Developmental changes in fronto-striatal glutamate and their association with functioning during inhibitory control in autism spectrum disorder and obsessive compulsive disorder

Viola Hollestein; Jan K. Buitelaar; Daniel Brandeis; Tobias Banaschewski; Anna Kaiser; Sarah Hohmann; Bob Oranje; Bram Gooskens; Sarah Durston; Steven C.R. Williams; David J. Lythgoe; Jilly Naaijen

NeuroImage: Clinical (Jan 2021)

Developmental changes in fronto-striatal glutamate and their association with functioning during inhibitory control in autism spectrum disorder and obsessive compulsive disorder

Viola Hollestein,
Jan K. Buitelaar,
Daniel Brandeis,
Tobias Banaschewski,
Anna Kaiser,
Sarah Hohmann,
Bob Oranje,
Bram Gooskens,
Sarah Durston,
Steven C.R. Williams,
David J. Lythgoe,
Jilly Naaijen

Affiliations

Viola Hollestein: Department of Cognitive Neuroscience, Donders Institute of Brain, Cognition and Behaviour, Radboud University Medical Center, the Netherlands; Corresponding author at: Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behavior, Radboud University Medical Center, P.O Box 9101, 6500 HB Nijmegen, the Netherlands.
Jan K. Buitelaar: Department of Cognitive Neuroscience, Donders Institute of Brain, Cognition and Behaviour, Radboud University Medical Center, the Netherlands; Karakter Child and Adolescent Psychiatry University Center, Nijmegen, the Netherlands
Daniel Brandeis: Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty, Mannheim/Heidelberg University, Mannheim, Germany; Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich, Switzerland; Center for Integrative Human Physiology, University of Zurich, Zurich, Switzerland; Neuroscience Center Zurich, University of Zurich, Zurich, Switzerland; ETH Zurich, Zurich, Switzerland
Tobias Banaschewski: Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty, Mannheim/Heidelberg University, Mannheim, Germany
Anna Kaiser: Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty, Mannheim/Heidelberg University, Mannheim, Germany
Sarah Hohmann: Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty, Mannheim/Heidelberg University, Mannheim, Germany
Bob Oranje: Department of Psychiatry, Brain Center, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
Bram Gooskens: Department of Psychiatry, Brain Center, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
Sarah Durston: Department of Psychiatry, Brain Center, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
Steven C.R. Williams: Department of Neuroimaging, King’s College London, Institute of Psychiatry, Psychology and Neuroscience, London, United Kingdom
David J. Lythgoe: Department of Neuroimaging, King’s College London, Institute of Psychiatry, Psychology and Neuroscience, London, United Kingdom
Jilly Naaijen: Department of Cognitive Neuroscience, Donders Institute of Brain, Cognition and Behaviour, Radboud University Medical Center, the Netherlands; Donders Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University, the Netherlands

Journal volume & issue: Vol. 30
p. 102622

Abstract

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Autism spectrum disorder (ASD) and obsessive compulsive disorder (OCD) show overlapping symptomatology and deficits in inhibitory control, which are associated with altered functioning and glutamatergic signaling in fronto-striatal circuitry. These parameters have never been examined together. The purpose of the current study was to investigate functioning during inhibitory control and its association with fronto-striatal glutamate concentrations across these disorders using a multi-center, longitudinal approach. Adolescents with ASD (n = 24), OCD (n = 15) and controls (n = 35) underwent two magnetic resonance imaging (MRI) sessions with a one-year interval. This included proton magnetic resonance spectroscopy (1H-MRS; n = 74) and functional MRI during an inhibitory control task (n = 53). We investigated 1H-MRS data and fMRI data separately as well as integrated in a multimodal analysis using linear models focusing on diagnosis and continuous measures of overlapping compulsivity symptoms. ACC glutamate was reduced over time in the ASD group compared with controls, while striatal glutamate decreased over time independent of diagnosis. Increased compulsive behavior seemed to be associated with increased striatal activity during failed inhibitory control. The integrated analyses showed differential involvement of increased striatal glutamate during failed but decreased striatal glutamate during successful inhibitory control in the OCD group compared to controls and ASD, suggesting different underlying mechanisms for OCD compared to ASD.

Published in NeuroImage: Clinical

ISSN: 2213-1582 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General): Computer applications to medicine. Medical informatics; Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry: Neurology. Diseases of the nervous system
Website: http://www.journals.elsevier.com/neuroimage-clinical/

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