Reduced inferior fronto-insular-thalamic activation during failed inhibition in young adults with combined ASD and ADHD compared to typically developing and pure disorder groups

Abstract Autism spectrum disorder (ASD) often co-occurs with attention-deficit/hyperactivity disorder (ADHD) and people with these conditions have frontostriatal functional atypicality during motor inhibition. We compared the neural and neurocognitive correlates of motor inhibition and performance m...

Full description

Bibliographic Details
Main Authors: Steve Lukito, Owen G. O’Daly, David J. Lythgoe, John Hodsoll, Stefanos Maltezos, Mark Pitts, Emily Simonoff, Katya Rubia
Format: Article
Language:English
Published: Nature Publishing Group 2023-04-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-023-02431-4
_version_ 1827961106955501568
author Steve Lukito
Owen G. O’Daly
David J. Lythgoe
John Hodsoll
Stefanos Maltezos
Mark Pitts
Emily Simonoff
Katya Rubia
author_facet Steve Lukito
Owen G. O’Daly
David J. Lythgoe
John Hodsoll
Stefanos Maltezos
Mark Pitts
Emily Simonoff
Katya Rubia
author_sort Steve Lukito
collection DOAJ
description Abstract Autism spectrum disorder (ASD) often co-occurs with attention-deficit/hyperactivity disorder (ADHD) and people with these conditions have frontostriatal functional atypicality during motor inhibition. We compared the neural and neurocognitive correlates of motor inhibition and performance monitoring in young adult males with “pure” and combined presentations with age-and sex-matched typically developing controls, to explore shared or disorder-specific atypicality. Males aged 20–27 years with typical development (TD; n = 22), ASD (n = 21), combined diagnoses ASD + ADHD (n = 23), and ADHD (n = 25) were compared using a modified tracking fMRI stop-signal task that measures motor inhibition and performance monitoring while controlling for selective attention. In addition, they performed a behavioural go/no-go task outside the scanner. While groups did not differ behaviourally during successful stop trials, the ASD + ADHD group relative to other groups had underactivation in typical performance monitoring regions of bilateral anterior insula/inferior frontal gyrus, right posterior thalamus, and right middle temporal gyrus/hippocampus during failed inhibition, which was associated with increased stop-signal reaction time. In the behavioural go/no-go task, both ADHD groups, with and without ASD, had significantly lower motor inhibition performance compared to TD controls. In conclusion, only young adult males with ASD + ADHD had neurofunctional atypicality in brain regions associated with performance monitoring, while inhibition difficulties on go/no-go task performance was shared with ADHD. The suggests that young people with ASD + ADHD are most severely impaired during motor inhibition tasks compared to ASD and ADHD but do not reflect a combination of the difficulties associated with the pure disorders.
first_indexed 2024-04-09T16:20:28Z
format Article
id doaj.art-77e6e0034bca425a8bc75d54bab2f970
institution Directory Open Access Journal
issn 2158-3188
language English
last_indexed 2024-04-09T16:20:28Z
publishDate 2023-04-01
publisher Nature Publishing Group
record_format Article
series Translational Psychiatry
spelling doaj.art-77e6e0034bca425a8bc75d54bab2f9702023-04-23T11:29:05ZengNature Publishing GroupTranslational Psychiatry2158-31882023-04-011311910.1038/s41398-023-02431-4Reduced inferior fronto-insular-thalamic activation during failed inhibition in young adults with combined ASD and ADHD compared to typically developing and pure disorder groupsSteve Lukito0Owen G. O’Daly1David J. Lythgoe2John Hodsoll3Stefanos Maltezos4Mark Pitts5Emily Simonoff6Katya Rubia7Department of Child and Adolescent Psychiatry, King’s College London, Institute of Psychiatry, Psychology and NeuroscienceDepartment of Neuroimaging, King’s College London, Institute of Psychiatry, Psychology and NeuroscienceDepartment of Neuroimaging, King’s College London, Institute of Psychiatry, Psychology and NeuroscienceDepartment of Biostatistics and Health Informatics, King’s College London, Institute of Psychiatry, Psychology and NeuroscienceThe Adult Attention-Deficit/Hyperactivity Disorder (ADHD) and Autism National Service, Behavioural and Developmental Psychiatry Clinical Academic Group, South London and Maudsley Foundation NHS TrustThe Adult Attention-Deficit/Hyperactivity Disorder (ADHD) and Autism National Service, Behavioural and Developmental Psychiatry Clinical Academic Group, South London and Maudsley Foundation NHS TrustDepartment of Child and Adolescent Psychiatry, King’s College London, Institute of Psychiatry, Psychology and NeuroscienceDepartment of Child and Adolescent Psychiatry, King’s College London, Institute of