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Published Online: 30 April 2024

Shared and Specific Neural Correlates of Attention Deficit Hyperactivity Disorder and Autism Spectrum Disorder: A Meta-Analysis of 243 Task-Based Functional MRI Studies

Hiroki Tamon, M.D., Junya Fujino, M.D., Ph.D., Takashi Itahashi, Ph.D., Lennart Frahm, M.S., Valeria Parlatini, M.D., Ph.D., Yuta Y. Aoki, M.D., Ph.D. [email protected], Francisco Xavier Castellanos, M.D., Simon B. Eickhoff, M.D., and Samuele Cortese, M.D., Ph.D.Authors Info & Affiliations
Publication: American Journal of Psychiatry
Volume 181, Number 6
https://doi.org/10.1176/appi.ajp.20230270
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Abstract

Objective:

To investigate shared and specific neural correlates of cognitive functions in attention deficit hyperactivity disorder (ADHD) and autism spectrum disorder (ASD), the authors performed a comprehensive meta-analysis and considered a balanced set of neuropsychological tasks across the two disorders.

Methods:

A broad set of electronic databases was searched up to December 4, 2022, for task-based functional MRI studies investigating differences between individuals with ADHD or ASD and typically developing control subjects. Spatial coordinates of brain loci differing significantly between case and control subjects were extracted. To avoid potential diagnosis-driven selection bias of cognitive tasks, the tasks were grouped according to the Research Domain Criteria framework, and stratified sampling was used to match cognitive component profiles. Activation likelihood estimation was used for the meta-analysis.

Results:

After screening 20,756 potentially relevant references, a meta-analysis of 243 studies was performed, which included 3,084 participants with ADHD (676 females), 2,654 participants with ASD (292 females), and 6,795 control subjects (1,909 females). ASD and ADHD showed shared greater activations in the lingual and rectal gyri and shared lower activations in regions including the middle frontal gyrus, the parahippocampal gyrus, and the insula. By contrast, there were ASD-specific greater and lower activations in regions including the left middle temporal gyrus and the left middle frontal gyrus, respectively, and ADHD-specific greater and lower activations in the amygdala and the global pallidus, respectively.

Conclusions:

Although ASD and ADHD showed both shared and disorder-specific standardized neural activations, disorder-specific activations were more prominent than shared ones. Functional brain differences between ADHD and ASD are more likely to reflect diagnosis-related pathophysiology than bias from the selection of specific neuropsychological tasks.

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Information & Authors

Information

Published In

Go to American Journal of Psychiatry
Go to American Journal of Psychiatry
American Journal of Psychiatry
Volume 181 • Number 6 • June 01, 2024
Pages: 541 - 552
PubMed: 38685858

History

Received: 5 April 2023
Revision received: 14 September 2023
Revision received: 25 October 2023
Accepted: 31 October 2023
Published online: 30 April 2024
Published in print: June 01, 2024

Keywords

  1. Activation Likelihood Estimation
  2. Attention Deficit Hyperactivity Disorder (ADHD)
  3. Autism Spectrum Disorder (ASD)
  4. Neurodevelopmental Disorders
  5. Neuropsychological Task
  6. Task-Based Functional Magnetic Resonance Imaging

