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. 2024 Nov:109:105384.
doi: 10.1016/j.ebiom.2024.105384. Epub 2024 Oct 30.

Association between prenatal maternal sleep quality, neonatal uncinate fasciculus white matter, and infant negative emotionality

Affiliations

Association between prenatal maternal sleep quality, neonatal uncinate fasciculus white matter, and infant negative emotionality

Melissa Nevarez-Brewster et al. EBioMedicine. 2024 Nov.

Abstract

Background: Poor prenatal maternal sleep is a pervasive, yet modifiable, health concern affecting maternal and foetal wellbeing. Experimental rodent studies demonstrate that prenatal maternal sleep deprivation affects offspring brain development and leads to adverse outcomes, including increased anxiety-like behaviour. We examined the relation between prenatal maternal sleep quality and neonatal white matter development and subsequent infant negative emotionality.

Methods: Participants included 116 mother-infant (53% female) dyads. Prenatal sleep quality was prospectively assessed three times during gestation (16, 29, and 35 gestational weeks) using the Pittsburgh Sleep Quality Index. Neonatal white matter, as indexed by fractional anisotropy (FA), was assessed via diffusion weighted magnetic resonance imaging. Negative emotionality was measured via behavioural observation and maternal report when the infant was 6-months of age.

Findings: More prenatal sleep problems across pregnancy were associated with higher neonatal FA in the uncinate fasciculus (left: b = 0.20, p = .004; right: b = 0.15, p = .027). Higher neonatal uncinate FA was linked to infant negative emotionality, and uncinate FA partially mediated the association between prenatal maternal sleep and behavioural observation of infant negative emotionality.

Interpretation: Findings highlight prenatal sleep as an environmental signal that affects the developing neonatal brain and later infant negative emotionality.

Funding: National Institutes of Health (R01MH109662, R01HL155744, P50HD103573, K12AR084226, F32 Training fellowships MH125572, HL165844, MH106440, and diversity supplement R01HL155744-01S1).

Keywords: Diffusion imaging; Intergenerational transmission; Negative emotionality; Neonatal magnetic resonance imaging; Prenatal sleep; Uncinate fasciculus.

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Conflict of interest statement

Declaration of interests The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

Fig. 1
Fig. 1
Schematic of study timeline.
Fig. 2
Fig. 2
Trajectories of prenatal maternal sleep quality by neonatal uncinate fasciculus fractional anisotropy (FA). Scores >5 on the PSQI indicate poor sleep quality. Data were analyzed continuously and are split +/− 1 SD from the mean FA for visualization purposes only. Topographical figure of the uncinate also included.
Fig. 3
Fig. 3
Neonatal uncinate fractional anisotropy partially mediates the association between prenatal maternal sleep quality and infant negative emotionality (top row = right uncinate; bottom row = left uncinate).
Supplementary Figure S1
Supplementary Figure S1
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