Association between prenatal maternal sleep quality, neonatal uncinate fasciculus white matter, and infant negative emotionalityResearch in context

Summary: 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 inc...

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Main Authors: Melissa Nevarez-Brewster, Catherine H. Demers, LillyBelle K. Deer, Özlü Aran, Robert J. Gallop, Mercedes Hoeflich Haase, Khalid Al-Ali, Maria M. Bagonis, John H. Gilmore, M. Camille Hoffman, Martin A. Styner, Benjamin L. Hankin, Elysia Poggi Davis
Format: Article
Language:English
Published: Elsevier 2024-11-01
Series:EBioMedicine
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352396424004201
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author Melissa Nevarez-Brewster
Catherine H. Demers
LillyBelle K. Deer
Özlü Aran
Robert J. Gallop
Mercedes Hoeflich Haase
Khalid Al-Ali
Maria M. Bagonis
John H. Gilmore
M. Camille Hoffman
Martin A. Styner
Benjamin L. Hankin
Elysia Poggi Davis
author_facet Melissa Nevarez-Brewster
Catherine H. Demers
LillyBelle K. Deer
Özlü Aran
Robert J. Gallop
Mercedes Hoeflich Haase
Khalid Al-Ali
Maria M. Bagonis
John H. Gilmore
M. Camille Hoffman
Martin A. Styner
Benjamin L. Hankin
Elysia Poggi Davis
author_sort Melissa Nevarez-Brewster
collection DOAJ
description Summary: 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).
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spelling doaj-art-8832bd2132064ae7b174f2e4caa74d0c2024-11-14T04:32:20ZengElsevierEBioMedicine2352-39642024-11-01109105384Association between prenatal maternal sleep quality, neonatal uncinate fasciculus white matter, and infant negative emotionalityResearch in contextMelissa Nevarez-Brewster0Catherine H. Demers1LillyBelle K. Deer2Özlü Aran3Robert J. Gallop4Mercedes Hoeflich Haase5Khalid Al-Ali6Maria M. Bagonis7John H. Gilmore8M. Camille Hoffman9Martin A. Styner10Benjamin L. Hankin11Elysia Poggi Davis12Department of Psychology, University of Denver, USA; Corresponding author. 2155 S. Race Street, Denver, CO 80210, USA.Department of Psychology, University of Denver, USA; Department of Psychiatry, University of Colorado Anschutz Medical Campus, USA; Corresponding author. Department of Psychology, University of Denver, USA.Department of Psychology, University of Denver, USADepartment of Psychology, University of Denver, USADepartment of Mathematics, West Chester University, West Chester, PA, USADepartment of Psychiatry, University of North Carolina, Chapel Hill, USADepartment of Psychiatry, School of Medicine, Indiana University, USADepartment of Psychiatry, University of North Carolina, Chapel Hill, USADepartment of Psychiatry, University of North Carolina, Chapel Hill, USADepartment of Psychiatry, University of Colorado Anschutz Medical Campus, USA; Division of Maternal and Foetal Medicine, Department of Obstetrics and Gynaecology, University of Colorado Denver School of Medicine, USADepartment of Psychiatry, University of North Carolina, Chapel Hill, USA; Department of Computer Science, University of North Carolina, Chapel Hill, USADepartment of Psychology, University of Illinois at Urbana, Champaign, USADepartment of Psychology, University of Denver, USA; Department of Paediatrics, University of California, Irvine, USASummary: 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).http://www.sciencedirect.com/science/article/pii/S2352396424004201Prenatal sleepUncinate fasciculusNegative emotionalityDiffusion imagingIntergenerational transmissionNeonatal magnetic resonance imaging
spellingShingle Melissa Nevarez-Brewster
Catherine H. Demers
LillyBelle K. Deer
Özlü Aran
Robert J. Gallop
Mercedes Hoeflich Haase
Khalid Al-Ali
Maria M. Bagonis
John H. Gilmore
M. Camille Hoffman
Martin A. Styner
Benjamin L. Hankin
Elysia Poggi Davis
Association between prenatal maternal sleep quality, neonatal uncinate fasciculus white matter, and infant negative emotionalityResearch in context
EBioMedicine
Prenatal sleep
Uncinate fasciculus
Negative emotionality
Diffusion imaging
Intergenerational transmission
Neonatal magnetic resonance imaging
title Association between prenatal maternal sleep quality, neonatal uncinate fasciculus white matter, and infant negative emotionalityResearch in context
title_full Association between prenatal maternal sleep quality, neonatal uncinate fasciculus white matter, and infant negative emotionalityResearch in context
title_fullStr Association between prenatal maternal sleep quality, neonatal uncinate fasciculus white matter, and infant negative emotionalityResearch in context
title_full_unstemmed Association between prenatal maternal sleep quality, neonatal uncinate fasciculus white matter, and infant negative emotionalityResearch in context
title_short Association between prenatal maternal sleep quality, neonatal uncinate fasciculus white matter, and infant negative emotionalityResearch in context
title_sort association between prenatal maternal sleep quality neonatal uncinate fasciculus white matter and infant negative emotionalityresearch in context
topic Prenatal sleep
Uncinate fasciculus
Negative emotionality
Diffusion imaging
Intergenerational transmission
Neonatal magnetic resonance imaging
url http://www.sciencedirect.com/science/article/pii/S2352396424004201
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