Newborn amygdalar volumes are associated with maternal prenatal psychological distress in a sex-dependent way

Lehtola, Satu J.; Tuulari, Jetro J.; Scheinin, Noora M.; Karlsson, Lena; Parkkola, Riitta; Merisaari, Harri; Lewis, John D.; Fonov, Vladimir; Collins, D. Louis; Evans, Alan C.; Saunavaara, Jani; Hashempour, Niloofar; Lähdesmäki, Tuire; Acosta, Henriette; Karlsson, Hasse

doi:10.1016/j.nicl.2020.102380

Cited by 34 publications

(46 citation statements)

References 115 publications

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“…It is challenging to place the magnitude of this observed effect in the context of previous findings in the literature, given the small number of studies of this or similar research questions, differences in statistical approach, and/or absence of reported effect size estimates. However, it is apparent that the size of the effect of maternal perceived stress on newborn HCV in our study is consistent with that reported in studies of maternal psychosocial stress and other subcortical structures ( Lehtola et al, 2020 ), and also with a study reporting a prospective association between serial measurements of perceived stress across a 20-year period and HCV in postmenopausal women ( Gianaros et al, 2007 ). Moreover, the effect in our study of maternal stress on infant social-emotional development via offspring HCV may portend clinical relevance.…”

Section: Discussionsupporting

confidence: 92%

“…Indeed, one recent study using fetal MRI reported an association between maternal psychosocial distress and fetal left HCV ( Wu et al, 2020 ). In contrast, two other studies ( Lehtola et al, 2020 ; Qiu et al, 2013 ) found no associations between maternal depressive and anxiety symptoms during pregnancy and newborn HCV (although maternal antenatal anxiety was associated with slower growth of the right hippocampus across the first 6 months of life ( Qiu et al, 2013 )).…”

Section: Introductionmentioning

confidence: 76%

“…The findings regarding HCV are in line with several prior animal studies ( Badihian et al, 2019 ; Charil et al, 2010 ) and a recent study employing fetal MRI in human pregnancy that reported an inverse association between maternal stress and anxiety and left fetal HCV ( Wu et al, 2020 ). However, two other studies report no effect of maternal anxiety and depression symptoms on newborn HCV ( Lehtola et al, 2020 ; Qiu et al, 2013 ). Instead, in the study by Qiu et al (2013) , antenatal anxiety was related to slower hippocampal growth over the first 6 months of life, and Ong et al (2019) observed in the same cohort that the association between prenatal distress and HCV was moderated by genetic factors.…”

Section: Discussionmentioning

confidence: 93%

“…Maternal perceived stress during pregnancy was not associated with offspring AGV in the present study, which is in concordance with observations by previous studies ( Donnici et al, 2021 ; Rifkin-Graboi et al, 2013 ). Others have reported associations between maternal distress during pregnancy and offspring AGV that differed by sex ( Acosta et al, 2019 ; Lehtola et al, 2020 ; Wen et al, 2017 ) . Such moderation of the association between maternal distress during pregnancy and offspring AGV by offspring sex was not observed in the present study.…”

Section: Discussionmentioning

confidence: 99%

“…Investigations of the association between maternal psychosocial stress and AGV have generated similar inconclusive results. One study in neonates observed no association between AGV and maternal depressive symptoms ( Rifkin-Graboi et al, 2013 ), whereas another study reported smaller left and right AGV in association with maternal psychosocial stress, albeit only in male neonates ( Lehtola et al, 2020 ). Sex-specific effects of maternal prenatal depression and anxiety have also been observed in two studies in preschool children.…”

Section: Introductionmentioning

confidence: 99%

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Prospective association of maternal psychosocial stress in pregnancy with newborn hippocampal volume and implications for infant social-emotional development

