Gray matter volumetric correlates of behavioral activation and inhibition system traits in children: An exploratory voxel-based morphometry study of the ABCD project data

Abstract

Approach and avoidance represent two fundamental behavioral traits that develop early in life. Previous studies have examined the neural correlates of approach and avoidance traits in adults and adolescents. Here, using the data set of the Adolescent Brain Cognition Development project, we investigated the structural cerebral bases of behavioral activation system (BAS) and behavioral inhibition system (BIS) in children. We employed voxel-based morphometry to examine how gray matter volumes (GMV) related specifically to BAS and BIS traits in 11,542 children (5491 girls, age 9-10 years) with 648 and 2697 identified as monozygotic twins (MZ) and dizygotic twins/siblings (DZ), respectively. After accounting for the BIS score, higher BAS scores (residuals) were positively correlated with the GMV of the ventral striatum (VS), and the correlation was stronger in MZ than in DZ and unrelated children, with a heritability (h²) of 0.8463. Higher BAS scores were negatively correlated with the GMV of bilateral visual, lateral orbitofrontal, temporal, and inferior frontal cortex, as well as the precuneus. Higher BIS (after accounting for BAS) scores were negatively correlated with the GMVs of the ventral caudate and bilateral putamen/pallidum, hypothalamus, and right anterior insula, and the correlation was stronger in MZ than in DZ and unrelated children, with a heritability of 0.8848. A cluster in the VS showed positive and negative correlation with the BAS and BIS scores, respectively. These findings suggest shared and distinct cerebral volumetric bases of the BAS and BIS traits in children. Whereas both traits have a strong genetic basis, the BAS relative to BIS appears to be more amenable to environmental influences. These findings add to the literature of developmental neuroscience and may help identify genetic risk factors of externalizing and internalizing psychopathology.

Keywords: ABCD; BAS; BIS; Heritability; Imaging; VBM.

Figure 1.

GMV correlates of BAS residual scores for girls and boys combined. One-sample t-test, p<0.05, FWE corrected. Color bars show voxel T values and the corresponding Cohen’s d scores. Warm/cool colors: positive/negative correlations. The regression for the whole sample showed clusters both in positive and in negative correlation with BAS residual scores. The inset highlights the ventral striatal and cerebellar vermis clusters in coronal and sagittal sections. The results for girls’ and boys’ groups are shown in Supplementary Figure S3. The clusters are summarized in Supplementary Table S1.

Figure 2.

Structural correlates of BIS residual scores for girls and boys combined. One-sample t-test, p<0.001, uncorrected. Color bars show voxel T values and the corresponding Cohen’s d scores. Warm/cool colors: positive/negative correlations. The inset shows the ventral striatal cluster at the same coordinates in coronal and sagittal sections as in Figure 1. The results for girls’ and boys’ groups are shown in Supplementary Figure S4. The clusters are summarized in Supplementary Table S2.

Figure 3

plots the correlation each of monozygotic twins (MZ, red), dizygotic twins and siblings (DZ, blue) and unrelated individuals (UR, green) of (A) BAS residual score for all; (B) BAS residual score for girls; (C) BAS residual scores for boys; (D) BIS residual score for all; (E) BIS residual score for girls; (F) BIS residual scores for boys. The results of slope test of these regressions are shown in Supplementary Table S3. Regression lines were built using pairs of scores for MZ and DZ. “Subject 1” and “Subject 2” represent MZ or DZ twin pairs. For UR, pairs of children were randomly constructed by shuffling and splitting the sample into halves. This procedure was repeated 100 times, and mean regression lines were computed. 95% confidence intervals were calculated and are represented in the plot by shaded areas for MZ and DZ.

Figure 4

plots the correlation each of monozygotic twins (MZ), dizygotic twins and siblings (DZ) and unrelated individuals (UR) of (A) BAS residual-positive GMV correlates for all; (B) BAS residual-negative GMV correlates for all; (C) girls’ BAS residual-negative GMV correlates; (D) boys’ BAS residual-negative GMV correlates; and (E) BIS residual-negative GMV correlates for all; (F) girls’ BIS residual-positive GMV correlates; (G) boys’ BIS residual-positive GMV correlates. The results of slope test of these regressions are shown in Supplementary Table S4. Regression lines were built using pairs of average GMVs for MZ and DZ. “Subject 1” and “Subject 2” represent MZ or DZ twin pairs. For UR, pairs of children were randomly constructed by shuffling and splitting the sample into halves. This procedure was repeated 100 times, and mean regression lines were computed. 95% confidence intervals were calculated and are represented in the plot by shaded areas for MZ and DZ.