Authors

Details

Hiroki Tamon, M.D.
Division of Infant and Toddler Mental Health, Department of Psychosocial Medicine, National Center for Child Health and Development, Tokyo (Tamon); Graduate School of Medicine and Department of Functional Brain Imaging, Institute of Development, Aging, and Cancer, Tohoku University, Miyagi, Japan (Tamon); Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo (Fujino); Division of the Humanities and Social Sciences, California Institute of Technology, Pasadena (Fujino); Medical Institute of Developmental Disabilities Research, Showa University, Tokyo (Itahashi, Aoki); Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Center Jülich, Jülich, Germany (Frahm, Eickhoff); Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany (Eickhoff); Department of Child and Adolescent Psychiatry, King’s College London (Parlatini); Aoki Clinic, Tokyo (Aoki); Department of Child and Adolescent Psychiatry, New York University (NYU) Grossman School of Medicine, New York, and Nathan Kline Institute for Psychiatric Research, Orangeburg, N.Y. (Castellanos); Centre for Innovation in Mental Health, School of Psychology, Faculty of Environmental and Life Sciences, and Clinical and Experimental Sciences (CNS and Psychiatry), Faculty of Medicine, University of Southampton, Southampton, U.K. (Cortese); Solent National Health System Trust, Southampton, U.K. (Cortese); Hassenfeld Children’s Hospital at NYU Langone, NYU Child Study Center, New York (Cortese); Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, Nottingham, U.K. (Cortese); Department of Precision and Regenerative Medicine-Jonic Area, University of Bari Aldo Moro, Bari, Italy (Cortese).
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Junya Fujino, M.D., Ph.D.
Division of Infant and Toddler Mental Health, Department of Psychosocial Medicine, National Center for Child Health and Development, Tokyo (Tamon); Graduate School of Medicine and Department of Functional Brain Imaging, Institute of Development, Aging, and Cancer, Tohoku University, Miyagi, Japan (Tamon); Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo (Fujino); Division of the Humanities and Social Sciences, California Institute of Technology, Pasadena (Fujino); Medical Institute of Developmental Disabilities Research, Showa University, Tokyo (Itahashi, Aoki); Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Center Jülich, Jülich, Germany (Frahm, Eickhoff); Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany (Eickhoff); Department of Child and Adolescent Psychiatry, King’s College London (Parlatini); Aoki Clinic, Tokyo (Aoki); Department of Child and Adolescent Psychiatry, New York University (NYU) Grossman School of Medicine, New York, and Nathan Kline Institute for Psychiatric Research, Orangeburg, N.Y. (Castellanos); Centre for Innovation in Mental Health, School of Psychology, Faculty of Environmental and Life Sciences, and Clinical and Experimental Sciences (CNS and Psychiatry), Faculty of Medicine, University of Southampton, Southampton, U.K. (Cortese); Solent National Health System Trust, Southampton, U.K. (Cortese); Hassenfeld Children’s Hospital at NYU Langone, NYU Child Study Center, New York (Cortese); Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, Nottingham, U.K. (Cortese); Department of Precision and Regenerative Medicine-Jonic Area, University of Bari Aldo Moro, Bari, Italy (Cortese).
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Takashi Itahashi, Ph.D.
Division of Infant and Toddler Mental Health, Department of Psychosocial Medicine, National Center for Child Health and Development, Tokyo (Tamon); Graduate School of Medicine and Department of Functional Brain Imaging, Institute of Development, Aging, and Cancer, Tohoku University, Miyagi, Japan (Tamon); Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo (Fujino); Division of the Humanities and Social Sciences, California Institute of Technology, Pasadena (Fujino); Medical Institute of Developmental Disabilities Research, Showa University, Tokyo (Itahashi, Aoki); Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Center Jülich, Jülich, Germany (Frahm, Eickhoff); Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany (Eickhoff); Department of Child and Adolescent Psychiatry, King’s College London (Parlatini); Aoki Clinic, Tokyo (Aoki); Department of Child and Adolescent Psychiatry, New York University (NYU) Grossman School of Medicine, New York, and Nathan Kline Institute for Psychiatric Research, Orangeburg, N.Y. (Castellanos); Centre for Innovation in Mental Health, School of Psychology, Faculty of Environmental and Life Sciences, and Clinical and Experimental Sciences (CNS and Psychiatry), Faculty of Medicine, University of Southampton, Southampton, U.K. (Cortese); Solent National Health System Trust, Southampton, U.K. (Cortese); Hassenfeld Children’s Hospital at NYU Langone, NYU Child Study Center, New York (Cortese); Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, Nottingham, U.K. (Cortese); Department of Precision and Regenerative Medicine-Jonic Area, University of Bari Aldo Moro, Bari, Italy (Cortese).
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Lennart Frahm, M.S.
