Reduced fronto-striatal volume in attention-deficit/hyperactivity disorder in two cohorts across the lifespan

Renata Basso Cupertino; Sourena Soheili-Nezhad; Eugenio Horacio Grevet; Cibele Edom Bandeira; Felipe Almeida Picon; Maria Eduarda de Araujo Tavares; Jilly Naaijen; Daan van Rooij; Sophie Akkermans; Eduardo Schneider Vitola; Marcel P. Zwiers; Diego Luiz Rovaris; Pieter J. Hoekstra; Vitor Breda; Jaap Oosterlaan; Catharina A. Hartman; Christian F. Beckmann; Jan K. Buitelaar; Barbara Franke; Claiton Henrique Dotto Bau; Emma Sprooten

doi:10.1016/j.nicl.2020.102403

Reduced fronto-striatal volume in attention-deficit/hyperactivity disorder in two cohorts across the lifespan

Renata Basso Cupertino
, Sourena Soheili-Nezhad
, Eugenio Horacio Grevet
, Cibele Edom Bandeira
, Felipe Almeida Picon
, Maria Eduarda de Araujo Tavares
, Jilly Naaijen
, Daan van Rooij
, Sophie Akkermans
, Eduardo Schneider Vitola
, Marcel P. Zwiers
, Diego Luiz Rovaris
, Pieter J. Hoekstra
, Vitor Breda
, Jaap Oosterlaan
, Catharina A. Hartman
, Christian F. Beckmann
, Jan K. Buitelaar
, Barbara Franke
, Claiton Henrique Dotto Bau^*

Emma Sprooten

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Attention-Deficit/Hyperactivity Disorder (ADHD) has been associated with altered brain anatomy in neuroimaging studies. However, small and heterogeneous study samples, and the use of region-of-interest and tissue-specific analyses have limited the consistency and replicability of these effects. We used a data-driven multivariate approach to investigate neuroanatomical features associated with ADHD in two independent cohorts: the Dutch NeuroIMAGE cohort (n = 890, 17.2 years) and the Brazilian IMpACT cohort (n = 180, 44.2 years). Using independent component analysis of whole-brain morphometry images, 375 neuroanatomical components were assessed for association with ADHD. In both discovery (corrected-p = 0.0085) and replication (p = 0.032) cohorts, ADHD was associated with reduced volume in frontal lobes, striatum, and their interconnecting white-matter. Current results provide further evidence for the role of the fronto-striatal circuit in ADHD in children, and for the first time show its relevance to ADHD in adults. The fact that the cohorts are from different continents and comprise different age ranges highlights the robustness of the findings.

Original language	English
Article number	102403
Pages (from-to)	1-9
Number of pages	9
Journal	NeuroImage: Clinical
Volume	28
Early online date	28 Aug 2020
DOIs	https://doi.org/10.1016/j.nicl.2020.102403
Publication status	Published - 2020

Funding

The NeuroIMAGE study was supported by NIH Grant R01MH62873 (to Stephen V. Faraone), NWO Large Investment Grant 1750102007010 (to Jan Buitelaar), ZonMW grant 60-60600-97-193, NWO grants 056-13-015 and 433-09-242, and matching grants from Radboud University Nijmegen Medical Center, University Medical Center Groningen and Accare, and Vrije Universiteit Amsterdam. The research leading to these results also received support from the European Community's Seventh Framework Programme (FP7/2007-2013) under grant agreement number 278948 (TACTICS). Brazilian IMpACT was financed by Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grants 476529/2012-3, 466722/2014-1 and 424041/2016-2), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 and FIPE-HCPA 160600. Barbara Franke was supported by a personal Vici grant from the Innovation Program of the Netherlands Organization for Scientific Research (NWO; grant 016-130-669). Renata B Cupertino was supported by International Brain Research Organization-Latin America (IBRO LARC) Exchange Fellowship. Emma Sprooten is funded by a Hypatia Fellowship (Radboudumc) and a NARSAD Young Investigator Grant (Brain and Behavior Research Foundation, ID: 25034). This study is part of the International Multicentre persistent ADHD Collaboration (IMpACT; www.impactadhdgenomics.com). IMpACT unites major research centres working on the genetics of ADHD persistence across the lifespan and has participants in The Netherlands, Germany, Spain, Norway, the United Kingdom, the United States, Brazil and Sweden. Principal investigators of IMpACT are: Barbara Franke (chair), Andreas Reif (co-chair), Stephen V. Faraone, Jan Haavik, Bru Cormand, J. Antoni Ramos-Quiroga, Marta Ribases, Philip Asherson, Klaus-Peter Lesch, Jonna Kuntsi, Claiton H.D. Bau, Jan K. Buitelaar, Alejandro Arias Vasquez,Tetyana Zayats, Henrik Larsson, Alysa Doyle, and Eugenio H. Grevet. Eugenio Grevet was on the speaker's bureau for Novartis and Shire for the last 3 years. He also received travel awards (air tickets and hotel accommodations) for participating in two psychiatric meetings from Shire and Novartis. Barbara Franke has received educational speaking fees from Medice. Jan K Buitelaar has served as a consultant to/member of advisory board of/and/or speaker for Shire, Roche, Medice, and Servier. He is not an employee of any of these companies, and not a stock shareholder of any of these companies. He has no other financial or material support, including expert testimony, patents, royalties. All other authors declare that they have no conflict of interest. The NeuroIMAGE study was supported by NIH Grant R01MH62873 (to Stephen V. Faraone), NWO Large Investment Grant 1750102007010 (to Jan Buitelaar), ZonMW grant 60-60600-97-193 , NWO grants 056-13-015 and 433-09-242 , and matching grants from Radboud University Nijmegen Medical Center , University Medical Center Groningen and Accare , and Vrije Universiteit Amsterdam . The research leading to these results also received support from the European Community’s Seventh Framework Programme ( FP7/2007-2013 ) under grant agreement number 278948 (TACTICS). Brazilian IMpACT was financed by Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grants 476529/2012-3 , 466722/2014-1 and 424041/2016-2 ), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 and FIPE - HCPA 160600 . Barbara Franke was supported by a personal Vici grant from the Innovation Program of the Netherlands Organization for Scientific Research ( NWO ; grant 016-130-669 ). Renata B Cupertino was supported by International Brain Research Organization -Latin America (IBRO LARC) Exchange Fellowship. Emma Sprooten is funded by a Hypatia Fellowship ( Radboudumc ) and a NARSAD Young Investigator Grant ( Brain and Behavior Research Foundation , ID: 25034).

