Associations of interpersonal and socioeconomic early life adversity dimensions with adolescents' corticolimbic circuits, cognition, and mental health

Abstract

Early life adversity (ELA) is highly prevalent and has significant detrimental effects on children's brain development and behavioral outcomes. However, associations of threat, unpredictability, and deprivation in dimensional models of ELA with corticolimbic circuits were unclear. Previous studies have highlighted the effects of proximity, especially the distinctions between interpersonal and socioeconomic ELA, on children's neurodevelopment. This study first examined the associations between multiple ELA categories (i.e., interpersonal threat, socioeconomic threat, interpersonal unpredictability, socioeconomic unpredictability, interpersonal deprivation, and socioeconomic deprivation) and the developmental changes in resting-state functional connectivity (rsFC) of the frontolimbic and temporal-limbic circuits implicated in cognition and psychopathology, using data from the Adolescent Brain Cognitive Development (ABCD) study, which included four measurements from baseline (mean ± SD age, 119.13 ± 7.51 months; 2815 females) to 3-year follow-up (N = 5885). Controlling for concurrent ELA categories, interpersonal unpredictability and socioeconomic deprivation were associated with accelerated development of rsFC between CON/RTN-amygdala/hippocampus (Cingulo-opercular Network, Retrosplenial Temporal Network). Compared to girls, boys' corticolimbic circuits development was more sensitive to interpersonal threat. Changes in rsFC mediated the associations between interpersonal unpredictability/socioeconomic deprivation with decreased crystallized cognition, fluid cognition, and internalizing problems. Additionally, socioeconomic deprivation was associated with decreased crystallized cognition through interpersonal unpredictability and changes in rsFC between CON and bilateral amygdala/right hippocampus. This study emphasized interpersonal unpredictability and socioeconomic deprivation as key environmental factors affecting corticolimbic circuit development implicated in cognition and psychopathology. Stable family environments and enriched neighborhoods are crucial for supporting optimal neural and behavioral development in children and adolescents.

Fig. 1. Research aims.

The blue arrows represent the associations between interpersonal/socioeconomic early life adversity (ELA) dimensions andresting-state functional connectivity (RSFC) of the corticolimbic circuits (1.1). The purple arrows indicate the mediating role of RSFC in the link between ELA and adolescent behaviors (2.1). The red arrows represent the multiple mediation pathways through which interpersonal ELA and RSFC mediate the association between socioeconomic ELA andadolescent behaviors (3). Yellow indcates sex differences (1.2 & 2.2).

Fig. 2. Changes in rsFC of CON/RTN-amygdala/hippocampus.

rsFC resting-state functional connectivity, CON cingulo-opercular network, RTN retrosplenial temporal network, aglh left amygdala, agrh right amygdala, hplh left hippocampus, hprh right hippocampus. **** p < 0.0001.

Fig. 3. Significant Associations between Interpersonal Unpredictability/Socioeconomic Deprivation and Changes in rsFC.

Blue lines indicated the associations between interpersonal unpredictability and changes in rsFC; red lines indicated the associations between socioeconomic deprivation and changes in rsFC. Solid lines represented positive effects; dashed lines represented negative effects. rsFC resting-state functional connectivity, CON cingulo-opercular network, RTN retrosplenial temporal network, aglh left amygdala, agrh right amygdala, hplh left hippocampus, hprh right hippocampus.

Fig. 4. Significant Mediating Effects of Changes in rsFC on the Associations between Interpersonal Unpredictability/Socioeconomic Deprivation and Adolescent Cognitive abilities/Behavioral Problems.

The two ends of the lines were the lower and upper limits of the confidence interval, and the middle points were the estimates of the mediating effects. The y-axis on the left side of the lines corresponded to the independent variables and mediators, while the colors represented the dependent variables in the legend. rsFC resting-state functional connectivity, IU interpersonal unpredictability, SD socioeconomic deprivation, CON cingulo-opercular network, RTN retrosplenial temporal network, aglh left amygdala, agrh right amygdala, hplh left hippocampus, hprh right hippocampus. ⁺p < 0.1, * p < 0.05, ** p < 0.01.

Fig. 5. Significant Serial Mediation Models of Interpersonal Unpredictability and Changes in rsFC Between Socioeconomic Deprivation and Crystallized Cognition.

A Multiple mediation pathways through which interpersonal unpredictability and CON-aglh rsFC mediate the association between socioeconomic deprivation andadolescent crystallized cognition. B Multiple mediation pathways through which interpersonal unpredictabilityand CON-agrh rsFC mediate the association between socioeconomic deprivation andadolescent crystallized cognition. C Multiple mediation pathways through which interpersonal unpredictability and CON-hprh rsFC mediate the association between socioeconomic deprivation and adolescent crystallized cognition.