Division of Infant and Toddler Mental Health, Department of Psychosocial Medicine, National Center for Child Health and Development, Tokyo (Tamon); Graduate School of Medicine and Department of Functional Brain Imaging, Institute of Development, Aging, and Cancer, Tohoku University, Miyagi, Japan (Tamon); Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo (Fujino); Division of the Humanities and Social Sciences, California Institute of Technology, Pasadena (Fujino); Medical Institute of Developmental Disabilities Research, Showa University, Tokyo (Itahashi, Aoki); Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Center Jülich, Jülich, Germany (Frahm, Eickhoff); Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany (Eickhoff); Department of Child and Adolescent Psychiatry, King’s College London (Parlatini); Aoki Clinic, Tokyo (Aoki); Department of Child and Adolescent Psychiatry, New York University (NYU) Grossman School of Medicine, New York, and Nathan Kline Institute for Psychiatric Research, Orangeburg, N.Y. (Castellanos); Centre for Innovation in Mental Health, School of Psychology, Faculty of Environmental and Life Sciences, and Clinical and Experimental Sciences (CNS and Psychiatry), Faculty of Medicine, University of Southampton, Southampton, U.K. (Cortese); Solent National Health System Trust, Southampton, U.K. (Cortese); Hassenfeld Children’s Hospital at NYU Langone, NYU Child Study Center, New York (Cortese); Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, Nottingham, U.K. (Cortese); Department of Precision and Regenerative Medicine-Jonic Area, University of Bari Aldo Moro, Bari, Italy (Cortese).
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Valeria Parlatini, M.D., Ph.D.
Division of Infant and Toddler Mental Health, Department of Psychosocial Medicine, National Center for Child Health and Development, Tokyo (Tamon); Graduate School of Medicine and Department of Functional Brain Imaging, Institute of Development, Aging, and Cancer, Tohoku University, Miyagi, Japan (Tamon); Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo (Fujino); Division of the Humanities and Social Sciences, California Institute of Technology, Pasadena (Fujino); Medical Institute of Developmental Disabilities Research, Showa University, Tokyo (Itahashi, Aoki); Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Center Jülich, Jülich, Germany (Frahm, Eickhoff); Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany (Eickhoff); Department of Child and Adolescent Psychiatry, King’s College London (Parlatini); Aoki Clinic, Tokyo (Aoki); Department of Child and Adolescent Psychiatry, New York University (NYU) Grossman School of Medicine, New York, and Nathan Kline Institute for Psychiatric Research, Orangeburg, N.Y. (Castellanos); Centre for Innovation in Mental Health, School of Psychology, Faculty of Environmental and Life Sciences, and Clinical and Experimental Sciences (CNS and Psychiatry), Faculty of Medicine, University of Southampton, Southampton, U.K. (Cortese); Solent National Health System Trust, Southampton, U.K. (Cortese); Hassenfeld Children’s Hospital at NYU Langone, NYU Child Study Center, New York (Cortese); Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, Nottingham, U.K. (Cortese); Department of Precision and Regenerative Medicine-Jonic Area, University of Bari Aldo Moro, Bari, Italy (Cortese).
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Yuta Y. Aoki, M.D., Ph.D. [email protected]
Division of Infant and Toddler Mental Health, Department of Psychosocial Medicine, National Center for Child Health and Development, Tokyo (Tamon); Graduate School of Medicine and Department of Functional Brain Imaging, Institute of Development, Aging, and Cancer, Tohoku University, Miyagi, Japan (Tamon); Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo (Fujino); Division of the Humanities and Social Sciences, California Institute of Technology, Pasadena (Fujino); Medical Institute of Developmental Disabilities Research, Showa University, Tokyo (Itahashi, Aoki); Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Center Jülich, Jülich, Germany (Frahm, Eickhoff); Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany (Eickhoff); Department of Child and Adolescent Psychiatry, King’s College London (Parlatini); Aoki Clinic, Tokyo (Aoki); Department of Child and Adolescent Psychiatry, New York University (NYU) Grossman School of Medicine, New York, and Nathan Kline Institute for Psychiatric Research, Orangeburg, N.Y. (Castellanos); Centre for Innovation in Mental Health, School of Psychology, Faculty of Environmental and Life Sciences, and Clinical and Experimental Sciences (CNS and Psychiatry), Faculty of Medicine, University of Southampton, Southampton, U.K. (Cortese); Solent National Health System Trust, Southampton, U.K. (Cortese); Hassenfeld Children’s Hospital at NYU Langone, NYU Child Study Center, New York (Cortese); Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, Nottingham, U.K. (Cortese); Department of Precision and Regenerative Medicine-Jonic Area, University of Bari Aldo Moro, Bari, Italy (Cortese).
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Francisco Xavier Castellanos, M.D.