Funders	Funder number
Young Investigator Grant
International Brain Research Organization-Latin America
Barbara Franke
Shire
European Commission
Radboud Universitair Medisch Centrum
Novartis
Seventh Framework Programme	278948
National Alliance for Research on Schizophrenia and Depression
Servier
International Brain Research Organization
Fundação Instituto de Pesquisas Econômicas	HCPA 160600
???publication-publication-funding-organisation-not-added???	016-130-669, 1750102007010, 433-09-242
Brain and Behavior Research Foundation	25034
National Institutes of Health	R01MH62873
Conselho Nacional de Desenvolvimento Científico e Tecnológico	476529/2012-3, 466722/2014-1, 424041/2016-2
ZonMw	60-60600-97-193, 056-13-015
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior	FIPE-HCPA 160600

Keywords

ADHD
Fronto-striatal
Independent component analysis
Tensor-based morphometry
White matter

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Cupertino, R. B., Soheili-Nezhad, S., Grevet, E. H., Bandeira, C. E., Picon, F. A., Tavares, M. E. D. A., Naaijen, J., van Rooij, D., Akkermans, S., Vitola, E. S., Zwiers, M. P., Rovaris, D. L., Hoekstra, P. J., Breda, V., Oosterlaan, J., Hartman, C. A., Beckmann, C. F., Buitelaar, J. K., Franke, B., ... Sprooten, E. (2020). Reduced fronto-striatal volume in attention-deficit/hyperactivity disorder in two cohorts across the lifespan. NeuroImage: Clinical, 28, 1-9. Article 102403. https://doi.org/10.1016/j.nicl.2020.102403

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title = "Reduced fronto-striatal volume in attention-deficit/hyperactivity disorder in two cohorts across the lifespan",

abstract = "Attention-Deficit/Hyperactivity Disorder (ADHD) has been associated with altered brain anatomy in neuroimaging studies. However, small and heterogeneous study samples, and the use of region-of-interest and tissue-specific analyses have limited the consistency and replicability of these effects. We used a data-driven multivariate approach to investigate neuroanatomical features associated with ADHD in two independent cohorts: the Dutch NeuroIMAGE cohort (n = 890, 17.2 years) and the Brazilian IMpACT cohort (n = 180, 44.2 years). Using independent component analysis of whole-brain morphometry images, 375 neuroanatomical components were assessed for association with ADHD. In both discovery (corrected-p = 0.0085) and replication (p = 0.032) cohorts, ADHD was associated with reduced volume in frontal lobes, striatum, and their interconnecting white-matter. Current results provide further evidence for the role of the fronto-striatal circuit in ADHD in children, and for the first time show its relevance to ADHD in adults. The fact that the cohorts are from different continents and comprise different age ranges highlights the robustness of the findings.",

keywords = "ADHD, Fronto-striatal, Independent component analysis, Tensor-based morphometry, White matter",

author = "Cupertino, \{Renata Basso\} and Sourena Soheili-Nezhad and Grevet, \{Eugenio Horacio\} and Bandeira, \{Cibele Edom\} and Picon, \{Felipe Almeida\} and Tavares, \{Maria Eduarda de Araujo\} and Jilly Naaijen and \{van Rooij\}, Daan and Sophie Akkermans and Vitola, \{Eduardo Schneider\} and Zwiers, \{Marcel P.\} and Rovaris, \{Diego Luiz\} and Hoekstra, \{Pieter J.\} and Vitor Breda and Jaap Oosterlaan and Hartman, \{Catharina A.\} and Beckmann, \{Christian F.\} and Buitelaar, \{Jan K.\} and Barbara Franke and Bau, \{Claiton Henrique Dotto\} and Emma Sprooten",

