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Coupled changes between ruminating thoughts and resting-state brain networks during the transition into adulthood

Molecular Psychiatry (2024)Cite this article

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Abstract

Perseverative negative thoughts, known as rumination, might arise from emotional challenges and preclude mental health when transitioning into adulthood. Due to its multifaceted nature, rumination can take several ruminative response styles, that diverge in manifestations, severity, and mental health outcomes. Still, prospective ruminative phenotypes remain elusive insofar. Longitudinal study designs are ideal for stratifying ruminative response styles, especially with resting-state functional MRI whose setup naturally elicits people’s ruminative traits. Here, we considered self-rated questionnaires on rumination and psychopathology, along with resting-state functional MRI data in 595 individuals assessed at age 18 and 22 from the IMAGEN cohort. We conducted independent component analysis to characterize eight single static resting-state functional networks in each subject and session and furthermore conducted a dynamic analysis, tackling the time variations of functional networks during the entire scanning time. We then investigated their longitudinal mediation role between changes in three ruminative response styles (reflective pondering, brooding, and depressive rumination) and changes in internalizing and co-morbid externalizing symptoms. Four static and two dynamic networks longitudinally differentiated these ruminative styles and showed complemental sensitivity to internalizing and co-morbid externalizing symptoms. Among these networks, the right frontoparietal network covaried with all ruminative styles but did not play any mediation role towards psychopathology. The default mode, the salience, and the limbic networks prospectively stratified these ruminative styles, suggesting that maladaptive ruminative styles are associated with altered corticolimbic function. For static measures, only the salience network played a longitudinal causal role between brooding rumination and internalizing symptoms. Dynamic measures highlighted the default-mode mediation role between the other ruminative styles and co-morbid externalizing symptoms. In conclusion, we identified the ruminative styles’ psychometric and neural outcome specificities, supporting their translation into applied research on young adult mental healthcare.

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Fig. 1: Main longitudinal mediation findings.
Fig. 2: Ruminative response styles related to the functional imbalance between rostral and orbital prefrontal cortexes: insights from static and dynamic FC networks.

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Data availability

Raw neuroimaging and psychometric data are publicly available on the IMAGEN website (https://imagen-project.org). Analytic codes and fully processed data are available upon request to the corresponding author.

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Acknowledgements

The IMAGEN consortium’s members Tobias Banaschewski, Arun LW Bokde, Sylvane Desrivières, Herta Flor, Hugh Garavan, Rüdiger Brühl, Penny Gowland, Andreas Heinz, Frauke Nees, Luise Poustka, Michael Smolka, Henrik Walter, Robert Whelan, Tomáš Paus, Gunter Schumann, Jean-Luc Martinot and Eric Artiges are acknowledged for their support as authors. A full list of the IMAGEN collaborators and their affiliations appears in the Supplemental Materials 8. Pr. Gilles Berstchy is acknowledged for his support. Pr. Stephane Lehericy and the radiographer staff at Center de NeuroImagerie de Recherche de l’Institut du Cerveau are acknowledged for their support in MRI datasets acquisition.

Funding

This work received support from the following sources: the European Union–funded FP6 Integrated Project IMAGEN (Grant No. LSHM- CT-2007-037286), the Horizon 2020 funded ERC Advanced Grant ‘STRATIFY’ (Brain network based stratification of reinforcement-related disorders) (695313); the Eranet Neuron (Grant No. ANR-18-NEUR00002-01– ADORe), Agence Nationale de la Recherche (Grant ANR-12-SAMA-0004 - GeBra), Assistance Publique-Hôpitaux de Paris and INSERM (interface grant), Paris Descartes University (Grant collaborative-project-2010), Paris Sud University (Grant No. IDEX-2012), Fondation de l’Avenir (Grant AP-RM-17-013), Fondation de France (Grant 00081242), Fédération pour la Recherche sur le Cerveau, and Fondation pour la Recherche Médicale (Grant DPA20140629802), The Ile-de-France region grant to the project VEAVE (How to reduce Violence against Children and Adolescents in the Ile-de-France region and its “whole life” consequences; action 16700103, Convention APHP INSERM n° 23002745–23002747); the National Institute for Health Research (NIHR) Biomedical Research Center at South London and Maudsley NHS Foundation Trust and King’s College London, the Bundesministerium für 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 and MR/S020306/1). The INSERM, Strasbourg University, and SATT CONECTUS provided sponsorship (PI: Jean-Luc Martinot).