Division of Infant and Toddler Mental Health, Department of Psychosocial Medicine, National Center for Child Health and Development, Tokyo (Tamon); Graduate School of Medicine and Department of Functional Brain Imaging, Institute of Development, Aging, and Cancer, Tohoku University, Miyagi, Japan (Tamon); Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo (Fujino); Division of the Humanities and Social Sciences, California Institute of Technology, Pasadena (Fujino); Medical Institute of Developmental Disabilities Research, Showa University, Tokyo (Itahashi, Aoki); Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Center Jülich, Jülich, Germany (Frahm, Eickhoff); Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany (Eickhoff); Department of Child and Adolescent Psychiatry, King’s College London (Parlatini); Aoki Clinic, Tokyo (Aoki); Department of Child and Adolescent Psychiatry, New York University (NYU) Grossman School of Medicine, New York, and Nathan Kline Institute for Psychiatric Research, Orangeburg, N.Y. (Castellanos); Centre for Innovation in Mental Health, School of Psychology, Faculty of Environmental and Life Sciences, and Clinical and Experimental Sciences (CNS and Psychiatry), Faculty of Medicine, University of Southampton, Southampton, U.K. (Cortese); Solent National Health System Trust, Southampton, U.K. (Cortese); Hassenfeld Children’s Hospital at NYU Langone, NYU Child Study Center, New York (Cortese); Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, Nottingham, U.K. (Cortese); Department of Precision and Regenerative Medicine-Jonic Area, University of Bari Aldo Moro, Bari, Italy (Cortese).
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Simon B. Eickhoff, M.D.
Division of Infant and Toddler Mental Health, Department of Psychosocial Medicine, National Center for Child Health and Development, Tokyo (Tamon); Graduate School of Medicine and Department of Functional Brain Imaging, Institute of Development, Aging, and Cancer, Tohoku University, Miyagi, Japan (Tamon); Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo (Fujino); Division of the Humanities and Social Sciences, California Institute of Technology, Pasadena (Fujino); Medical Institute of Developmental Disabilities Research, Showa University, Tokyo (Itahashi, Aoki); Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Center Jülich, Jülich, Germany (Frahm, Eickhoff); Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany (Eickhoff); Department of Child and Adolescent Psychiatry, King’s College London (Parlatini); Aoki Clinic, Tokyo (Aoki); Department of Child and Adolescent Psychiatry, New York University (NYU) Grossman School of Medicine, New York, and Nathan Kline Institute for Psychiatric Research, Orangeburg, N.Y. (Castellanos); Centre for Innovation in Mental Health, School of Psychology, Faculty of Environmental and Life Sciences, and Clinical and Experimental Sciences (CNS and Psychiatry), Faculty of Medicine, University of Southampton, Southampton, U.K. (Cortese); Solent National Health System Trust, Southampton, U.K. (Cortese); Hassenfeld Children’s Hospital at NYU Langone, NYU Child Study Center, New York (Cortese); Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, Nottingham, U.K. (Cortese); Department of Precision and Regenerative Medicine-Jonic Area, University of Bari Aldo Moro, Bari, Italy (Cortese).
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Samuele Cortese, M.D., Ph.D.
Division of Infant and Toddler Mental Health, Department of Psychosocial Medicine, National Center for Child Health and Development, Tokyo (Tamon); Graduate School of Medicine and Department of Functional Brain Imaging, Institute of Development, Aging, and Cancer, Tohoku University, Miyagi, Japan (Tamon); Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo (Fujino); Division of the Humanities and Social Sciences, California Institute of Technology, Pasadena (Fujino); Medical Institute of Developmental Disabilities Research, Showa University, Tokyo (Itahashi, Aoki); Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Center Jülich, Jülich, Germany (Frahm, Eickhoff); Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany (Eickhoff); Department of Child and Adolescent Psychiatry, King’s College London (Parlatini); Aoki Clinic, Tokyo (Aoki); Department of Child and Adolescent Psychiatry, New York University (NYU) Grossman School of Medicine, New York, and Nathan Kline Institute for Psychiatric Research, Orangeburg, N.Y. (Castellanos); Centre for Innovation in Mental Health, School of Psychology, Faculty of Environmental and Life Sciences, and Clinical and Experimental Sciences (CNS and Psychiatry), Faculty of Medicine, University of Southampton, Southampton, U.K. (Cortese); Solent National Health System Trust, Southampton, U.K. (Cortese); Hassenfeld Children’s Hospital at NYU Langone, NYU Child Study Center, New York (Cortese); Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, Nottingham, U.K. (Cortese); Department of Precision and Regenerative Medicine-Jonic Area, University of Bari Aldo Moro, Bari, Italy (Cortese).
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Notes

Send correspondence to Dr. Aoki ([email protected]).

Competing Interests

Dr. Cortese has received honoraria and reimbursement for educational lectures from the Association for Child and Adolescent Central Health, the British Association of Psychopharmacology, the Canadian ADHD Alliance Resource, and Medice. The other authors report no financial relationships with commercial interests.

Funding Information

This work was partly supported by the Japan Society for the Promotion of Science (grant 21K15719 to Dr. Aoki) and the Japan Agency for Medical Research and Development (grant JP18dm0307008). Dr. Eickhoff was supported by the European Union’s Horizon 2020 Research and Innovation Program (grants 945539 [HBP SGA3] and 826421 [VBC]), the Deutsche Forschungsgemeinschaft (DFG, SFB 1451; and IRTG 2150), and NIH (grant R01MH074457). Dr. Cortese was supported by a National Institute for Health and Care Research (NIHR) Research Professorship (grant NIHR303122), by NIHR grants NIHR203684, NIHR203035, NIHR130077, NIHR128472, and RP-PG-0618-20003, and by European Research Executive Agency grant 101095568-HORIZONHLTH-2022-DISEASE-07-03.

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