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Neuroimaging Association Scores: reliability and validity of aggregate measures of brain structural features linked to mental disorders in youth

European Child & Adolescent Psychiatry volume 30, pages 1895–1906 (2021)Cite this article

Abstract

In genetics, aggregation of many loci with small effect sizes into a single score improved prediction. Nevertheless, studies applying easily replicable weighted scores to neuroimaging data are lacking. Our aim was to assess the reliability and validity of the Neuroimaging Association Score (NAS), which combines information from structural brain features previously linked to mental disorders. Participants were 726 youth (aged 6–14) from two cities in Brazil who underwent MRI and psychopathology assessment at baseline and 387 at 3-year follow-up. Results were replicated in two samples: IMAGEN (n = 1627) and the Healthy Brain Network (n = 843). NAS were derived by summing the product of each standardized brain feature by the effect size of the association of that brain feature with seven psychiatric disorders documented by previous meta-analyses. NAS were calculated for surface area, cortical thickness and subcortical volumes using T1-weighted scans. NAS reliability, temporal stability and psychopathology and cognition prediction were analyzed. NAS for surface area showed high internal consistency and 3-year stability and predicted general psychopathology and cognition with higher replicability than specific symptomatic domains for all samples. They also predicted general psychopathology with higher replicability than single structures alone, accounting for 1–3% of the variance, but without directionality. The NAS for cortical thickness and subcortical volumes showed lower internal consistency and less replicable associations with behavioural phenotypes. These findings indicate the NAS based on surface area might be replicable markers of general psychopathology, but these links are unlikely to be causal or clinically useful yet.

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Acknowledgements

We thank the children and families from the Brazilian High-Risk Study for their participation, which made this research possible.