Psychiatry, Psychology and NeuroscienceAbstract Autism spectrum disorder (ASD) often co-occurs with attention-deficit/hyperactivity disorder (ADHD) and people with these conditions have frontostriatal functional atypicality during motor inhibition. We compared the neural and neurocognitive correlates of motor inhibition and performance monitoring in young adult males with “pure” and combined presentations with age-and sex-matched typically developing controls, to explore shared or disorder-specific atypicality. Males aged 20–27 years with typical development (TD; n = 22), ASD (n = 21), combined diagnoses ASD + ADHD (n = 23), and ADHD (n = 25) were compared using a modified tracking fMRI stop-signal task that measures motor inhibition and performance monitoring while controlling for selective attention. In addition, they performed a behavioural go/no-go task outside the scanner. While groups did not differ behaviourally during successful stop trials, the ASD + ADHD group relative to other groups had underactivation in typical performance monitoring regions of bilateral anterior insula/inferior frontal gyrus, right posterior thalamus, and right middle temporal gyrus/hippocampus during failed inhibition, which was associated with increased stop-signal reaction time. In the behavioural go/no-go task, both ADHD groups, with and without ASD, had significantly lower motor inhibition performance compared to TD controls. In conclusion, only young adult males with ASD + ADHD had neurofunctional atypicality in brain regions associated with performance monitoring, while inhibition difficulties on go/no-go task performance was shared with ADHD. The suggests that young people with ASD + ADHD are most severely impaired during motor inhibition tasks compared to ASD and ADHD but do not reflect a combination of the difficulties associated with the pure disorders.https://doi.org/10.1038/s41398-023-02431-4
spellingShingle Steve Lukito
Owen G. O’Daly
David J. Lythgoe
John Hodsoll
Stefanos Maltezos
Mark Pitts
Emily Simonoff
Katya Rubia
Reduced inferior fronto-insular-thalamic activation during failed inhibition in young adults with combined ASD and ADHD compared to typically developing and pure disorder groups
Translational Psychiatry
title Reduced inferior fronto-insular-thalamic activation during failed inhibition in young adults with combined ASD and ADHD compared to typically developing and pure disorder groups
title_full Reduced inferior fronto-insular-thalamic activation during failed inhibition in young adults with combined ASD and ADHD compared to typically developing and pure disorder groups
title_fullStr Reduced inferior fronto-insular-thalamic activation during failed inhibition in young adults with combined ASD and ADHD compared to typically developing and pure disorder groups
title_full_unstemmed Reduced inferior fronto-insular-thalamic activation during failed inhibition in young adults with combined ASD and ADHD compared to typically developing and pure disorder groups
title_short Reduced inferior fronto-insular-thalamic activation during failed inhibition in young adults with combined ASD and ADHD compared to typically developing and pure disorder groups
title_sort reduced inferior fronto insular thalamic activation during failed inhibition in young adults with combined asd and adhd compared to typically developing and pure disorder groups
url https://doi.org/10.1038/s41398-023-02431-4
work_keys_str_mv AT stevelukito reducedinferiorfrontoinsularthalamicactivationduringfailedinhibitioninyoungadultswithcombinedasdandadhdcomparedtotypicallydevelopingandpuredisordergroups
AT owengodaly reducedinferiorfrontoinsularthalamicactivationduringfailedinhibitioninyoungadultswithcombinedasdandadhdcomparedtotypicallydevelopingandpuredisordergroups
AT davidjlythgoe reducedinferiorfrontoinsularthalamicactivationduringfailedinhibitioninyoungadultswithcombinedasdandadhdcomparedtotypicallydevelopingandpuredisordergroups
AT johnhodsoll reducedinferiorfrontoinsularthalamicactivationduringfailedinhibitioninyoungadultswithcombinedasdandadhdcomparedtotypicallydevelopingandpuredisordergroups
AT stefanosmaltezos reducedinferiorfrontoinsularthalamicactivationduringfailedinhibitioninyoungadultswithcombinedasdandadhdcomparedtotypicallydevelopingandpuredisordergroups
AT markpitts reducedinferiorfrontoinsularthalamicactivationduringfailedinhibitioninyoungadultswithcombinedasdandadhdcomparedtotypicallydevelopingandpuredisordergroups
AT emilysimonoff reducedinferiorfrontoinsularthalamicactivationduringfailedinhibitioninyoungadultswithcombinedasdandadhdcomparedtotypicallydevelopingandpuredisordergroups
AT katyarubia reducedinferiorfrontoinsularthalamicactivationduringfailedinhibitioninyoungadultswithcombinedasdandadhdcomparedtotypicallydevelopingandpuredisordergroups