Moog

Nolvi

Kleih

et al. 2021

Neurobiology of Stress

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Maternal psychosocial stress during pregnancy can impact the developing fetal brain and influence offspring mental health. In this context, animal studies have identified the hippocampus and amygdala as key brain regions of interest, however, evidence in humans is sparse. We, therefore, examined the associations between maternal prenatal psychosocial stress, newborn hippocampal and amygdala volumes, and child social-emotional development. In a sample of 86 mother-child dyads, maternal perceived stress was assessed serially in early, mid and late pregnancy. Following birth, newborn (aged 5–64 postnatal days, mean: 25.8 ± 12.9) hippocampal and amygdala volume was assessed using structural magnetic resonance imaging. Infant social-emotional developmental milestones were assessed at 6- and 12-months age using the Bayley-III. After adjusting for covariates, maternal perceived stress during pregnancy was inversely associated with newborn left hippocampal volume ( β = −0.26, p = .019), but not with right hippocampal ( β = −0.170, p = .121) or bilateral amygdala volumes ( p s > .5). Furthermore, newborn left hippocampal volume was positively associated with infant social-emotional development across the first year of postnatal life (B = 0.01, p = .011). Maternal perceived stress was indirectly associated with infant social-emotional development via newborn left hippocampal volume (B = −0.34, 95% CI BC [-0.97, −0.01]), suggesting mediation. This study provides prospective evidence in humans linking maternal psychosocial stress in pregnancy with newborn hippocampal volume and subsequent infant social-emotional development across the first year of life. These findings highlight the importance of maternal psychosocial state during pregnancy as a target amenable to interventions to prevent or attenuate its potentially unfavorable neural and behavioral consequences in the offspring.

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Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 76%

Section: Discussionmentioning

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Prospective association of maternal psychosocial stress in pregnancy with newborn hippocampal volume and implications for infant social-emotional development

Moog

Nolvi

Kleih

et al. 2021

Neurobiology of Stress

View full text Add to dashboard Cite

show abstract

Association of Prenatal Exposure to Early-Life Adversity With Neonatal Brain Volumes at Birth

et al. 2022

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Key Points Question Is prenatal exposure to maternal social disadvantage and psychosocial stress associated with global and relative infant brain volumes at birth? Findings In this longitudinal, observational cohort study of 280 mother-infant dyads, prenatal exposure to greater maternal social disadvantage, but not psychosocial stress, was associated with statistically significant reductions in white matter, cortical gray matter, and subcortical gray matter volumes and cortical folding at birth after accounting for maternal health and diet. Meaning These findings suggest that prenatal exposure to social disadvantage is associated with global reductions in brain volumes and folding in the first weeks of life.

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Prenatal depressive symptoms and childhood development of brain limbic and default mode network structure

Donnici

Long

Reynolds

et al. 2023

Human Brain Mapping

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Prenatal depressive symptoms are linked to negative child behavioral and cognitive outcomes and predict later psychopathology in adolescent children. Prior work links prenatal depressive symptoms to child brain structure in regions like the amygdala; however, the relationship between symptoms and the development of brain structure over time remains unclear. We measured maternal depressive symptoms during pregnancy and acquired longitudinal T1‐weighted and diffusion imaging data in children ( n = 111; 60 females) between 2.6 and 8 years of age. Controlling for postnatal symptoms, we used linear mixed effects models to test relationships between prenatal depressive symptoms and age‐related changes in (i) amygdala and hippocampal volume and (ii) structural properties of the limbic and default‐mode networks using graph theory. Higher prenatal depressive symptoms in the second trimester were associated with more curvilinear trajectories of left amygdala volume changes. Higher prenatal depressive symptoms in the third trimester were associated with slower age‐related changes in limbic global efficiency and average node degree across childhood. Our work provides evidence that moderate symptoms of prenatal depression in a low sociodemographic risk sample are associated with structural brain development in regions and networks implicated in emotion processing.

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Newborn amygdalar volumes are associated with maternal prenatal psychological distress in a sex-dependent way

Cited by 34 publications

References 115 publications

Prospective association of maternal psychosocial stress in pregnancy with newborn hippocampal volume and implications for infant social-emotional development

Prospective association of maternal psychosocial stress in pregnancy with newborn hippocampal volume and implications for infant social-emotional development

Association of Prenatal Exposure to Early-Life Adversity With Neonatal Brain Volumes at Birth

Prenatal depressive symptoms and childhood development of brain limbic and default mode network structure

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