Convergent neural correlates of prenatal exposure to air pollution and behavioral phenotypes of risk for internalizing and externalizing problems: Potential biological and cognitive pathways

Margolis, Amy; Liu, Ran; Conceição, Vasco A.; Ramphal, Bruce; Pagliaccio, David; DeSerisy, Mariah; Koe, Emily; Selmanovic, Ena; Raudales, Amarelis; Emanet, Nur; Quinn, Aurabelle E.; Beebe, Beatrice; Pearson, Brandon L.; Herbstman, Julie B.; Rauh, Virginia; Fifer, William P.; Champagne, Frances A.

doi:10.1016/j.neubiorev.2022.104645

Cited by 14 publications

(7 citation statements)

References 187 publications

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“…Higher prenatal PAH exposure predicted increased shyness, which in turn predicted greater internalizing problems. These findings are in line with animal models pointing to the effects of gestational air pollution exposure on behavioral phenotypes (Gao et al, 2017;Margolis et al, 2022;Miller et al, 2016). Moreover, our findings demonstrate the moderating effect of left ACC activity during the engagement of cognitive control on the association between prenatal exposure to air pollution and internalizing problems, consistent with theoretical models pointing to the role of high monitoring in the manifestation of social anxiety (Buzzell et al, 2018).…”

Section: Discussionsupporting

confidence: 90%

“…Greater prenatal exposure to PAH is associated with increased shyness in early childhood. Animal models suggest that prenatal exposure to air pollution increases the risk for adverse behavioral phenotypes (i.e., behavioral inhibition, irritability) through various mechanisms, including altered dopaminergic signaling, neuroinflammatory responses, and hippocampal structure, BDNF expression in the hippocampus (Margolis et al, 2022). Notably, humans with higher exposure to air pollution have reduced BDNF (Tang et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Other risk markers for internalizing problems that share conceptual similarities with shyness include behavioral inhibition, social wariness, and fear (Buss et al, 2013; Fox et al, 2021). Animal models document the effects of gestational exposure to PAH on animal behaviors that are analogous to human risk markers of behavioral inhibition (Margolis et al, 2022). For example, gestational exposure to PAH increases fearful behaviors in zebrafish (Gao et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

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Prenatal exposure to air pollution and childhood internalizing problems: roles of shyness and anterior cingulate cortex activity

Liu

Pagliaccio

Herbstman

et al. 2023

Child Psychology Psychiatry

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Background Prenatal exposure to air pollution increases the risk for psychiatric disorders characterized by internalizing problems. In this study, we examined the roles of shyness and anterior cingulate cortex (ACC) activity in the association between prenatal exposure to polycyclic aromatic hydrocarbons (PAH) and children's internalizing problems at 7–9 years old. Methods Participants include 53 children (31 girls, 22 boys). Personal air monitoring was conducted over 48 continuous hours during the third trimester of pregnancy to measure 8 PAHs. Mothers reported children's shyness (Emotionality Activity Sociability Temperament Survey) at age 5 and internalizing problems (Child Behavior Checklist) at ages 7–9. ACC activity was measured by fMRI during the Simon Spatial Incompatibility task at ages 7–9. Results Shyness mediated the association between prenatal PAH exposure and internalizing problems. Higher prenatal PAH exposure predicted increased shyness, which in turn predicted greater internalizing problems. Moreover, left ACC activity during the Simon task moderated the association between prenatal PAH exposure and internalizing problems. Prenatal PAH exposure predicted increased risk for internalizing problems only when children showed heightened left ACC activity during the resolution of cognitive conflict. Conclusions Our study innovatively synthesizes the fields of developmental psychology and environmental health science to offer new insights into the risk factors for anxiety disorders. Facilitating the development of healthy reactive and regulatory processes may improve the developmental outcomes for children highly exposed to air pollution.

