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. 2024 Jul 4;2(4):274-289.
doi: 10.1016/j.jaacop.2024.04.009. eCollection 2024 Dec.

Independent and Interactive Impacts of Prenatal Exposure to Legal Substances and Childhood Trauma on Emotion Processing in Pre-Adolescents: Preliminary Findings From the ABCD Study

Affiliations

Independent and Interactive Impacts of Prenatal Exposure to Legal Substances and Childhood Trauma on Emotion Processing in Pre-Adolescents: Preliminary Findings From the ABCD Study

Lauren Lepow et al. JAACAP Open. .

Abstract

Objective: This paper investigated the effects of prenatal drug exposure (PDE), childhood trauma (CT), and their interactions on the neurobiological markers for emotion processing.

Method: Here, in a non-clinical sample of pre-adolescents (9-10 years of age) from the Adolescent Brain Cognitive Development (ABCD) Study (N = 6,146), we investigate the impact of PDE to commonly used substances (ie, alcohol, cigarettes, and marijuana), CT, and their interaction on emotion processing. From the Emotional N-back functional magnetic resonance imaging task data, we selected 26 regions of interests, previously implicated in emotion processing, and conducted separate linear mixed models (108 total) and accounted for available environmental risk factors.

Results: PDE was associated with reductions in response bias related to the processing of fearful compared to happy faces in widespread cortical regions (including the superior frontal and fusiform gyri and the inferior parietal lobule). Reduced response bias in the superior frontal gyrus emerged as PDE driven and was present regardless of CT status, but correlated with several items on the Child Behavior Checklist only in those children with both PDE and CT. The lower response bias of the left inferior parietal lobule, on the other hand, was observed only in children with both PDE and CT, and correlated with internalizing and externalizing behaviors.

Conclusion: The study's results support the diathesis-stress model, and suggest that PDE may confer vulnerability to the effects of later CT through altered neurodevelopment. Children experiencing these "double-hit" conditions may represent at-risk individuals who could benefit from early interventions to mitigate the onset of psychopathology. Because of limitations in the way that PDE was reported in the ABCD Study, including lack of severity measures and retrospective reporting, results are not sufficient for making recommendations or dictating policy for pregnant persons. Nevertheless, this study is a necessary first step in examining the interactive effects of prenatal and early-life exposures, as well as many aspects of the sociodemographic and psychological environment.

Keywords: ABCD Study; adolescents; childhood trauma; emotion processing; prenatal drug exposure.

Plain language summary

This study looked at how prenatal drug exposure of commonly used substances (alcohol, cigarettes, and cannabis) and childhood trauma affect brain activity related to processing emotions in children from the Adolescent Brain Cognitive Development (ABCD) Study. Using brain imaging data from 6,146 children aged 9-10, the study found that prenatal drug exposure was associated with differing brain activity to emotional faces in several brain regions involved in emotion processing. Children who experienced both prenatal drug exposure and childhood trauma showed altered brain activity patterns that correlated with greater behavioral problems reported by parents. These findings suggest prenatal drug exposure may make children more vulnerable to the negative effects of childhood trauma on brain development and mental health.

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Figures

Figure 1
Figure 1
Main Effect of Prenatal Drug Exposure on Region of Interest (ROI) Activation in the Valence Condition Note:In the main effect model, during the valence condition (A) PDE+ was associated with widespread reductions in activity across ROIs involved in emotion processing. Gray represents both unexplored and statistically non-significant regions. Coefficient describes the effect size and direction of the effect. (B) Bars represent the effect size in each ROI for PDE+ compared to PDE– (dotted line), and whiskers represent confidence interval. All depicted reductions in activity (cold-colored regions) were statistically significant for the PDE main effect (PDE+ < PDE–). PDE = prenatal drug exposure.
Figure 2
Figure 2
Main Effect of Childhood Trauma on Region of Interest (ROI) Activation in the Valence Condition Note:In the main effect model, during the valence condition (A) CT+ was associated with greater activity in the left amygdala. Gray represents both unexplored and statistically non-significant regions. The coefficient describes the effect size and direction of the effect. (B) The red line shows the variation in effect size for CT+ compared to CT– (0-line). CT = childhood trauma.
Figure 3
Figure 3
Interaction Effects of Prenatal Drug Exposure and Childhood Trauma on Region of Interest (ROI) Activation in the Valence Condition Note:(A) A double-hit specific decrease in the left inferior parietal lobule activity was revealed in the interaction models during the valence condition. Gray represents both unexplored and statistically non-significant regions. The coefficient describes the effect size and direction of the effect. (B) Whereas PDE+/CT+ was significantly associated with this effect, other subgroups were not. The dashed 0-line represents the PDE–/CT– reference group. (C) A double-hit specific increase in the right fusiform gyrus activity was revealed in the interaction models during the arousal condition. Gray represents both unexplored and statistically non-significant regions. The coefficient describes the effect size and direction of the effect. (D) Whereas PDE+/CT+ was significantly associated with this effect, other subgroups were not. The dashed 0-line represents the PDE–/CT– (reference) group. CT = childhood trauma; PDE = prenatal drug exposure.
FIGURE 4
FIGURE 4
Correlations Between Subclinical Problematic Behaviors and Beta Contrasts of Significant Region of Interest (ROI) Activations Note:Matrices illustrate correlations between ROIs significant in mixed models with clinical symptoms from scales including CBCL, UPPS, BIS BAS, and Youth Prosocial Behavior Survey for (A) PDE+ children, and interaction subgroups (B) PDE+/CT– and(C)PDE+/CT+ children. Green-shaded cells are significant at p < .05 after having been false discovery rate corrected for multiple comparisons. CBCL = Child Behavior Checklist; BIS BAS = behavioral inhibition system and behavioral activation system; CT = childhood trauma; PDE = prenatal drug exposure.

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