Funding

This work was funded through research grants by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil; grant number 573974/2008–0), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil), the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Brazil; grant number 2008/57896–8) and the Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS, Brazil). All of them are public institutions of the Brazilian government developed for scientific research support. It was also funded by the National Institute of Mental Health (grant number 1-R01-MH-120482–01). Funding sources have no involvement in this study, including no role in data collection, analysis, and interpretation of the data. IMAGEN consortium is composed of Tobias Banaschewski, M.D., Ph.D.; Gareth J. Barker, Ph.D.; Arun L.W. Bokde, Ph.D.; Erin Burke Quinlan, PhD; Sylvane Desrivières, Ph.D.; Herta Flor, Ph.D.; Antoine Grigis, Ph.D.; Hugh Garavan, Ph.D.; Penny Gowland, Ph.D.; Andreas Heinz, M.D., Ph.D.; Bernd Ittermann, Ph.D.; Jean-Luc Martinot, M.D., Ph.D., Marie-Laure Paillère Martinot, M.D., Ph.D., Eric Artiges, M.D., Ph.D.; Frauke Nees, Ph.D.; Dimitri Papadopoulos Orfanos, Ph.D., Herve Lemaitre, Ph.D; Tomáš Paus, M.D., Ph.D.; Luise Poustka, M.D., Sarah Hohmann, M.D, Sabina Millenet, PhD; Juliane H. Fröhner, MSc; Michael N. Smolka, M.D; Henrik Walter, M.D., Ph.D.; Robert Whelan, Ph.D. and Gunter Schumann, M.D. IMAGEN work received support from the following sources: the European Union-funded FP6 Integrated Project IMAGEN (Reinforcement-related behaviour in normal brain function and psychopathology) (LSHM-CT- 2007–037286), the Horizon 2020 funded ERC Advanced Grant ‘STRATIFY’ (Brain network based stratification of reinforcement-related disorders) (695313), ERANID (Understanding the Interplay between Cultural, Biological and Subjective Factors in Drug Use Pathways) (PR-ST-0416-10004), BRIDGET (JPND: Brain Imaging, cognition Dementia and next generation Genomics) (MR/N027558/1), Human Brain Project (HBP SGA 2, 785907), the FP7 project MATRICS (603016), the Medical Research Council Grant ‘c-VEDA’ (Consortium on Vulnerability to Externalizing Disorders and Addictions) (MR/N000390/1), the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London, the Bundesministeriumfür Bildung und Forschung (BMBF grants 01GS08152; 01EV0711; Forschungsnetz AERIAL 01EE1406A, 01EE1406B), the Deutsche Forschungsgemeinschaft (DFG grants SM 80/7-2, SFB 940, TRR 265, NE 1383/14-1), the Medical Research Foundation and Medical Research Council (grants MR/R00465X/1 and MR/S020306/1), the National Institutes of Health (NIH) funded ENIGMA (grants 5U54EB020403-05 and 1R56AG058854-01). Further support was provided by grants from: the ANR (ANR-12-SAMA-0004, AAPG2019—GeBra), the Eranet Neuron (AF12-NEUR0008-01—WM2NA; and ANR-18-NEUR00002-01—ADORe), the Fondation de France (00081242), the Fondation pour la Recherche Médicale (DPA20140629802), the Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives (MILDECA), the Assistance-Publique-Hôpitaux-de-Paris and INSERM (interface grant), Paris Sud University IDEX 2012, the Fondation de l’Avenir (Grant AP-RM-17-013), the Fédération pour la Recherche sur le Cerveau; the National Institutes of Health, Science Foundation Ireland (16/ERCD/3797), U.S.A. (Axon, Testosterone and Mental Health during Adolescence; RO1 MH085772-01A1), and by NIH Consortium grant U54 EB020403, supported by a cross-NIH alliance that funds Big Data to Knowledge Centres of Excellence. Further support was provided by grants from: –the ANR (ANR-12-SAMA-0004, AAPG2019—GeBra), the Eranet Neuron (AF12-NEUR0008-01—WM2NA; and ANR-18-NEUR00002-01—ADORe), the Fondation de France (00,081,242), the Fondation pour la Recherche Médicale (DPA20140629802), the Mission Interministérielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives (MILDECA), the Assistance-Publique-Hôpitaux-de-Paris and INSERM (interface grant), Paris Sud University IDEX 2012, the Fondation de l’Avenir (grant AP-RM-17–013), the Fédération pour la Recherche sur le Cerveau. The Healthy Brain Network (https://www.healthybrainnetwork.org) work was supported by philanthropic contributions from the following individuals, foundations, and organizations: Lee Alexander, Robert Allard, Lisa Bilotti Foundation, Inc., Margaret Billoti, Christopher Boles, Brooklyn Nets, Agapi and Bruce Burkhard, Randolph Cowen and Phyllis Green, Elizabeth and David DePaolo, Charlotte Ford, Valesca Guerrand-Hermes, Sarah and Geoffrey Gund, George Hall, Joseph Healey and Elaine Thomas, Hearst Foundations, Eve and Ross Joffe, Anton and Robin Katz, Rachael and Marshall Levine, Ke Li, Jessica Lupovici, Javier Macaya, Christine and Richard Mack, Susan Miller and Byron Grote, John and Amy Phelan, Linnea and George Roberts, Jim and Linda Robinson Foundation, Inc, Caren and Barry Roseman, Zibby Schwarzman, David Shapiro and Abby Pogrebin, Stavros Niarchos Foundation, Nicholas Van Dusen, David Wolkoff and Stephanie Winston Wolkoff, and the Donors to the Brant Art Auction of 2012. MPM is a Randolph Cowen and Phyllis Green Scholar.

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Authors and Affiliations

  1. Section On Negative Affect and Social Processes, Departamento de Psiquiatria e Medicina Legal, Hospital de Clínicas de Porto Alegre, Universidade Federal Do Rio Grande Do Sul, Ramiro Barcelos, 2350, Room 2202, Porto Alegre, 90035-003, Brazil

    Luiza Kvitko Axelrud, André Rafael Simioni, Felipe Picon, Luis Augusto Rohde & Giovanni Abrahão Salum

  2. National Institute of Developmental Psychiatry (INPD, CNPq), São Paulo, Brazil

    Luiza Kvitko Axelrud, André Rafael Simioni, Pedro Mario Pan, André Zugman, Felipe Picon, Andrea Jackowski, Marcelo Queiroz Hoexter, Luis Augusto Rohde & Giovanni Abrahão Salum

  3. National Institute of Mental Health Intramural Research Program, Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA

    Daniel Samuel Pine & Anderson Marcelo Winkler

  4. Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UK

    Gareth Barker & Edward Dylan Barker

  5. Departamento de Psiquiatria, Universidade Federal de São Paulo, São Paulo, Brazil

    Pedro Mario Pan, André Zugman, Andrea Jackowski & Marcelo Queiroz Hoexter

  6. Centro de Matemática, Computação E Cognição, Universidade Federal Do ABC, Santo André, Brazil

    João Ricardo Sato

  7. Departments of Psychology and Psychiatry, University of Toronto, Toronto, ON, Canada

    Nadine Parker

  8. Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, USA

    Theodore Satterthwaite

  9. Institut National de La Santé Et de La Recherche Médicale, INSERM Unit 1000 “Neuroimaging and Psychiatry”, University Paris Saclay, University Paris Descartes, Paris, France