year = "2020",

doi = "10.1016/j.nicl.2020.102403",

language = "English",

volume = "28",

pages = "1--9",

journal = "NeuroImage: Clinical",

issn = "2213-1582",

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Cupertino, RB, Soheili-Nezhad, S, Grevet, EH, Bandeira, CE, Picon, FA, Tavares, MEDA, Naaijen, J, van Rooij, D, Akkermans, S, Vitola, ES, Zwiers, MP, Rovaris, DL, Hoekstra, PJ, Breda, V, Oosterlaan, J, Hartman, CA, Beckmann, CF, Buitelaar, JK, Franke, B, Bau, CHD & Sprooten, E 2020, 'Reduced fronto-striatal volume in attention-deficit/hyperactivity disorder in two cohorts across the lifespan', NeuroImage: Clinical, vol. 28, 102403, pp. 1-9. https://doi.org/10.1016/j.nicl.2020.102403

TY - JOUR

T1 - Reduced fronto-striatal volume in attention-deficit/hyperactivity disorder in two cohorts across the lifespan

AU - Cupertino, Renata Basso

AU - Soheili-Nezhad, Sourena

AU - Grevet, Eugenio Horacio

AU - Bandeira, Cibele Edom

AU - Picon, Felipe Almeida

AU - Tavares, Maria Eduarda de Araujo

AU - Naaijen, Jilly

AU - van Rooij, Daan

AU - Akkermans, Sophie

AU - Vitola, Eduardo Schneider

AU - Zwiers, Marcel P.

AU - Rovaris, Diego Luiz

AU - Hoekstra, Pieter J.

AU - Breda, Vitor

AU - Oosterlaan, Jaap

AU - Hartman, Catharina A.

AU - Beckmann, Christian F.

AU - Buitelaar, Jan K.

AU - Franke, Barbara

AU - Bau, Claiton Henrique Dotto

AU - Sprooten, Emma

PY - 2020

Y1 - 2020

N2 - Attention-Deficit/Hyperactivity Disorder (ADHD) has been associated with altered brain anatomy in neuroimaging studies. However, small and heterogeneous study samples, and the use of region-of-interest and tissue-specific analyses have limited the consistency and replicability of these effects. We used a data-driven multivariate approach to investigate neuroanatomical features associated with ADHD in two independent cohorts: the Dutch NeuroIMAGE cohort (n = 890, 17.2 years) and the Brazilian IMpACT cohort (n = 180, 44.2 years). Using independent component analysis of whole-brain morphometry images, 375 neuroanatomical components were assessed for association with ADHD. In both discovery (corrected-p = 0.0085) and replication (p = 0.032) cohorts, ADHD was associated with reduced volume in frontal lobes, striatum, and their interconnecting white-matter. Current results provide further evidence for the role of the fronto-striatal circuit in ADHD in children, and for the first time show its relevance to ADHD in adults. The fact that the cohorts are from different continents and comprise different age ranges highlights the robustness of the findings.

AB - Attention-Deficit/Hyperactivity Disorder (ADHD) has been associated with altered brain anatomy in neuroimaging studies. However, small and heterogeneous study samples, and the use of region-of-interest and tissue-specific analyses have limited the consistency and replicability of these effects. We used a data-driven multivariate approach to investigate neuroanatomical features associated with ADHD in two independent cohorts: the Dutch NeuroIMAGE cohort (n = 890, 17.2 years) and the Brazilian IMpACT cohort (n = 180, 44.2 years). Using independent component analysis of whole-brain morphometry images, 375 neuroanatomical components were assessed for association with ADHD. In both discovery (corrected-p = 0.0085) and replication (p = 0.032) cohorts, ADHD was associated with reduced volume in frontal lobes, striatum, and their interconnecting white-matter. Current results provide further evidence for the role of the fronto-striatal circuit in ADHD in children, and for the first time show its relevance to ADHD in adults. The fact that the cohorts are from different continents and comprise different age ranges highlights the robustness of the findings.

KW - ADHD

KW - Fronto-striatal

KW - Independent component analysis

KW - Tensor-based morphometry

KW - White matter

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U2 - 10.1016/j.nicl.2020.102403

DO - 10.1016/j.nicl.2020.102403

M3 - Article

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AN - SCOPUS:85090884924

SN - 2213-1582

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SP - 1

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JO - NeuroImage: Clinical

JF - NeuroImage: Clinical

M1 - 102403

ER -

Reduced fronto-striatal volume in attention-deficit/hyperactivity disorder in two cohorts across the lifespan

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