Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years.

Regina Boecker,Arlette F Buchmann,Dorothea Blomeyer,Tobias Banaschewski,Sarah Baumeister,Andreas Meyer-Lindenberg,Manfred Laucht,Nathalie E Holz,Michael M Plichta,Daniel Brandeis,Isabella Wolf

doi:10.1371/journal.pone.0104185

Abstract

Several lines of evidence have implicated the mesolimbic dopamine reward pathway in altered brain function resulting from exposure to early adversity. The present study examined the impact of early life adversity on different stages of neuronal reward processing later in life and their association with a related behavioral phenotype, i.e. attention deficit/hyperactivity disorder (ADHD). 162 healthy young adults (mean age = 24.4 years; 58% female) from an epidemiological cohort study followed since birth participated in a simultaneous EEG-fMRI study using a monetary incentive delay task. Early life adversity according to an early family adversity index (EFA) and lifetime ADHD symptoms were assessed using standardized parent interviews conducted at the offspring's age of 3 months and between 2 and 15 years, respectively. fMRI region-of-interest analysis revealed a significant effect of EFA during reward anticipation in reward-related areas (i.e. ventral striatum, putamen, thalamus), indicating decreased activation when EFA increased. EEG analysis demonstrated a similar effect for the contingent negative variation (CNV), with the CNV decreasing with the level of EFA. In contrast, during reward delivery, activation of the bilateral insula, right pallidum and bilateral putamen increased with EFA. There was a significant association of lifetime ADHD symptoms with lower activation in the left ventral striatum during reward anticipation and higher activation in the right insula during reward delivery. The present findings indicate a differential long-term impact of early life adversity on reward processing, implicating hyporesponsiveness during reward anticipation and hyperresponsiveness when receiving a reward. Moreover, a similar activation pattern related to lifetime ADHD suggests that the impact of early life stress on ADHD may possibly be mediated by a dysfunctional reward pathway.

Highlights

Accumulating evidence suggests that adversity in early childhood may impair human brain development and mental health later in life [1,2,3]
A significant effect of early family adversity index (EFA) on Reaction times (RT) of monetary trials emerged (F(1,160) = 9.22, p = .003), with RT increasing with the level of adversity
Our findings demonstrated a differential impact of adversity on neural responding to distinct phases of reward processing, indicating that the activation of specific reward-related brain areas (VS, putamen, thalamus) decreased with the level of adversity during reward anticipation, while there was an increase in activity of other reward-related areas with the level of adversity during reward delivery

Summary

Introduction

Accumulating evidence suggests that adversity in early childhood may impair human brain development and mental health later in life [1,2,3]. Several functionally related brain regions have been implicated in the processing of rewards by a large body of functional magnetic resonance imaging (fMRI) findings and have been related to different stages of reward processing [11,12]. These findings emphasize a functional dissection of reward processing. While anticipation or ‘‘wanting’’ of a reward addresses the motivational aspect to receive a reward, reward delivery or ‘‘liking’’ has been interpreted as the hedonic impact of a reward producing the feeling of pleasure [13]

Methods

Results

Discussion

Conclusion