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Distinct effects of ASD and ADHD symptoms on reward anticipation in participants with ADHD, their unaffected siblings and healthy controls: a cross-sectional study

BACKGROUND: Autism spectrum disorder (ASD) traits are continuously distributed throughout the population, and ASD symptoms are also frequently observed in patients with attention-deficit/hyperactivity disorder (ADHD). Both ASD and ADHD have been linked to alterations in reward-related neural process...

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Autores principales: van Dongen, Eelco V., von Rhein, Daniel, O’Dwyer, Laurence, Franke, Barbara, Hartman, Catharina A., Heslenfeld, Dirk J., Hoekstra, Pieter J., Oosterlaan, Jaap, Rommelse, Nanda, Buitelaar, Jan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4551566/
https://www.ncbi.nlm.nih.gov/pubmed/26322219
http://dx.doi.org/10.1186/s13229-015-0043-y
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author van Dongen, Eelco V.
von Rhein, Daniel
O’Dwyer, Laurence
Franke, Barbara
Hartman, Catharina A.
Heslenfeld, Dirk J.
Hoekstra, Pieter J.
Oosterlaan, Jaap
Rommelse, Nanda
Buitelaar, Jan
author_facet van Dongen, Eelco V.
von Rhein, Daniel
O’Dwyer, Laurence
Franke, Barbara
Hartman, Catharina A.
Heslenfeld, Dirk J.
Hoekstra, Pieter J.
Oosterlaan, Jaap
Rommelse, Nanda
Buitelaar, Jan
author_sort van Dongen, Eelco V.
collection PubMed
description BACKGROUND: Autism spectrum disorder (ASD) traits are continuously distributed throughout the population, and ASD symptoms are also frequently observed in patients with attention-deficit/hyperactivity disorder (ADHD). Both ASD and ADHD have been linked to alterations in reward-related neural processing. However, whether both symptom domains interact and/or have distinct effects on reward processing in healthy and ADHD populations is currently unknown. METHODS: We examined how variance in ASD and ADHD symptoms in individuals with ADHD and healthy participants was related to the behavioural and neural response to reward during a monetary incentive delay (MID) task. Participants (mean age: 17.7 years, range: 10–28 years) from the NeuroIMAGE study with a confirmed diagnosis of ADHD (n = 136), their unaffected siblings (n = 83), as well as healthy controls (n = 105) performed an MID task in a magnetic resonance imaging (MRI) scanner. ASD and ADHD symptom scores were used as predictors of the neural response to reward anticipation and reward receipt. Behavioural responses were modeled using linear mixed models; neural responses were analysed using FMRIB’s Software Library (FSL) proprietary mixed effects analysis (FLAMEO). RESULTS: ASD and ADHD symptoms were associated with alterations in BOLD activity during reward anticipation, but not reward receipt. Specifically, ASD scores were related to increased insular activity during reward anticipation across the sample. No interaction was found between this effect and the presence of ADHD, suggesting that ASD symptoms had no differential effect in ADHD and healthy populations. ADHD symptom scores were associated with reduced dorsolateral prefrontal activity during reward anticipation. No interactions were found between the effects of ASD and ADHD symptoms on reward processing. CONCLUSIONS: Variance in ASD and ADHD symptoms separately influence neural processing during reward anticipation in both individuals with (an increased risk of) ADHD and healthy participants. Our findings therefore suggest that both symptom domains affect reward processing through distinct mechanisms, underscoring the importance of multidimensional and multimodal assessment in psychiatry. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13229-015-0043-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-45515662015-08-29 Distinct effects of ASD and ADHD symptoms on reward anticipation in participants with ADHD, their unaffected siblings and healthy controls: a cross-sectional study van Dongen, Eelco V. von Rhein, Daniel O’Dwyer, Laurence Franke, Barbara Hartman, Catharina A. Heslenfeld, Dirk J. Hoekstra, Pieter J. Oosterlaan, Jaap Rommelse, Nanda Buitelaar, Jan Mol Autism Research BACKGROUND: Autism spectrum disorder (ASD) traits are continuously distributed throughout the population, and ASD symptoms are also frequently observed in patients with attention-deficit/hyperactivity disorder (ADHD). Both ASD and ADHD have been linked to alterations in reward-related neural processing. However, whether both symptom domains interact and/or have distinct effects on reward processing in healthy and ADHD populations is currently unknown. METHODS: We examined how variance in ASD and ADHD symptoms in individuals with ADHD and healthy participants was related to the behavioural and neural response to reward during a monetary incentive delay (MID) task. Participants (mean age: 17.7 years, range: 10–28 years) from the NeuroIMAGE study with a confirmed diagnosis of ADHD (n = 136), their unaffected siblings (n = 83), as well as healthy controls (n = 105) performed an MID task in a magnetic resonance imaging (MRI) scanner. ASD and ADHD symptom scores were used as predictors of the neural response to reward anticipation and reward receipt. Behavioural responses were modeled using linear mixed models; neural responses were analysed using FMRIB’s Software Library (FSL) proprietary mixed effects analysis (FLAMEO). RESULTS: ASD and ADHD symptoms were associated with alterations in BOLD activity during reward anticipation, but not reward receipt. Specifically, ASD scores were related to increased insular activity during reward anticipation across the sample. No interaction was found between this effect and the presence of ADHD, suggesting that ASD symptoms had no differential effect in ADHD and healthy populations. ADHD symptom scores were associated with reduced dorsolateral prefrontal activity during reward anticipation. No interactions were found between the effects of ASD and ADHD symptoms on reward processing. CONCLUSIONS: Variance in ASD and ADHD symptoms separately influence neural processing during reward anticipation in both individuals with (an increased risk of) ADHD and healthy participants. Our findings therefore suggest that both symptom domains affect reward processing through distinct mechanisms, underscoring the importance of multidimensional and multimodal assessment in psychiatry. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13229-015-0043-y) contains supplementary material, which is available to authorized users. BioMed Central 2015-08-28 /pmc/articles/PMC4551566/ /pubmed/26322219 http://dx.doi.org/10.1186/s13229-015-0043-y Text en © van Dongen et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
van Dongen, Eelco V.
von Rhein, Daniel
O’Dwyer, Laurence
Franke, Barbara
Hartman, Catharina A.
Heslenfeld, Dirk J.
Hoekstra, Pieter J.
Oosterlaan, Jaap
Rommelse, Nanda
Buitelaar, Jan
Distinct effects of ASD and ADHD symptoms on reward anticipation in participants with ADHD, their unaffected siblings and healthy controls: a cross-sectional study
title Distinct effects of ASD and ADHD symptoms on reward anticipation in participants with ADHD, their unaffected siblings and healthy controls: a cross-sectional study
title_full Distinct effects of ASD and ADHD symptoms on reward anticipation in participants with ADHD, their unaffected siblings and healthy controls: a cross-sectional study
title_fullStr Distinct effects of ASD and ADHD symptoms on reward anticipation in participants with ADHD, their unaffected siblings and healthy controls: a cross-sectional study
title_full_unstemmed Distinct effects of ASD and ADHD symptoms on reward anticipation in participants with ADHD, their unaffected siblings and healthy controls: a cross-sectional study
title_short Distinct effects of ASD and ADHD symptoms on reward anticipation in participants with ADHD, their unaffected siblings and healthy controls: a cross-sectional study
title_sort distinct effects of asd and adhd symptoms on reward anticipation in participants with adhd, their unaffected siblings and healthy controls: a cross-sectional study
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4551566/
https://www.ncbi.nlm.nih.gov/pubmed/26322219
http://dx.doi.org/10.1186/s13229-015-0043-y
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