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

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 w...

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Main Authors: Regina Boecker, Nathalie E Holz, Arlette F Buchmann, Dorothea Blomeyer, Michael M Plichta, Isabella Wolf, Sarah Baumeister, Andreas Meyer-Lindenberg, Tobias Banaschewski, Daniel Brandeis, Manfred Laucht
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4131910?pdf=render
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spelling doaj-0ae3b82b204a4b8ab05488b70ed1d89c2020-11-24T21:38:21ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0198e10418510.1371/journal.pone.0104185Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years.Regina BoeckerNathalie E HolzArlette F BuchmannDorothea BlomeyerMichael M PlichtaIsabella WolfSarah BaumeisterAndreas Meyer-LindenbergTobias BanaschewskiDaniel BrandeisManfred LauchtSeveral 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.http://europepmc.org/articles/PMC4131910?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Regina Boecker
Nathalie E Holz
Arlette F Buchmann
Dorothea Blomeyer
Michael M Plichta
Isabella Wolf
Sarah Baumeister
Andreas Meyer-Lindenberg
Tobias Banaschewski
Daniel Brandeis
Manfred Laucht
spellingShingle Regina Boecker
Nathalie E Holz
Arlette F Buchmann
Dorothea Blomeyer
Michael M Plichta
Isabella Wolf
Sarah Baumeister
Andreas Meyer-Lindenberg
Tobias Banaschewski
Daniel Brandeis
Manfred Laucht
Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years.
PLoS ONE
author_facet Regina Boecker
Nathalie E Holz
Arlette F Buchmann
Dorothea Blomeyer
Michael M Plichta
Isabella Wolf
Sarah Baumeister
Andreas Meyer-Lindenberg
Tobias Banaschewski
Daniel Brandeis
Manfred Laucht
author_sort Regina Boecker
title Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years.
title_short Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years.
title_full Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years.
title_fullStr Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years.
title_full_unstemmed Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years.
title_sort impact of early life adversity on reward processing in young adults: eeg-fmri results from a prospective study over 25 years.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2014-01-01
description 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.
url http://europepmc.org/articles/PMC4131910?pdf=render
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