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; Ariella Wagner; Siddhartha Peri; Faith Adams; Srinivasan Anantha Ramakrishnan; Md Ashad Alam; Riaz B Shaik; Nicholas A Hubbard; Harold W Koenigsberg; Yasmin Hurd; Susan F Tapert; Iliyan Ivanov; Muhammad A Parvaz

doi:10.1016/j.jaacop.2024.04.009

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

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

Authors

Lauren Lepow^{1

2}, Ariella Wagner^{1

3}, Siddhartha Peri¹, Faith Adams¹, Srinivasan Anantha Ramakrishnan^{1

4}, Md Ashad Alam⁵, Riaz B Shaik¹, Nicholas A Hubbard⁶, Harold W Koenigsberg¹, Yasmin Hurd^{1

2}, Susan F Tapert⁷, Iliyan Ivanov¹, Muhammad A Parvaz^{1

2}

Affiliations

¹ Icahn School of Medicine at Mount Sinai, New York, New York.
² Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, New York.
³ Tufts University School of Medicine, Boston, Massachusetts.
⁴ Rutgers University, New Brunswick, New Jersey.
⁵ Centers for Outcomes and Health Services Research, Ochsner Health, New Orleans, Louisiana.
⁶ University of Nebraska-Lincoln, Lincoln, Nebraska.
⁷ University of California, San Diego, California.

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.