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Federated Analysis in COINSTAC Reveals Functional Network Connectivity and Spectral Links to Smoking and Alcohol Consumption in Nearly 2,000 Adolescent Brains

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Abstract

With the growth of decentralized/federated analysis approaches in neuroimaging, the opportunities to study brain disorders using data from multiple sites has grown multi-fold. One such initiative is the Neuromark, a fully automated spatially constrained independent component analysis (ICA) that is used to link brain network abnormalities among different datasets, studies, and disorders while leveraging subject-specific networks. In this study, we implement the neuromark pipeline in COINSTAC, an open-source neuroimaging framework for collaborative/decentralized analysis. Decentralized exploratory analysis of nearly 2000 resting-state functional magnetic resonance imaging datasets collected at different sites across two cohorts and co-located in different countries was performed to study the resting brain functional network connectivity changes in adolescents who smoke and consume alcohol. Results showed hypoconnectivity across the majority of networks including sensory, default mode, and subcortical domains, more for alcohol than smoking, and decreased low frequency power. These findings suggest that global reduced synchronization is associated with both tobacco and alcohol use. This proof-of-concept work demonstrates the utility and incentives associated with large-scale decentralized collaborations spanning multiple sites.

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Data Availability Statement

Data sharing is not applicable to this article as no new data were created or analyzed in this study.

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Acknowledgements

This work was funded by the National Institutes of Health (grants: R01DA040487, R01MH121246, R01DA049238, and 1R01DA040487) and the National Science Foundation (grant: 2112455). This work received support from the following sources: Consortium on Vulnerability to Externalizing Disorders and Addictions (cVEDA) is jointly funded by the Indian Council for Medical Research (ICMR/MRC/3/M/2015-NCD-I) and the Newton Grant from the Medical Research Council(MR/N000390/1), United Kingdom, 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), Human Brain Project (HBP SGA 2, 785907, and HBP SGA 3, 945539), the National Institute of Health (NIH) (R01DA049238, A decentralized macro and micro gene-by-environment interaction analysis of substance use behavior and its brain biomarkers), 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; Forschungsnetz IMAC-Mind 01GL1745B), 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 - MRF-058-0004-RG-DESRI and MR/S020306/1 - MRF-058-0009-RG-DESR-C0759), 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. ImagenPathways “Understanding the Interplay between Cultural, Biological and Subjective Factors in Drug Use Pathways” is a collaborative project supported by the European Research Area Network on Illicit Drugs (ERANID). This paper is based on independent research commissioned and funded in England by the National Institute for Health Research (NIHR) Policy Research Programme (project ref. PR-ST-0416-10001). The views expressed in this article are those of the authors and not necessarily those of the national funding agencies or ERANID. Author ZZ received a fellowship from the Medical Research Foundation (MRF-058-0014-F-ZHAN-C0866).

Author information

Author notes

  1. Vivek Benegal

    Present address: Centre for Addiction Medicine, NIMHANS, Bengaluru, India

  2. Harshvardhan Gazula and Kelly Rootes-Murdy contributed equally to this work.

Authors and Affiliations

  1. Martinos Center for Biomedical Imaging, MGH and Harvard Medical School, Boston, USA

    Harshvardhan Gazula

  2. Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State University, Georgia Institute of Technology, Emory University, Atlanta, GA, USA

    Kelly Rootes-Murdy, Sunitha Basodi, Eric Verner, Ross Kelly, Jessica A. Turner, Sergey M. Plis & Vince D. Calhoun

  3. Department of Psychiatry, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, India

    Bharath Holla, Pratima Murthy & Vivek Benegal

  4. Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King’s College London, London, SE5 8AF, United Kingdom

