Disentangling the autism−anxiety overlap: fMRI of reward processing in a community-based longitudinal study

Up to 40% of youth with autism spectrum disorder (ASD) also suffer from anxiety, and this comorbidity is linked with significant functional impairment. However, the mechanisms of this overlap are poorly understood. We investigated the interplay between ASD traits and anxiety during reward processing...

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Main Authors: Mikita, N, Simonoff, E, Pine, D S, Goodman, R, Artiges, E, Banaschewski, T, Bokde, A L, Bromberg, U, Büchel, C, Cattrell, A, Conrod, P J, Desrivières, S, Flor, H, Frouin, V, Gallinat, J, Garavan, H, Heinz, A, Ittermann, B, Jurk, S, Martinot, J L, Paillère Martinot, M L, Nees, F, Papadopoulos Orfanos, D, Paus, T, Poustka, L, Smolka, M N, Walter, H, Whelan, R, Schumann, G, Stringaris, A
Format: Online
Language:English
Published: Nature Publishing Group 2016
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4931605/
id pubmed-4931605
recordtype oai_dc
spelling pubmed-49316052016-07-05 Disentangling the autism−anxiety overlap: fMRI of reward processing in a community-based longitudinal study Mikita, N Simonoff, E Pine, D S Goodman, R Artiges, E Banaschewski, T Bokde, A L Bromberg, U Büchel, C Cattrell, A Conrod, P J Desrivières, S Flor, H Frouin, V Gallinat, J Garavan, H Heinz, A Ittermann, B Jurk, S Martinot, J L Paillère Martinot, M L Nees, F Papadopoulos Orfanos, D Paus, T Poustka, L Smolka, M N Walter, H Whelan, R Schumann, G Stringaris, A Original Article Up to 40% of youth with autism spectrum disorder (ASD) also suffer from anxiety, and this comorbidity is linked with significant functional impairment. However, the mechanisms of this overlap are poorly understood. We investigated the interplay between ASD traits and anxiety during reward processing, known to be affected in ASD, in a community sample of 1472 adolescents (mean age=14.4 years) who performed a modified monetary incentive delay task as part of the Imagen project. Blood-oxygen-level dependent (BOLD) responses to reward anticipation and feedback were compared using a 2x2 analysis of variance test (ASD traits: low/high; anxiety symptoms: low/high), controlling for plausible covariates. In addition, we used a longitudinal design to assess whether neural responses during reward processing predicted anxiety at 2-year follow-up. High ASD traits were associated with reduced BOLD responses in dorsal prefrontal regions during reward anticipation and negative feedback. Participants with high anxiety symptoms showed increased lateral prefrontal responses during anticipation, but decreased responses following feedback. Interaction effects revealed that youth with combined ASD traits and anxiety, relative to other youth, showed high right insula activation when anticipating reward, and low right-sided caudate, putamen, medial and lateral prefrontal activations during negative feedback (all clusters PFWE<0.05). BOLD activation patterns in the right dorsal cingulate and right medial frontal gyrus predicted new-onset anxiety in participants with high but not low ASD traits. Our results reveal both quantitatively enhanced and qualitatively distinct neural correlates underlying the comorbidity between ASD traits and anxiety. Specific neural responses during reward processing may represent a risk factor for developing anxiety in ASD youth. Nature Publishing Group 2016-06 2016-06-28 /pmc/articles/PMC4931605/ /pubmed/27351599 http://dx.doi.org/10.1038/tp.2016.107 Text en Copyright © 2016 Macmillan Publishers Limited http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Mikita, N
Simonoff, E
Pine, D S
Goodman, R
Artiges, E
Banaschewski, T
Bokde, A L
Bromberg, U
Büchel, C
Cattrell, A
Conrod, P J
Desrivières, S
Flor, H
Frouin, V
Gallinat, J
Garavan, H
Heinz, A
Ittermann, B
Jurk, S
Martinot, J L
Paillère Martinot, M L
Nees, F
Papadopoulos Orfanos, D
Paus, T
Poustka, L
Smolka, M N
Walter, H
Whelan, R
Schumann, G
Stringaris, A
spellingShingle Mikita, N
Simonoff, E
Pine, D S
Goodman, R
Artiges, E
Banaschewski, T
Bokde, A L
Bromberg, U
Büchel, C
Cattrell, A
Conrod, P J
Desrivières, S
Flor, H
Frouin, V
Gallinat, J
Garavan, H
Heinz, A
Ittermann, B
Jurk, S
Martinot, J L
Paillère Martinot, M L
Nees, F
Papadopoulos Orfanos, D
Paus, T
Poustka, L
Smolka, M N
Walter, H
Whelan, R
Schumann, G
Stringaris, A
Disentangling the autism−anxiety overlap: fMRI of reward processing in a community-based longitudinal study
author_facet Mikita, N
Simonoff, E
Pine, D S
Goodman, R
Artiges, E
Banaschewski, T
Bokde, A L
Bromberg, U
Büchel, C
Cattrell, A
Conrod, P J
Desrivières, S
Flor, H
Frouin, V
Gallinat, J
Garavan, H
Heinz, A
Ittermann, B
Jurk, S
Martinot, J L
Paillère Martinot, M L
Nees, F
Papadopoulos Orfanos, D
Paus, T
Poustka, L
Smolka, M N
Walter, H
Whelan, R
Schumann, G
Stringaris, A
author_sort Mikita, N
title Disentangling the autism−anxiety overlap: fMRI of reward processing in a community-based longitudinal study
title_short Disentangling the autism−anxiety overlap: fMRI of reward processing in a community-based longitudinal study
title_full Disentangling the autism−anxiety overlap: fMRI of reward processing in a community-based longitudinal study
title_fullStr Disentangling the autism−anxiety overlap: fMRI of reward processing in a community-based longitudinal study
title_full_unstemmed Disentangling the autism−anxiety overlap: fMRI of reward processing in a community-based longitudinal study
title_sort disentangling the autism−anxiety overlap: fmri of reward processing in a community-based longitudinal study
description Up to 40% of youth with autism spectrum disorder (ASD) also suffer from anxiety, and this comorbidity is linked with significant functional impairment. However, the mechanisms of this overlap are poorly understood. We investigated the interplay between ASD traits and anxiety during reward processing, known to be affected in ASD, in a community sample of 1472 adolescents (mean age=14.4 years) who performed a modified monetary incentive delay task as part of the Imagen project. Blood-oxygen-level dependent (BOLD) responses to reward anticipation and feedback were compared using a 2x2 analysis of variance test (ASD traits: low/high; anxiety symptoms: low/high), controlling for plausible covariates. In addition, we used a longitudinal design to assess whether neural responses during reward processing predicted anxiety at 2-year follow-up. High ASD traits were associated with reduced BOLD responses in dorsal prefrontal regions during reward anticipation and negative feedback. Participants with high anxiety symptoms showed increased lateral prefrontal responses during anticipation, but decreased responses following feedback. Interaction effects revealed that youth with combined ASD traits and anxiety, relative to other youth, showed high right insula activation when anticipating reward, and low right-sided caudate, putamen, medial and lateral prefrontal activations during negative feedback (all clusters PFWE<0.05). BOLD activation patterns in the right dorsal cingulate and right medial frontal gyrus predicted new-onset anxiety in participants with high but not low ASD traits. Our results reveal both quantitatively enhanced and qualitatively distinct neural correlates underlying the comorbidity between ASD traits and anxiety. Specific neural responses during reward processing may represent a risk factor for developing anxiety in ASD youth.
publisher Nature Publishing Group
publishDate 2016
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4931605/
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