebase =1.5cm/s, gridlines denote 10 s intervals. Bottom EEG: detail of the previous page, timebase = 3cm/s, gridlines denote 1 s intervals.
Figure 5.
Figure 5.
REM sleep stage with relatively low amplitude activities, accompanying conjugate rapid eye movements, irregular respiration rate and lower chin EMG.
Figure 6.
Figure 6.
Distribution of sleep spindle frequencies (Hz) from all sleep cycles recorded.

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