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

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.

Figure 1. MID paradigm.

The task requires a fast button press after a flash, indicated by either a laughing or a scrambled smiley, to receive either monetary or verbal feedback.

Figure 2

Left: neuronal activity (p_FWE<.05; ROI corr.) for the contrast monetary > verbal reward during reward anticipation by early family adversity (EFA) in a) left VS, b) left putamen and c) left thalamus; right: scatterplots of the correlations between the mean BOLD response of the respective regions and EFA; d) left: Scalp distribution of CNV difference (monetary > verbal condition; mean difference: 2–3 sec after stimulus presentation) dependent on EFA; right: scatterplot of the correlation between CNV difference at Cz (marked with an asterisk) and EFA [F_(1,160) = 9.14, p = .003].

Figure 3

Left: neuronal activity (p_FWE<.05; ROI corr.) for the contrast win > no-win trials during reward delivery by EFA in a) right insula, b) right pallidum and c) left putamen; right: scatterplots of the correlations between the mean BOLD response of the respective regions and EFA.

Figure 4

Left: neuronal activity (p_FWE<.05; ROI corr.) for the contrast verbal win > no-win trials during reward delivery by EFA in a) right pallidum, b) right insula, c) left substantia nigra and d) right posterior hippocampus; right: scatterplots of the correlations between the mean BOLD response of the respective regions and EFA.