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

PLoS One. 2014 Aug 13;9(8):e104185. doi: 10.1371/journal.pone.0104185. eCollection 2014.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Attention Deficit Disorder with Hyperactivity / epidemiology
  • Brain Mapping
  • Cerebral Cortex
  • Child
  • Child Development
  • Child, Preschool
  • Electroencephalography
  • Female
  • Humans
  • Infant
  • Magnetic Resonance Imaging
  • Male
  • Motivation
  • Neostriatum
  • Prospective Studies
  • Reaction Time
  • Reward*
  • Risk Factors
  • Stress, Psychological*

Grants and funding

This work was supported by grants from the German Research Foundation (DFG LA 733/1–2) to ML, DB, TB, and AML. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.