Comparative meta-analyses of brain structural and functional abnormalities during cognitive control in attention-deficit/hyperactivity disorder and autism spectrum disorder

Lukito, Steve; Norman, Luke; Carlisi, Christina; Radua, Joaquim; Hart, Heledd; Simonoff, Emily; Rubia, Katya

doi:10.1017/s0033291720000574

Cited by 248Attention Deficit Hyperactivity DisorderAutism Spectrum Disorder ResearchNeural and Behavioral Psychology Studies

Comparative meta-analyses of brain structural and functional abnormalities during cognitive control in attention-deficit/hyperactivity disorder and autism spectrum disorder

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Lukito, Steve, Norman, Luke, Carlisi, Christina, Radua, Joaquim, Hart, Heledd, Simonoff, Emily, Rubia, Katya·2020·Psychological Medicine

DOI 10.1017/s0033291720000574PMC PMC7212063

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Abstract

Background: People with attention-deficit/hyperactivity disorder (ADHD) and autism spectrum disorder (ASD) have abnormalities in frontal, temporal, parietal and striato-thalamic networks. It is unclear to what extent these abnormalities are distinctive or shared. This comparative meta-analysis aimed to identify the most consistent disorder-differentiating and shared structural and functional abnormalities. Methods: Systematic literature search was conducted for whole-brain voxel-based morphometry (VBM) and functional magnetic resonance imaging (fMRI) studies of cognitive control comparing people with ASD or ADHD with typically developing controls. Regional gray matter volume (GMV) and fMRI abnormalities during cognitive control were compared in the overall sample and in age-, sex- and IQ-matched subgroups with seed-based d mapping meta-analytic methods. Results: Eighty-six independent VBM (1533 ADHD and 1295 controls; 1445 ASD and 1477 controls) and 60 fMRI datasets (1001 ADHD and 1004 controls; 335 ASD and 353 controls) were identified. The VBM meta-analyses revealed ADHD-differentiating decreased ventromedial orbitofrontal ( z = 2.22, p < 0.0001) but ASD-differentiating increased bilateral temporal and right dorsolateral prefrontal GMV ( z s ⩾ 1.64, p s ⩽ 0.002). The fMRI meta-analyses of cognitive control revealed ASD-differentiating medial prefrontal underactivation but overactivation in bilateral ventrolateral prefrontal cortices and precuneus ( z s ⩾ 1.04, p s ⩽ 0.003). During motor response inhibition specifically, ADHD relative to ASD showed right inferior fronto-striatal underactivation ( z s ⩾ 1.14, p s ⩽ 0.003) but shared right anterior insula underactivation. Conclusions: People with ADHD and ASD have mostly distinct structural abnormalities, with enlarged fronto-temporal GMV in ASD and reduced orbitofrontal GMV in ADHD; and mostly distinct functional abnormalities, which were more pronounced in ASD.

