The Impact of Insufficient Sleep on White Matter Development in Late Childhood and Early Adolescence.

Abstract

Purpose: Sleep is vital for brain development. Animal models have suggested that insufficient sleep affects axons and dendrites (known as neurites). However, the effects of insufficient sleep on neurites during brain development in humans remain understudied. Deriving neurite density index and orientation dispersion index (ODI) in a large sample (N = 1,016; 47.44% girls), we aimed to identify the effects of insufficient sleep on white matter development between late childhood (mean age [standard deviation] = 9.96 [0.62] years) and early adolescence (mean age [standard deviation] = 11.94 [0.64] years).

Methods: Longitudinal Latent Class Analysis was used to derive longitudinal classes based on sleep duration from the Sleep Disturbance Scale for Children. The Child Behavior Checklist characterized behavioral (internalizing: anxious/depressed, withdrawn/depressed, somatic; externalizing: social, thought, attention, rule-breaking, and aggressive) problems. Regression analyses evaluated the effects of sleep classes on neurite density index, ODI, and standard tensor-based metrics (Fractional Anisotropy) changes over time, the focal or widespread effects along the tracts, and whether these effects were associated with behavioral problems.

Results: Insufficient (<9 hours; N = 569) and sufficient sleep (>9 hours; N = 447) groups were identified. Insufficient sleep was associated with worsening fiber coherence (greater ODI) in most tracts, including cingulum bundle (F_(1,982) = 9.22, p = .002, Q = 0.009), forceps minor (F_(1,982) = 5.30, p = .021, Q = 0.026), and superior longitudinal fasciculus (F_(1,982) = 7.41, p = .007, Q = 0.015). These effects were focal, particularly in the frontal portions of the tracts. No other metric was affected (p > .050). In addition, greater ODI in the cingulum bundle was associated with more anxious/depressed problems (β = 0.10, p = .012, Q = 0.036).

Discussion: Our findings suggest that insufficient sleep during this sensitive period affects white matter development, which in turn affects internalizing problems. Our findings support the importance of promoting sufficient sleep during early adolescence.