    Jean-Luc Martinot & Marie Laure Paillère Martinot

  10. Child Mind Institute, New York, NY, USA

    Michael Milham

Authors
  1. Luiza Kvitko Axelrud
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  2. André Rafael Simioni
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  3. Daniel Samuel Pine
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  4. Anderson Marcelo Winkler
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  5. Pedro Mario Pan
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  6. João Ricardo Sato
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  7. André Zugman
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  8. Nadine Parker
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  9. Felipe Picon
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  11. Marcelo Queiroz Hoexter
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  12. Gareth Barker
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  14. Marie Laure Paillère Martinot
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  15. Theodore Satterthwaite
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  16. Luis Augusto Rohde
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  17. Michael Milham
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  18. Edward Dylan Barker
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  19. Giovanni Abrahão Salum
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Consortia

IMAGEN Consortium

  • Tobias Banaschewski
  • , Gareth J. Barker
  • , Arun L. W. Bokde
  • , Erin Burke Quinlan
  • , Sylvane Desrivières
  • , Herta Flor
  • , Antoine Grigis
  • , Hugh Garavan
  • , Penny Gowland
  • , Andreas Heinz
  • , Bernd Ittermann
  • , Jean-Luc Martinot
  • , Marie-Laure Paillère Martinot
  • , Eric Artiges
  • , Frauke Nees
  • , Dimitri Papadopoulos Orfanos
  • , Herve Lemaitre
  • , Tomáš Paus
  • , Luise Poustka
  • , Sarah Hohmann
  • , Sabina Millenet
  • , Juliane H. Fröhner
  • , Michael N. Smolka
  • , Henrik Walter
  • , Robert Whelan
  •  & Gunter Schumann

Corresponding author

Correspondence to Luiza Kvitko Axelrud.

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Conflict of interest

Ms. Axelrud, Dr. Simioni, Dr. Pine, Dr. Winkler, Dr. Barker, Dr. Sato, Dr. Zugman, Dr. Parker, Dr. Picon, Dr. Jackowski, Dr. Hoexter, Dr Satterthwaite, Dr. Barker, Dr. JL Martinot, Dr. MLP Martinot, Dr Milham and Dr. Salum report no biomedical financial interests or potential conflicts of interest. Dr. Pan has received payment for the development of educational material for Janssen-Cilag and Astra-Zeneca. Dr. Rohde has received Honoraria, has been on the speakers' bureau/advisory board and/or has acted as a consultant for Eli-Lilly, Janssen-Cilag, Novartis and Shire in the last 2 years. He receives authorship royalties from Oxford Press and ArtMed. He also received travel awards for taking part of 2014 APA and 2015 WFADHD meetings from Shire. The ADHD and Juvenile Bipolar Disorder Outpatient Programs chaired by him received unrestricted educational and research support from the following pharmaceutical companies in the last three years: Eli-Lilly, Janssen-Cilag, Novartis, and Shire. Regarding the IMAGEN Consortium, Dr. Banaschewski served in an advisory or consultancy role for Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Shire. He received conference support or speaker’s fee by Lilly, Medice, Novartis and Shire. He has been involved in clinical trials conducted by Shire & Viforpharma. He received royalties from Hogrefe, Kohlhammer, CIP Medien, Oxford University Press. The other authors report no biomedical financial interests or potential conflicts of interest.

Ethical approval

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008. The Ethics Committee of the University of São Paulo approved the study. Parents of the participants and participants provided written or verbal consent.

Additional information

The members of the IMAGEN Consortium group are mentioned in "Acknowledgements" section.

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Axelrud, L.K., Simioni, A.R., Pine, D.S. et al. Neuroimaging Association Scores: reliability and validity of aggregate measures of brain structural features linked to mental disorders in youth. Eur Child Adolesc Psychiatry 30, 1895–1906 (2021). https://doi.org/10.1007/s00787-020-01653-x

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  • DOI: https://doi.org/10.1007/s00787-020-01653-x

Keywords

  • Brain structure
  • Cortical surface area
  • Cortical thickness
  • Psychopathology
  • Cognition
  • Replicability