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Transl Psychiatry. 2016 Jun 28;6(6):e845. doi: 10.1038/tp.2016.107.

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

Author information

1
Department of Child and Adolescent Psychiatry, King's CollegeLondon, Institute of Psychiatry, Psychology & Neuroscience, London, UK.
2
NIHR Biomedical Research Centre and Dementia Unit at SouthLondon and Maudsley NHS Foundation Trust and the Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
3
Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD, USA.
4
Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 "Neuroimaging & Psychiatry", Service Hospitalier Frédéric Joliot, Orsay, France.
5
University Paris-Sud 11, Orsay, France.
6
University Paris Descartes - Sorbonne Paris Cité, Paris, France.
7
Psychiatry Department, Orsay Hospital, Orsay, France.
8
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
9
Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College, Dublin, Ireland.
10
University Medical Centre Hamburg-Eppendorf, Hamburg, Germany.
11
Medical Research Council - Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
12
Department of Psychiatry, Universite de Montreal, CHU Ste Justine Hospital, Montreal, QC, Canada.
13
Department of Psychological Medicine and Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
14
Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
15
Neurospin, Commissariat à l'Energie Atomique, CEA-Saclay Center, Paris, France.
16
Department of Psychiatry and Psychotherapy, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
17
Department of Psychiatry, University of Vermont, Burlington, VT, USA.
18
Department of Psychology, University of Vermont, Burlington, VT, USA.
19
Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin, Berlin, Germany.
20
Physikalisch-Technische Bundesanstalt, Braunschweig, Germany.
21
Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
22
AP-HP, Department of Adolescent Psychopathology and Medicine, Maison de Solenn, Cochin Hospital, Paris, France.
23
Rotman Research Institute, Baycrest, Toronto, ON, Canada.
24
Child Mind Institute, New York, NY, USA.
25
Department of Psychology, University of Toronto, Toronto, ON, Canada.
26
Department of Psychiatry, University of Toronto, Toronto, ON, Canada.
27
Department of Child and Adolescent Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria.
28
Department of Psychology, University College Dublin, Dublin, Ireland.

Abstract

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.

PMID:
27351599
PMCID:
PMC4931605
DOI:
10.1038/tp.2016.107
[Indexed for MEDLINE]
Free PMC Article

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