    Zuo Zhang, Sylvane Desrivieres & Gunter Schumann

  5. ICMR-Center on Non-communicable Diseases, Kolkata, India

    Amit Chakrabarti

  6. Department of Psychiatry, Postgraduate Institute of Medical Education & Research, Chandigarh, India

    Debasish Basu & Subodh Bhagyalakshmi Nanjayya

  7. Department of Psychiatry, Regional Institute of Medical Sciences, Imphal, Manipur, India

    Rajkumar Lenin Singh

  8. Department of Psychology, Regional Institute of Medical Sciences, Imphal, Manipur, India

    Roshan Lourembam Singh

  9. Rural Health Centre, Rishi Valley, Andhra Pradesh, India

    Kartik Kalyanram & Kamakshi Kartik

  10. Epidemiology Research Unit, CSI Holdsworth Memorial Hospital, Mysore, India

    Kumaran Kalyanaraman & Krishnaveni Ghattu

  11. Division of Nutrition, St John’s Research Institute, Bengaluru, India

    Rebecca Kuriyan

  12. Department of Psychiatry & Department of Medical Ethics, St. John’s Medical College & Hospital, Bangalore, India

    Sunita Simon Kurpad

  13. Department of Neuroimaging, Institute of Psychology, Psychiatry & Neuroscience, King’s College London, London, UK

    Gareth J Barker

  14. Department of Neuroimaging and Interventional Radiology, NIMHANS, Bengaluru, India

    Rose Dawn Bharath

  15. Molecular Genetics Laboratory, NIMHANS, Bengaluru, India

    Meera Purushottam

  16. NeuroSpin, CEA, Université Paris-Saclay, Paris, France

    Dimitri Papadopoulos Orfanos & Antoine Grigis

  17. Department of Child & Adolescent Psychiatry, NIMHANS, Bengaluru, India

    Eesha Sharma

  18. Bristol Medical School, University of Bristol, Bristol, UK

    Matthew Hickman

  19. MRC Centre for Environment and Health, School of Public Health, Imperial College London, London, UK

    Mireille Toledano

  20. Centre for Addiction Medicine, NIMHANS, Bengaluru, India

    Nilakshi Vaidya

  21. Centre for Population Neuroscience and Precision Medicine (PONS), Department of Psychiatry and Psychotherapy, Charité Universitätsmedizin Berlin, Berlin, Germany

    Nilakshi Vaidya, Frauke Nees & Gunter Schumann

  22. Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, 68159, Germany

    Tobias Banaschewski & Frauke Nees

  23. Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland

    Arun L. W. Bokde

  24. Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany

    Herta Flor & Frauke Nees

  25. Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, 68131, Germany

    Herta Flor

  26. Departments of Psychiatry and Psychology, University of Vermont, Burlington, Vermont, 05405, USA

    Hugh Garavan

  27. Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom

    Penny Gowland

  28. Department of Psychiatry and Psychotherapy CCM, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany

    Andreas Heinz, Henrik Walter & Jeanne Winterer

  29. Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Berlin, Germany

    Rüdiger Brühl

  30. Institut National de la Santé et de la Recherche Médicale, INSERM U A10 “Trajectoires développementales en psychiatrie”; Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli;, Gif-sur-Yvette, France

    Jean-Luc Martinot, Marie-Laure Paillére Martinot & Eric Artiges

  31. AP-HP. Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France

    Marie-Laure Paillére Martinot

  32. Psychiatry Department, EPS Barthélémy Durand, Etampes, France

    Eric Artiges

  33. Department of Psychiatry, Faculty of Medicine and Centre Hospitalier Universitaire Sainte-Justine, University of Montreal, Montreal, Quebec, Canada

    Tomás Paus

  34. Departments of Psychiatry and Psychology, University of Toronto, Toronto, Ontario, Canada

    Tomás Paus

  35. Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, Göttingen, 37075, Germany

    Luise Poustka

  36. Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany

    Juliane H. Fröhner & Michael N. Smolka

  37. Department of Psychological Medicine, Section for Eating Disorders, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, SE5 8AF, UK

    Lauren Robinson

  38. Department of Education and Psychology, Freie Universität Berlin, Berlin, Germany

    Jeanne Winterer

  39. School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland

    Robert Whelan

  40. Department of Psychology, Georgia State University, Atlanta, GA, USA

    Jessica A. Turner & Vince D. Calhoun

  41. Department of Electrical and Computer Engineering, Rutgers, The State University of New Jersey, Piscataway, NJ, USA

    Anand D. Sarwate

  42. Department of Computer Science, Georgia State University, Atlanta, GA, USA

    Sergey M. Plis

  43. Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, P.R. China

    Gunter Schumann

  44. Integrative Medicine, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, India

    Bharath Holla

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  1. Harshvardhan Gazula
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Consortia

IMAGEN Consortium

Contributions

HG led the manuscript writing with support from KR, BH and SB. BH contributed data and was instrumental in performing the analysis in COINSTAC. ZZ contributed data to the study as well as contributed to describing the data. EV and RK manage the COINSTAC project. SP, AD and JT are part of the COINSTAC team. VB and GS are the principal investigators of the CVEDA-IMAGEN consortium and have been instrumental in facilitating this multi-site study. VC is also a co-investigator and leads the COINSTAC team, formed the vision for this work, and helped interpret the results. All others who were not mentioned here are part of either the cVEDA or IMAGEN consortia.

Corresponding authors

Correspondence to Harshvardhan Gazula or Bharath Holla.

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Conflict of Interest

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 present work is unrelated to the above grants and relationships. Dr. Barker has received honoraria from General Electric Healthcare for teaching on scanner programming courses. Dr. Poustka served in an advisory or consultancy role for Roche and Viforpharm and received speaker’s fee by Shire. She received royalties from Hogrefe, Kohlhammer and Schattauer. The present work is unrelated to the above grants and relationships. The other authors report no biomedical financial interests or potential conflicts of interest.

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Gazula, H., Rootes-Murdy, K., Holla, B. et al. Federated Analysis in COINSTAC Reveals Functional Network Connectivity and Spectral Links to Smoking and Alcohol Consumption in Nearly 2,000 Adolescent Brains. Neuroinform 21, 287–301 (2023). https://doi.org/10.1007/s12021-022-09604-4

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