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

Nina Karolina Mikita; Emily Simonoff; Daniel S.  Pine; Robert Nicholas Goodman; Eric Artiges; Tobias Banaschewski; Arun L W Bokde; Christian Buchel; Anna Cattrell; Patricia Conrad; Sylvane Desrivieres; Vincent Frouin; Jürgen Gallinat; Hugh Garavan; Andreas Heinz; Bernd Ittermann; Sarah Jurk; Jean-Luc Martinot; Marie-Laure Paillere Martinot; F Nees; Dimitri Papadopoulos Orfanos; Tomáš Paus; Luis Poustka; Michael N. Smolka; Henrik Walter; Robert Whelan; Gunter Schumann; Argyris Stringaris

doi:10.1038/tp.2016.107

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

Nina Karolina Mikita, Emily Simonoff, Daniel S. Pine, Robert Nicholas Goodman, Eric Artiges, Tobias Banaschewski, Arun L W Bokde, Christian Buchel, Anna Cattrell, Patricia Conrad, Sylvane Desrivieres, Vincent Frouin, Jürgen Gallinat, Hugh Garavan, Andreas Heinz, Bernd Ittermann, Sarah Jurk, Jean-Luc Martinot, Marie-Laure Paillere Martinot, F NeesDimitri Papadopoulos Orfanos, Tomáš Paus, Luis Poustka, Michael N. Smolka, Henrik Walter, Robert Whelan, Gunter Schumann, Argyris Stringaris

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Abstract

Up to 40% of youth with 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 ANOVA (ASD traits: low/high, anxiety symptoms: low/high), controlling for plausible covariates. Additionally, we used a longitudinal design to assess whether neural responses during reward processing predicted anxiety at two-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<.05). BOLD activation patterns in 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.

Original language	English
Journal	Translational psychiatry
Volume	6
DOIs	https://doi.org/10.1038/tp.2016.107
Publication status	Accepted/In press - 20 Apr 2016

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Mikita, N. K., Simonoff, E., Pine, D. S., Goodman, R. N., Artiges, E., Banaschewski, T., Bokde, A. L. W., Buchel, C., Cattrell, A., Conrad, P., Desrivieres, S., Frouin, V., Gallinat, J., Garavan, H., Heinz, A., Ittermann, B., Jurk, S., Martinot, J.-L., Martinot, M.-L. P., ... Stringaris, A. (Accepted/In press). Disentangling the autism-anxiety overlap: fMRI of reward processing in a community-based longitudinal study. Translational psychiatry, 6. https://doi.org/10.1038/tp.2016.107

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title = "Disentangling the autism-anxiety overlap: fMRI of reward processing in a community-based longitudinal study",

abstract = "Up to 40% of youth with 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 ANOVA (ASD traits: low/high, anxiety symptoms: low/high), controlling for plausible covariates. Additionally, we used a longitudinal design to assess whether neural responses during reward processing predicted anxiety at two-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<.05). BOLD activation patterns in 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.",

author = "Mikita, {Nina Karolina} and Emily Simonoff and Pine, {Daniel S.} and Goodman, {Robert Nicholas} and Eric Artiges and Tobias Banaschewski and Bokde, {Arun L W} and Christian Buchel and Anna Cattrell and Patricia Conrad and Sylvane Desrivieres and Vincent Frouin and J{\"u}rgen Gallinat and Hugh Garavan and Andreas Heinz and Bernd Ittermann and Sarah Jurk and Jean-Luc Martinot and Martinot, {Marie-Laure Paillere} and F Nees and Orfanos, {Dimitri Papadopoulos} and Tom{\'a}{\v s} Paus and Luis Poustka and Smolka, {Michael N.} and Henrik Walter and Robert Whelan and Gunter Schumann and Argyris Stringaris",

year = "2016",

month = apr,

day = "20",

doi = "10.1038/tp.2016.107",

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Mikita, NK , Simonoff, E, Pine, DS, Goodman, RN, Artiges, E, Banaschewski, T, Bokde, ALW, Buchel, C, Cattrell, A, Conrad, P, Desrivieres, S, Frouin, V, Gallinat, J, Garavan, H, Heinz, A, Ittermann, B, Jurk, S, Martinot, J-L, Martinot, M-LP, Nees, F, Orfanos, DP, Paus, T, Poustka, L, Smolka, MN, Walter, H, Whelan, R, Schumann, G & Stringaris, A 2016, 'Disentangling the autism-anxiety overlap: fMRI of reward processing in a community-based longitudinal study', Translational psychiatry, vol. 6. https://doi.org/10.1038/tp.2016.107

TY - JOUR

T1 - Disentangling the autism-anxiety overlap: fMRI of reward processing in a community-based longitudinal study

AU - Mikita, Nina Karolina

AU - Simonoff, Emily

AU - Pine, Daniel S.

AU - Goodman, Robert Nicholas

AU - Artiges, Eric

AU - Banaschewski, Tobias

AU - Bokde, Arun L W

AU - Buchel, Christian

AU - Cattrell, Anna

AU - Conrad, Patricia

AU - Desrivieres, Sylvane

AU - Frouin, Vincent

AU - Gallinat, Jürgen

AU - Garavan, Hugh

AU - Heinz, Andreas

AU - Ittermann, Bernd

AU - Jurk, Sarah

AU - Martinot, Jean-Luc

AU - Martinot, Marie-Laure Paillere

AU - Nees, F

AU - Orfanos, Dimitri Papadopoulos

AU - Paus, Tomáš

AU - Poustka, Luis

AU - Smolka, Michael N.

AU - Walter, Henrik

AU - Whelan, Robert

AU - Schumann, Gunter

AU - Stringaris, Argyris

PY - 2016/4/20

Y1 - 2016/4/20

N2 - Up to 40% of youth with 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 ANOVA (ASD traits: low/high, anxiety symptoms: low/high), controlling for plausible covariates. Additionally, we used a longitudinal design to assess whether neural responses during reward processing predicted anxiety at two-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<.05). BOLD activation patterns in 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.

AB - Up to 40% of youth with 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 ANOVA (ASD traits: low/high, anxiety symptoms: low/high), controlling for plausible covariates. Additionally, we used a longitudinal design to assess whether neural responses during reward processing predicted anxiety at two-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<.05). BOLD activation patterns in 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.

U2 - 10.1038/tp.2016.107

DO - 10.1038/tp.2016.107

M3 - Article

SN - 2158-3188

VL - 6

JO - Translational psychiatry

JF - Translational psychiatry

ER -

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

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