Relationship Between Sleep Maturation and Brain Structural Growth in Infants from Birth to 27 Months

Poster No:

942 

Submission Type:

Abstract Submission 

Authors:

Yiding Gui1, Weiyan Yin2, Zhengwang Wu3, Gang Li3, Li Wang3, Seoyoon Cho1, Tengfei Li3, Guanghai Wang4, Yujiao Deng4, Fan Jiang4, Weili Lin2

Institutions:

1University of North Carolina at Chapel Hill, Chapel hill, NC, 2UNC Chapel Hill, Chapel Hill, NC, 3UNC-CH, CHAPEL HILL, NC, 4Shanghai Children's Medical Center, Shanghai, Shanghai

First Author:

Yiding Gui  
University of North Carolina at Chapel Hill
Chapel hill, NC

Co-Author(s):

Weiyan Yin  
UNC Chapel Hill
Chapel Hill, NC
Zhengwang Wu  
UNC-CH
CHAPEL HILL, NC
Gang Li  
UNC-CH
CHAPEL HILL, NC
Li Wang  
UNC-CH
CHAPEL HILL, NC
Seoyoon Cho  
University of North Carolina at Chapel Hill
Chapel hill, NC
Tengfei Li  
UNC-CH
CHAPEL HILL, NC
Guanghai Wang  
Shanghai Children's Medical Center
Shanghai, Shanghai
Yujiao Deng  
Shanghai Children's Medical Center
Shanghai, Shanghai
Fan Jiang  
Shanghai Children's Medical Center
Shanghai, Shanghai
Weili Lin  
UNC Chapel Hill
Chapel Hill, NC

Introduction:

Sleep, one of the most crucial activities during infancy, plays a fundamental role in early development. The first two years represent a critical period for sleep development, when children develop adult-like sleep patterns. Concurrently, the brain also undergoes rapid development during this time, reaching 80-90% of the adult volume. While previous studies have highlighted the close interplay of sleep and brain maturation, few have explored the neural correlatives between sleep and brain structural development in infancy. We leveraged the rich data collected by the Baby Connectome Project (BCP) to investigate the relationships between sleep and brain structural development in 0-to-27-month-olds.

Methods:

218 infants (460 visits) from the BCP cohort were included (Howell et al., 2019). Sleep was assessed using the Brief Infant Sleep Questionnaire (Sadeh, 2004), including total sleep duration, sleep onset latency, and night waking numbers. Brain images were processed using the iBEAT toolbox (Wang et al., 2023) and aligned to the UNC 4D infant cortical surface atlases. Cortical volume and cortical thickness (CT) (surface-based analysis) and subcortical volumes (volume-based analysis) were outcome measures.
General additive models were used to control for age effects for all sleep and brain metrics. Subjects were grouped into three age groups (0-6, 6-12, 12-27 months), reflecting key developmental stages. Linear mixed-effect models were used by controlling the sex, site, race, gestational age, maternal education, household income, breastfed or not, and intracranial volume. All reported p-values in the Results section were FDR corrected for multiple comparisons.

Results:

All sleep metrics declined rapidly in the first 6 months, followed by a continuing decline but with a slower pace, consistent with results reported in the literature (Galland et al., 2012),. (Figure1).
Age specific associations between brain structural phenotypes and sleep parameters were observed. Total sleep duration was positively associated with whole brain average CT (β=0.01, p=0.042) (Figure 2A) during the first 6 months of life. More specifically, 19 of 70 cortical regions were positively associated with total sleep duration (p<0.05, Figure 2B). In addition, CT of the left lingual cortex (β=0.130, p=0.034) and right cuneus cortex (β=0.107, p=0.034) were significantly positively correlated with sleep onset latency.
In 6-to-12-month-olds, night-waking number was negatively correlated with subcortical volumes, including the bilateral putamen (Left β=-49.65, p=0.047; Right β=-50.87, p=0.046), right hippocampus (β=-33.89, p<0.001), and right amygdala (β=-9.71, p=0.030). In contrast, night-waking number was positively associated with the right pars orbitalis cortex (β=48.90, P=0.048).
Finally, no significant association between sleep and brain structural measurements was found in 12-to-27-month-olds.
Supporting Image: Figure1.png
   ·Figure 1. Infant sleep development from 0 to 27 months
Supporting Image: Figure2.png
   ·Figure 2. Association between infant sleep metrics and brain structural development in 0-to-6-month-olds
 

Conclusions:

Our findings revealed age-specific associations between sleep maturation and early brain development. Cortical thickness, reflecting synaptic density, develops most rapidly in the first six months and correlated with total sleep duration, underscoring its roles in synaptogenesis during this critical period (Li et al., 2017). In addition, sleep onset latency is associated with CT of the cuneus and lingual gyrus implicated in sensory gating and visual processing, highlighting the roles of sleep initiation and visual functional development. After 6 months, night-waking is associated with the development of the putamen, amygdala, and hippocampus, which have been shown to undergo rapid increase in volume during this period (Chen et al., 2023). Together, our results highlights the importance of sleep health to early brain development during a critical period of early brain development.

Lifespan Development:

Early life, Adolescence, Aging 1
Normal Brain Development: Fetus to Adolescence

Neuroanatomy, Physiology, Metabolism and Neurotransmission:

Normal Development

Perception, Attention and Motor Behavior:

Sleep and Wakefulness 2

Keywords:

Cortex
Development
PEDIATRIC
Sleep

1|2Indicates the priority used for review

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Provide references using APA citation style.

Chen, L., Wang, Y., Wu, Z., Shan, Y., Li, T., Hung, S.-C., Xing, L., Zhu, H., Wang, L., Lin, W., & Li, G. (2023). Four-dimensional mapping of dynamic longitudinal brain subcortical development and early learning functions in infants. Nature Communications, 14(1), 3727.
Galland, B. C., Taylor, B. J., Elder, D. E., & Herbison, P. (2012). Normal sleep patterns in infants and children: A systematic review of observational studies. Sleep Medicine Reviews, 16(3), 213–222.
Howell, B. R., Styner, M. A., Gao, W., Yap, P.-T., Wang, L., Baluyot, K., Yacoub, E., Chen, G., Potts, T., Salzwedel, A., Li, G., Gilmore, J. H., Piven, J., Smith, J. K., Shen, D., Ugurbil, K., Zhu, H., Lin, W., & Elison, J. T. (2019). The UNC/UMN Baby Connectome Project (BCP): An overview of the study design and protocol development. NeuroImage, 185, 891–905.
Knickmeyer, R. C., Gouttard, S., Kang, C., Evans, D., Wilber, K., Smith, J. K., Hamer, R. M., Lin, W., Gerig, G., & Gilmore, J. H. (2008). A Structural MRI Study of Human Brain Development from Birth to 2 Years. The Journal of Neuroscience, 28(47), 12176–12182.
Li, W., Ma, L., Yang, G., & Gan, W.-B. (2017). REM sleep selectively prunes and maintains new synapses in development and learning. Nature Neuroscience, 20(3), 427–437.
Sadeh, A. (2004). A Brief Screening Questionnaire for Infant Sleep Problems: Validation and Findings for an Internet Sample. Pediatrics, 113(6), e570–e577.
Wang, L., Wu, Z., Chen, L., Sun, Y., Lin, W., & Li, G. (2023). iBEAT V2.0: A multisite-applicable, deep learning-based pipeline for infant cerebral cortical surface reconstruction. Nature Protocols, 18(5), 1488–1509.

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