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Structural grey matter reductions in basal ganglia and insula in ADHD are disorder-specific relative to OCD, while medial frontal reductions are specific to ASD.
“Comparative meta-analyses show that structural grey matter volume reductions in basal ganglia and insula are disorder-specific relative to OCD in 30 data sets with 1,870 participants (Norman et al., 2016) while medial frontal reductions were specific to ASD in 66 data sets with 3,610 participants (Lukito et al., 2020).”
From The World Federation of ADHD International Consensus Statement: 208 Evidence-based conclusions about the disorder (2021) · cites this paper as Lukito et al., 2020
The Results (Disorder-Differentiating and Shared Brain Structure Abnormalities; page unavailable) report medial frontal grey-matter reduction in ASD relative to controls, but identify medial prefrontal reduction as ADHD-differentiating relative to ASD, particularly in pediatric participants. They therefore do not support calling the structural reduction ASD-specific. The sample-characteristics Results also report 86 structural datasets, not 66. (LLM, conf=0.87)
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Functional under-activations in right inferior frontal cortex and basal ganglia during cognitive control are disorder-specific relative to OCD, and inferior frontal dysfunction is specific relative to autism.
“The functional under-activations in right inferior frontal cortex and basal ganglia during tasks of cognitive control were disorder-specific relative to OCD in 1,870 participants (Norman et al., 2016), while the inferior frontal dysfunction was specific relative to autism in 3,610 participants (Lukito et al., 2020).”
From The World Federation of ADHD International Consensus Statement: 208 Evidence-based conclusions about the disorder (2021) · cites this paper as Lukito et al., 2020
The Results (Disorder-Differentiating and Shared Brain Abnormalities during Cognitive Control) report ADHD-differentiating right inferior frontal underactivation relative to ASD specifically during motor response inhibition. But the Results (Search Results and Sample Characteristics) list 2,693 participants across the cognitive-control fMRI datasets, not 3,610. The OCD comparison belongs to the separately cited Norman et al. (2016), rather than the part attributed to Lukito et al. (LLM, conf=0.88)
Experimental — accuracy not yet measured
ADHD is associated with under-activation in right inferior frontal cortex, supplementary motor area, and basal ganglia during inhibitory control, replicated in further meta-analyses.
“A meta-analysis of 21 functional MRI studies with 607 participants found that those with ADHD showed consistent and replicable under-activation in typical regions of inhibitory control such as right inferior frontal cortex, supplementary motor area and the basal ganglia relative to typically developing individuals (Hart et al., 2013). The inferior frontal under-activation findings were replicated”
From The World Federation of ADHD International Consensus Statement: 208 Evidence-based conclusions about the disorder (2021) · cites this paper as Lukito et al., 2020
The Introduction reports prior meta-analyses finding ADHD-related underactivation in right inferior frontal gyrus, supplementary motor area and striatum during cognitive control. This paper’s Results replicate right inferior frontal and caudate underactivation during motor response inhibition, but report supplementary motor area underactivation only for the broader cognitive-control analysis, not inhibition specifically. The 21-study sample cited in the printed sentence is attributed to Hart et al. (2013), not to this paper. (LLM, conf=0.86)
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ADHD medications are not associated with brain structure deficits but with improved brain function in inferior frontal and striatal regions.
“Meta-analyses and systematic reviews showed that the medications used to treat ADHD are not associated with observed deficits in brain structure (Hoogman et al., 2017; Hoogman et al., 2019; Lukito et al., 2020; Norman et al., 2016; Spencer et al., 2013), but with improved brain function, most prominently in inferior frontal and striatal regions (Hart et al., 2013; Lukito et al., 2020; Norman et al”
From The World Federation of ADHD International Consensus Statement: 208 Evidence-based conclusions about the disorder (2021) · cites this paper as Lukito et al., 2020
The Results (ADHD VBM and ADHD fMRI; page unavailable) associate current or lifetime psychostimulant exposure with increased orbitofrontal gray-matter volume and lifetime exposure with greater left inferior frontal activation. They do not report medication-associated improvement in striatal function. The findings concern psychostimulant exposure, rather than all ADHD medications, and are associations rather than demonstrated treatment effects. (LLM, conf=0.85)
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Previous large scale studies and meta-analyses of neuroimaging, neurophysiological and neuropsychological impairments have highlighted areas of overlap, particularly between ADHD and ASD.
“Similarly, previous large scale studies and meta-analyses of neuroimaging, neurophysiological and neuropsychological impairments have highlighted areas of overlap, particularly between ADHD and ASD 53-56 .”
From Candidate diagnostic biomarkers for neurodevelopmental disorders in children and adolescents: a systematic review (2023) · cites this paper as [54]
The Introduction describes partially overlapping brain abnormalities and cognitive-control deficits in ADHD and ASD. The Results identify a shared functional abnormality during motor response inhibition, although the Conclusions emphasize that brain abnormalities are mostly distinct. This paper supports overlap in neuroimaging findings and cognitive control, but does not establish overlap in neurophysiological impairments. (LLM, conf=0.84)
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“The region is also implicated in functions such as sensory, emotion and social-processing domains typically impaired in ASD (Kana, Patriquin, Black, Channell, & Wicker, 2016; Martinez-Sanchis, 2014; South & Rodgers, 2017).”
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Authors: Lukito, S., Norman, L., Carlisi, C., Radua, J., Hart, H., Simonoff, E., & Rubia, K.
Affiliations: King's College London (GB)
National Institutes of Health (US)
Corresponding author: Lukito, Steve
ORCID: Lukito, Steve
Norman, Luke
Carlisi, Christina
Hart, Heledd
Simonoff, Emily
Rubia, Katya
Venue: Psychological Medicine
Publisher: Cambridge University Press (CUP)
Published: 2020-03-27
Volume: 50
Issue: 6
Pages: 894-919
ISSN: 0033-2917 (ISSN-L)
1469-8978
DOI: 10.1017/s0033291720000574
PMC: PMC7212063
OpenAlex: W2998651304
Semantic Scholar: 149256fab88748ba0bc73fec857807db9020efac
Cited by: 248
References: 246
Citations by year: 2026: 27 · 2025: 43 · 2024: 47 · 2023: 50 · 2022: 38 · 2021: 36 · 2020: 6 · 2019: 1
FWCI: 23.71
Type: journal article
Language: en
Open access: green
kclpure.kcl.ac.uk
Licence: other-oa
www.cambridge.org/core/terms (unspecified)
Locations: Psychological Medicine (publishedVersion)
PubMed (publishedVersion)
Research Portal (King's College London) (submittedVersion, other-oa)
UCL Discovery (University College London) (submittedVersion)
Funders: Wellcome Trust (206459/Z/17/Z, Z/17/Z, 206459)
Maudsley Charity
National Institute for Health and Care Research (NF-SI-0514-10073, IS-BRC-1215, BRC-1215-20018, RP-PG-1211-20016, IS-BRC-1215–20018)
King's College London (IS-BRC-1215-20018, 115300)
European Commission (115300, CPII19/00009)
Fondation pour la Recherche Médicale
Institute of Psychiatry, Psychology and Neuroscience, King’s College London
Medical Research Council (MR/P012647/1, 115300, MR/P019293/1, MR/R000832/1)
Economic and Social Research Council (ESRC 003041/1, 003041/1)
Instituto de Salud Carlos III ((CPII19/00009), PI19/00394)
European Regional Development Fund (CPII19/00009)
European Social Fund (CPII19/00009)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Attention Deficit Hyperactivity Disorder
Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: attention deficit hyperactivity disorder, autism spectrum disorder, cognitive control, structural brain abnormalities, functional brain abnormalities, gray matter volume, dorsolateral prefrontal cortex, medial prefrontal cortex, ventrolateral prefrontal cortex, precuneus, anterior insula, response inhibition, seed-based d mapping
MeSH terms: Autism Spectrum Disorder, Adolescent, Adult, Attention Deficit Disorder with Hyperactivity, Brain, Cerebral Cortex, Child, Cognition, Female, Humans, Magnetic Resonance Imaging, Male, Parietal Lobe, Thalamus, Young Adult, Gray Matter

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Comparative meta-analyses of brain structural and functional abnormalities during cognitive control in attention-deficit/hyperactivity disorder and autism spectrum disorder

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