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Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Prenatal exposure to air pollution and childhood internalizing problems: roles of shyness and anterior cingulate cortex activity

Liu

Pagliaccio

Herbstman

et al. 2023

Child Psychology Psychiatry

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“…Further, prior findings show that shifting the standard score cutoff for identifying academic challenges changes concordance between LD and LDiff identification (Quinn & Wagner, 2015), pointing to the importance of using metrics that reflect skill deficits rather than categorical diagnoses when working with populations for whom categorical diagnosis may over‐or under‐represent children. Further, given sex‐specific differences in LD/LDiff (Quinn & Wagner, 2015) and in effects of air pollution and other neurotoxicants on neurodevelopment (Margolis et al, 2022), particularly endocrine disrupting compounds (phenols, phthalates) (Ghassabian & Trasande, 2018), future studies should be designed to be powered to test sex‐specific environmentally‐associated phenotypes of LDiff.…”

Section: Future Directionsmentioning

confidence: 99%

The Role of Environmental Chemicals in the Etiology of Learning Difficulties: A Novel Theoretical Framework

Margolis

Greenwood

Dranovsky

et al. 2023

Mind Brain and Education

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Children from economically disadvantaged communities have a disproportionate risk of exposure to chemicals, social stress, and learning difficulties. Although animal models and epidemiologic studies link exposures and neurodevelopment, little focus has been paid to academic outcomes in environmental health studies. Similarly, in the educational literature, environmental chemical exposures are overlooked as potential etiologic factors in learning difficulties. We propose a theoretical framework for the etiology of learning difficulties that focuses on these understudied exogenous factors. We discuss findings from animal models and longitudinal, prospective birth cohort studies that support this theoretical framework. Studies reviewed point to the effects of prenatal exposure to polycyclic aromatic hydrocarbons on reading comprehension and math skills via effects on inhibitory control processes. Long term, this work will help close the achievement gap in the United States by identifying behavioral and neural pathways from prenatal exposures to learning difficulties in children from economically disadvantaged families.

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“…The period encompassing pregnancy and the first two years after birth -the perinatal period- has also been termed ‘the first 1000 days’ or ‘the first 1001 critical days’. Furthermore, preclinical, epidemiological, and clinical studies indicate that perinatal adaptations to adverse environmental factors (e.g., parental psychosocial stress, health problems, unhealthy life style factors, toxic chemicals, air pollution) and to promotive factors (e.g., parental resilience, health, stable and supportive context, green space), in interaction with genetic susceptibility and timing, intensity and duration of the exposure, may influence offspring endocrine, immune, metabolic, microbiome, and other biological systems, which in turn can affect offspring neurobehavioral development [5 ▪ ,6–13].…”

Section: Introductionmentioning

confidence: 99%

Current perspectives on perinatal mental health and neurobehavioral development: focus on regulation, coregulation and self-regulation

Van den Bergh,

Antonelli,

Stein

2024

Current Opinion in Psychiatry

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Purpose of review Perinatal mental health research provides an important perspective on neurobehavioral development. Here, we aim to review the association of maternal perinatal health with offspring neurodevelopment, providing an update on (self-)regulation problems, hypothesized mechanistic pathways, progress and challenges, and implications for mental health. Recent findings (1) Meta-analyses confirm that maternal perinatal mental distress is associated with (self-)regulation problems which constitute cognitive, behavioral, and affective social-emotional problems, while exposure to positive parental mental health has a positive impact. However, effect sizes are small. (2) Hypothesized mechanistic pathways underlying this association are complex. Interactive and compensatory mechanisms across developmental time are neglected topics. (3) Progress has been made in multiexposure studies. However, challenges remain and these are shared by clinical, translational and public health sciences. (4) From a mental healthcare perspective, a multidisciplinary and system level approach employing developmentally-sensitive measures and timely treatment of (self-)regulation and coregulation problems in a dyadic caregiver-child and family level approach seems needed. The existing evidence-base is sparse. Summary During the perinatal period, addressing vulnerable contexts and building resilient systems may promote neurobehavioral development. A pluralistic approach to research, taking a multidisciplinary approach to theoretical models and empirical research needs to be fostered.

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Convergent neural correlates of prenatal exposure to air pollution and behavioral phenotypes of risk for internalizing and externalizing problems: Potential biological and cognitive pathways

Cited by 14 publications

References 187 publications

Prenatal exposure to air pollution and childhood internalizing problems: roles of shyness and anterior cingulate cortex activity

Prenatal exposure to air pollution and childhood internalizing problems: roles of shyness and anterior cingulate cortex activity

The Role of Environmental Chemicals in the Etiology of Learning Difficulties: A Novel Theoretical Framework

Current perspectives on perinatal mental health and neurobehavioral development: focus on regulation, coregulation and self-regulation

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