Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Boecker, Regina, Holz, Nathalie E., Buchmann, Arlette F., Blomeyer, Dorothea, Plichta, Michael M., Wolf, Isabella, Baumeister, Sarah, Meyer-Lindenberg, Andreas, Banaschewski, Tobias, Brandeis, Daniel, Laucht, Manfred
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4131910/
https://www.ncbi.nlm.nih.gov/pubmed/25118701
http://dx.doi.org/10.1371/journal.pone.0104185
_version_ 1782330539323162624
author Boecker, Regina
Holz, Nathalie E.
Buchmann, Arlette F.
Blomeyer, Dorothea
Plichta, Michael M.
Wolf, Isabella
Baumeister, Sarah
Meyer-Lindenberg, Andreas
Banaschewski, Tobias
Brandeis, Daniel
Laucht, Manfred
author_facet Boecker, Regina
Holz, Nathalie E.
Buchmann, Arlette F.
Blomeyer, Dorothea
Plichta, Michael M.
Wolf, Isabella
Baumeister, Sarah
Meyer-Lindenberg, Andreas
Banaschewski, Tobias
Brandeis, Daniel
Laucht, Manfred
author_sort Boecker, Regina
collection PubMed
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.
format Online
Article
Text
id pubmed-4131910
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-41319102014-08-19 Impact of Early Life Adversity on Reward Processing in Young Adults: EEG-fMRI Results from a Prospective Study over 25 Years Boecker, Regina Holz, Nathalie E. Buchmann, Arlette F. Blomeyer, Dorothea Plichta, Michael M. Wolf, Isabella Baumeister, Sarah Meyer-Lindenberg, Andreas Banaschewski, Tobias Brandeis, Daniel Laucht, Manfred PLoS One Research Article 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. Public Library of Science 2014-08-13 /pmc/articles/PMC4131910/ /pubmed/25118701 http://dx.doi.org/10.1371/journal.pone.0104185 Text en © 2014 Boecker et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Boecker, Regina
Holz, Nathalie E.
Buchmann, Arlette F.
Blomeyer, Dorothea
Plichta, Michael M.
Wolf, Isabella
Baumeister, Sarah
Meyer-Lindenberg, Andreas
Banaschewski, Tobias
Brandeis, Daniel
Laucht, Manfred
Impact of Early Life Adversity on Reward Processing in Young Adults: EEG-fMRI Results from a Prospective Study over 25 Years
title 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_short 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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4131910/
https://www.ncbi.nlm.nih.gov/pubmed/25118701
http://dx.doi.org/10.1371/journal.pone.0104185
work_keys_str_mv AT boeckerregina impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years
AT holznathaliee impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years
AT buchmannarlettef impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years
AT blomeyerdorothea impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years
AT plichtamichaelm impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years
AT wolfisabella impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years
AT baumeistersarah impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years
AT meyerlindenbergandreas impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years
AT banaschewskitobias impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years
AT brandeisdaniel impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years
AT lauchtmanfred impactofearlylifeadversityonrewardprocessinginyoungadultseegfmriresultsfromaprospectivestudyover25years