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Introduction Poor prenatal sleep health is a pervasive reproductive health concern that informs the health of the mother and fetal development. Despite the almost ubiquitous nature of sleep disturbances across pregnancy, sleep health within pregnant populations, and its effects on the next generation, remain poorly studied. We recently showed that prenatal maternal sleep quality predicts newborn hippocampal volume. However, the relation between prenatal sleep quality and neonatal neural circuit development remains unknown. Changes in neonatal white matter microstructure presage compromised socioemotional and cognitive health, including the development of psychopathology and neurocognitive disorders, making it a plausible neurobiological pathway linking prenatal maternal sleep and offspring socioemotional health. This study first examined the relations between trajectories of prenatal maternal sleep quality and subsequent neonatal white matter integrity. We next evaluated whether neonatal white matter integrity partially mediates associations between prenatal sleep and infant negative emotionality. Methods Pregnant participants (n = 116) provided prospective and longitudinal data of prenatal maternal sleep quality at 16, 29, and 35 gestational weeks using the Pittsburgh Sleep Quality Index. Neonatal (53% female) white matter integrity was assessed via diffusion weighed images using magnetic resonance imaging (MRI). Infant negative emotionality was collected at 6 postpartum months using the Infant Behavior Questionnaire. Results Trajectories of prenatal maternal sleep quality predicted higher bilateral neonatal fractional anisotropy (FA) in the uncinate fasciculus (e.g., right: b = 0.15, p = .023). Further, higher uncinate FA predicted more infant negative emotionality (e.g., right: b = 0.25, p = .011) and uncinate FA partially mediated the association between prenatal maternal sleep and infant negative emotionality (right: indirect effect = 0.014, CI = [.0001, .0323], p < .05). Associations remained after covarying for infant postconceptional age at MRI, motion in MRI scan, sex, and income-to-needs ratio. Conclusion These findings highlight prenatal maternal sleep health as a prenatal signal with intergenerational connections to offspring neurobiology and negative emotionality, both of which have been previously implicated in the development of psychopathology. Pregnancy is a sensitive period in which interventions may inform the health of two generations. Support (if any) NIMH R01MH109662, NHLBI R01HL155744, and diversity training supplement for 1st author; F32MH125572 for 2nd author.

Introduction The prenatal period is characterized by immense fetal neuronal growth. Such rapid growth can increase fetal susceptibility to prenatal environmental insults (Barker, 1998). A promising prenatal process that may alter fetal development is maternal prenatal sleep quality. Poor prenatal sleep quality is a public health concern affecting approximately 78% of pregnant individuals (Lucena et al., 2018). In rodents, maternal sleep deprivation across gestation predicts offspring hippocampal neurogenesis, with pups exposed to sleep deprivation early and late in pregnancy exhibiting more anxiety and depression-like behaviors (Peng et al., 2015). In humans, poor sleep quality in other developmental stages predicts hippocampi and amygdalae changes (Marshall & Born, 2007; Saghir et al., 2018). However, the relation between prenatal sleep quality and offspring brain development in humans remains poorly understood. The present study examined associations between maternal sleep quality in early, mid, and late pregnancy, and newborn hippocampal and amygdala volume, regions implicated in memory and emotion. Methods Pregnant individuals (N=94; Mage=30.5; SDage=5.3) reported on sleep quality three times during pregnancy. Newborn (Mageinweeks=5.1; SDageinweeks=2.7) hippocampi and amygdalae volumes were assessed during an unsedated sleep cycle using magnetic resonance imaging (MRI). Tissue segmentation was collected using a multiatlas iterative algorithm that individually segmented the regions of interest and subsequently combined T1- and T2-weighted high-resolution images (See neonate multiatlas at https://www.nitrc.org/projects/unc_brain_atlas/). Bivariate correlations examined the association between prenatal sleep quality and hippocampus and amygdala volume. Partial correlations examined these associations in the presence of significant cofounding variables including intracranial volume, body weight percentile, sex, and postconceptional age. Results Partial correlations revealed that poor maternal sleep quality early in pregnancy predicted larger newborn bilateral hippocampal volume (all rs<.25; ps<.038). Associations with sleep later in gestation persisted for the right hippocampus (all rs<.25; ps<.038). Prenatal maternal sleep quality did not significantly predict newborn amygdala volume (all rs<-.06; ps>.58). Conclusion This study provides novel evidence linking prenatal sleep quality and newborn hippocampal volume in humans, suggesting the presence of an intergenerational link between prenatal sleep health and offspring well-being. Support (If Any) Support (if any): NIMH R01MH109662, NHLBI R01HL155744, and diversity training supplement for 1st author; F32MH125572 for 2nd author.

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