Sex Differences in Vulnerability to Prenatal Stress: a Review of the Recent Literature

Sutherland, Susanna; Brunwasser, Steven M.

doi:10.1007/s11920-018-0961-4

Cited by 129 publications

(113 citation statements)

References 78 publications

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“…SA-born males (particularly WT males) exhibited reduced PPI, whereas SA-born female WT mice exhibited an anxiogenic profile in the EPM. These findings are consistent with other reports of sex-specific changes as a result of perinatal stress exposure, and how these differences might contribute to subsequent health outcomes of offspring 79 . One study showed greater prenatal maternal stressor sensitivity in male offspring for subsequent development of SZ spectrum disorders 80 .…”

Section: Discussionsupporting

confidence: 92%

Short-active photoperiod gestation induces psychiatry-relevant behavior in healthy mice but a resiliency to such effects are seen in mice with reduced dopamine transporter expression

Kwiatkowski

Cope

Lavadia

et al. 2020

Sci Rep

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A higher incidence of multiple psychiatric disorders occurs in people born in late winter/early spring. Reduced light exposure/activity level impacts adult rodent behavior and neural mechanisms, yet few studies have investigated such light exposure on gestating fetuses. A dysfunctional dopamine system is implicated in most psychiatric disorders, and genetic polymorphisms reducing expression of the dopamine transporter (DAT) are associated with some conditions. Furthermore, adult mice with reduced DAT expression (DAT-HT) were hypersensitive to short active (SA; 19:5 L:D) photoperiod exposure versus their wildtype (WT) littermates. Effects of SA photoperiod exposure during gestation in these mice have not been examined. We confirmed adult females exhibit a heightened corticosterone response when in SA photoperiod. We then tested DAT-HT mice and WT littermates in psychiatryrelevant behavioral tests after SA or normal active (NA; 12:12 L:D) photoperiod exposure during gestation and early life. SA-born WT mice exhibited sensorimotor gating deficits (males), increased reward preference, less immobility, open arm avoidance (females), less motivation to obtain a reward, and reversal learning deficits, vs. NA-born WT mice. DAT-HT mice were largely resilient to these effects, however. Future studies will determine the mechanism(s) by which SA photoperiod exposure influences brain development to predispose toward emergence of psychiatry-relevant behaviors.

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Section: Discussionsupporting

confidence: 92%

Short-active photoperiod gestation induces psychiatry-relevant behavior in healthy mice but a resiliency to such effects are seen in mice with reduced dopamine transporter expression

Kwiatkowski

Cope

Lavadia

et al. 2020

Sci Rep

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“…The potential for child sex to determine these associations also requires additional investigation. That our exploratory analyses provide some evidence that the association between prenatal mood entropy and 2-year child cognitive development scores appears to be present among girls, but not boys is consistent with findings from previous studies documenting sex differences in fetal programming (Sandman et al, 2013;Sutherland & Brunwasser, 2018). However, we did not find a sex difference in the association between maternal mood entropy and 6to 9-year child expressive language scores.…”

Section: Discussionsupporting

confidence: 91%

Prenatal maternal mood entropy is associated with child neurodevelopment.

Howland

Sandman

Davis

et al. 2021

Emotion

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Emerging evidence indicates that the predictability of signals early in life may influence the developing brain. This study examines links between a novel indicator of maternal mood dysregulation, mood entropy, and child neurodevelopmental outcomes. Associations between prenatal maternal mood entropy and child neurodevelopment were assessed in 2 longitudinal cohorts. Maternal mood was measured several times over pregnancy beginning as early as 15 weeks' gestation. Shannon's mood entropy was applied to distributions of mothers' responses on mood questionnaires. Child cognitive and language development were evaluated at 2 and 6-9 years of age. Higher prenatal maternal mood entropy was associated with lower cognitive development scores at 2 years of age and lower expressive language scores at 6-9 years of age. These associations persisted after adjusting for maternal pre and postnatal mood levels and for other relevant sociodemographic factors. Our findings identify maternal mood entropy as a novel predictor of child neurodevelopment. Characterizing components of maternal mood in addition to level of severity or valence may further our understanding of specific processes by which maternal mood shapes child development.

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“…Adaptation of the maternal hypothalamic-pituitary-adrenal (HPA) axis is a key mechanism by which maternal stress modulates offspring neurodevelopment (3), and there is evidence that this mechanism operates in a sexually dimorphic manner (4). For, example, higher waking maternal salivary cortisol in pregnancy is associated with increased internalizing behaviours in female infants and reduced internalizing behaviours in males (5,6).…”

Section: Introductionmentioning

confidence: 99%

Maternal cortisol is associated with neonatal amygdala microstructure and connectivity in a sexually dimorphic manner

Stoye

Blesa

Sullivan

et al. 2020

Preprint

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The mechanisms that link maternal stress in pregnancy with infant brain development and neurobehavioral outcomes in a sexually dimorphic manner are poorly understood. We tested the hypothesis that increased maternal hypothalamic-pituitary-adrenal (HPA) axis activity, as measured by hair cortisol concentration (HCC), is associated with microstructure, structural connectivity and volume of the amygdala of newborn infants. In 78 human mother-infant dyads (44 male, 34 female) with a median gestational age (GA) at birth of 38.4 weeks (range 24.0-42.0), 3 cm maternal hair was sampled in the early postnatal period for quantification of cortisol by liquid chromatography-tandem mass spectrometry, and infants underwent structural and diffusion magnetic resonance imaging at term equivalent age (median 41.9 weeks, range 38.6-45.9). After adjustment for GA at birth, age at scan, birth weight z-score, and socioeconomic deprivation, higher maternal HCC was associated with higher left amygdala fractional anisotropy (FA) (b=0.677, p=0.010), lower left amygdala orientation dispersion index (b=-0.597, p=0.034), and higher FA in connections between the right amygdala and putamen (b=0.475, p=0.007) in girls compared to boys. Maternal HPA activity during pregnancy is related to architecture and connectivity of the human newborn amygdala in a sexually dimorphic manner. Given the fundamental role of the amygdala in the emergence of emotion regulation, these findings offer new insights into mechanisms linking maternal stress in pregnancy with adverse neuropsychiatric outcomes of children. Significance StatementMaternal health and wellbeing are associated with brain development, behavior, and emotion regulation in children, but little is known about how maternal stress is transmitted to infant development. This study linked neonatal brain magnetic resonance imaging with maternal hair cortisol concentration at the time of delivery, which reflects chronic hypothalamic-pituitaryadrenal activity in the final 3 months of pregnancy. There were strong associations between maternal cortisol and microstructure and structural connectivity of the amygdalae. These findings reveal that the amygdala, a structure of known importance for emotion regulation and behaviour across the life course, is susceptible to variations in the prenatal stress environment, and that cortisol imparts sex specific effects on human fetal neurodevelopment.

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Sex Differences in Vulnerability to Prenatal Stress: a Review of the Recent Literature

Cited by 129 publications

References 78 publications

Short-active photoperiod gestation induces psychiatry-relevant behavior in healthy mice but a resiliency to such effects are seen in mice with reduced dopamine transporter expression

Short-active photoperiod gestation induces psychiatry-relevant behavior in healthy mice but a resiliency to such effects are seen in mice with reduced dopamine transporter expression

Prenatal maternal mood entropy is associated with child neurodevelopment.

Maternal cortisol is associated with neonatal amygdala microstructure and connectivity in a sexually dimorphic manner

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