Lower neighborhood quality in adolescence predicts higher mesolimbic sensitivity to reward anticipation in adulthood

Abstract

Life history theory suggests that adult reward sensitivity should be best explained by childhood, but not current, socioeconomic conditions. In this functional magnetic resonance imaging (fMRI) study, 83 participants from a larger longitudinal sample completed the monetary incentive delay (MID) task in adulthood (∼25 years old). Parent-reports of neighborhood quality and parental SES were collected when participants were 13 years of age. Current income level was collected concurrently with scanning. Lower adolescent neighborhood quality, but neither lower current income nor parental SES, was associated with heightened sensitivity to the anticipation of monetary gain in putative mesolimbic reward areas. Lower adolescent neighborhood quality was also associated with heightened sensitivity to the anticipation of monetary loss activation in visuo-motor areas. Lower current income was associated with heightened sensitivity to anticipated loss in occipital areas and the operculum. We tested whether externalizing behaviors in childhood or adulthood could better account for neighborhood quality findings, but they did not. Findings suggest that neighborhood ecology in adolescence is associated with greater neural reward sensitivity in adulthood above the influence of parental SES or current income and not mediated through impulsivity and externalizing behaviors.

Fig. 1

Flow diagram of MID task. Cues signaling monetary gain, loss, or no consequence in the MID paradigm are on the upper right of the figure. Each run consisted of 72 trials with 27 reward cues, 27 punishment cues, and 18 neutral cues. The participants are taught the cues first by an experimenter and then by the practice run.

Fig. 2

Visualization of areas with greater activation in the Reward > Neutral contrasts at the group level. Images were FDR corrected (q =0.01) and overlaid on to the MNI T1 wted high resolution anatomical image. Coronal (A) and Axial (B) slices located at Y = 16, Z = −8.

Fig. 3

Visualization of areas with greater activation in the Punishment > Neutral contrasts at the group level. Images were FDR corrected (q = 0.01) and overlaid on to the MNI T1 wted high resolution anatomical image. Axial (A) and Saggital (B) slices are located at X = 2, Y = 16, Z = 42.

Fig. 4

Coronal (A), sagittal (B & C), and axial (D) visualizations of clusters negatively correlated with adolescent neighborhood quality in the Reward > Neutral contrast at the group level. Images’ slice locations are below them. The “L Orbital frontal cortex” in image B is an extension of the “striatum” cluster in image A.

Fig. 5

Axial (A) slice of clusters negatively correlated with Current Income in the Punishment > Neutral contrast at the group level. Image located at Z = 18.

Fig. 6

Higher adolescent Neighborhood Quality (centered) is associated with lower average BOLD activation (displayed here in average Z statistic for the NAcc mask used). One outlier was removed due to excess leverage. Removal of this outlier does not change interpretation. Image on the right is a coronal slice (Y = 20) showing the binarized NaCC mask from the Harvard- Oxford Subcortical Atlas.