Adolescent behavioral and neural reward sensitivity: a test of the differential susceptibility theory.

J S Richards,J Oosterlaan,D J Heslenfeld,A Arias Vásquez,D Van Der Meer,D Von Rhein,C A Hartman,S V Faraone,J K Buitelaar,P J Hoekstra,B Franke

doi:10.1038/tp.2016.37

Abstract

Little is known about the causes of individual differences in reward sensitivity. We investigated gene–environment interactions (GxE) on behavioral and neural measures of reward sensitivity, in light of the differential susceptibility theory. This theory states that individuals carrying plasticity gene variants will be more disadvantaged in negative, but more advantaged in positive environments. Reward responses were assessed during a monetary incentive delay task in 178 participants with and 265 without attention-deficit/hyperactivity disorder (ADHD), from N=261 families. We examined interactions between variants in candidate plasticity genes (DAT1, 5-HTT and DRD4) and social environments (maternal expressed emotion and peer affiliation). HTTLPR short allele carriers showed the least reward speeding when exposed to high positive peer affiliation, but the most when faced with low positive peer affiliation or low maternal warmth. DAT1 10-repeat homozygotes displayed similar GxE patterns toward maternal warmth on general task performance. At the neural level, DRD4 7-repeat carriers showed the least striatal activation during reward anticipation when exposed to high maternal warmth, but the most when exposed to low warmth. Findings were independent of ADHD severity. Our results partially confirm the differential susceptibility theory and indicate the importance of positive social environments in reward sensitivity and general task performance for persons with specific genotypes.

Highlights

Reward sensitivity is an evolutionary important construct; rewards bring about positive feelings, and thereby reinforce the behavior associated with them, enabling learning.[1]
Given its relevance in child development and previous associations with reward sensitivity[19,21,22,23] we focused on the social environment, which was studied through maternal expressed emotions (EEs) and peer affiliation
A significant rGE was found between adolescent dopamine receptor D4 (DRD4) genotype and deviant peer affiliation (r = 0.11, P = 0.028; Supplementary Table S1)

Summary

INTRODUCTION

Reward sensitivity is an evolutionary important construct; rewards bring about positive feelings, and thereby reinforce the behavior associated with them, enabling learning.[1]. Repeat allele of the variable number of tandem repeat polymorphism in exon 3 preferred immediate smaller over delayed larger rewards sooner when raised in low socioeconomic status families, but far less when not.[26] The fact that in both studies genetic variants moderated the sensitivity toward positive and negative environmental influences is in line with the differential susceptibility theory.[27] This theory states that individuals differ in the dopamine transporter gene (SLC6A3/ DAT1) These genes have been frequently linked to ADHD42 and shown to act as plasticity genes in children with and without ADHD.[43]. This view extends the commonly applied diathesis-stress or dual-risk models, which focus only on the vulnerability to adverse effects of negative environments, referring to genes involved in GxE as ‘vulnerability genes’.29,30 Support for the differential susceptibility theory comes from various studies in other contexts, there have been negative findings see for a recent review Belsky et al.[31]

Participants

RESULTS

DISCUSSION