Author information

Author notes

  1. These authors contributed equally: Jean-Luc Martinot, Eric Artiges.

Authors and Affiliations

  1. Ecole Normale Supérieure Paris-Saclay, University Paris-Saclay, University Paris-City, INSERM U1299 “Developmental Trajectories & Psychiatry, Centre Borelli CNRS UMR9010, Gif-sur-Yvette, France

    Rocco Marchitelli, Marie-Laure Paillère Martinot, Alain Trouvé, Jean-Luc Martinot & Eric Artiges

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

    Marie-Laure Paillère Martinot

  3. Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, and German Center for Mental Health (DZPG) partner site Mannheim-Heidelberg-Ulm, Heidelberg University, Mannheim, Germany

    Tobias Banaschewski, Frauke Nees, Sarah Hohmann & Nathalie Holz

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

    Arun L. W. Bokde

  5. Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, UK

    Sylvane Desrivières

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

    Herta Flor & Frauke Nees

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

    Herta Flor

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

    Hugh Garavan

  9. Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, UK

    Penny Gowland

  10. 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

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

    Rüdiger Brühl

  12. Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, Germany

    Frauke Nees

  13. NeuroSpin, CEA, Université Paris-Saclay, F-91191, Gif-sur-Yvette, France

    Dimitri Papadopoulos Orfanos

  14. Department of Psychiatry and Neuroscience, Faculty of Medicine, CHU Sainte-Justine Research Center, Population Neuroscience Laboratory, University of Montreal, Montreal, QC, Canada

    Tomáš Paus

  15. Department of Child and Adolescent Psychiatry, Center for Psychosocial Medicine, University Hospital Heidelberg, Heidelberg, Germany

    Luise Poustka

  16. Centre for Population Neuroscience and Stratified Medicine (PONS), Department of Psychiatry and Neuroscience, Charité Universitätsmedizin Berlin, Berlin, Germany

    Nilakshi Vaidya

  17. Department of Psychiatry and Psychotherapy, Medical Faculty, Technische Universität Dresden, Dresden, Germany

    Juliane H. Fröhner & Michael N. Smolka

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

    Robert Whelan

  19. Centre for Population Neuroscience and Stratified Medicine (PONS), ISTBI Fudan University, Shanghai, China

    Gunter Schumann

  20. Department of Psychiatry and Neuroscience, Charité University Medicine, Berlin, Germany

    Gunter Schumann

  21. Department of Psychiatry, Lab-D-PSY, EPS Barthélémy Durand, Etampes, France

    Jean-Luc Martinot & Eric Artiges

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Consortia

the IMAGEN consortium

  • Marie-Laure Paillère Martinot
  • , Jean-Luc Martinot
  • , Eric Artiges
  • , Tobias Banaschewski
  • , Sarah Hohmann
  • , Nathalie Holz
  • , Arun L. W. Bokde
  • , Sylvane Desrivières
  • , Herta Flor
  • , Hugh Garavan
  • , Penny Gowland
  • , Andreas Heinz
  • , Henrik Walter
  • , Rüdiger Brühl
  • , Frauke Nees
  • , Dimitri Papadopoulos Orfanos
  • , Tomáš Paus
  • , Luise Poustka
  • , Nilakshi Vaidya
  • , Juliane H. Fröhner
  • , Michael N. Smolka
  • , Robert Whelan
  •  & Gunter Schumann

Contributions

The IMAGEN consortium’s authors provided substantial contributions to the conception, design, and acquisition of data for the current work. All authors approved the finalized article, ensuring its content’s accuracy and integrity as suitable for publication purposes. Rocco Marchitelli was involved in the auditing of sample data. He was in charge of the preprocessing of all neuroimaging data and conducted all statistical analyses. Alain Trouvé developed the software for dynamic FC analysis. Rocco Marchitelli, Marie-Laure Paillere Martinot, Jean-Luc Martinot, and Eric Artiges interpreted the work’s findings and critically revised it with respect to its intellectual content. Rocco Marchitelli, Jean-Luc Martinot, and Eric Artiges wrote and revised the article.

Corresponding author

Correspondence to Jean-Luc Martinot.

Ethics declarations

Competing interests

TB served in an advisory or consultancy role for ADHS Digital, Infectopharm, Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Roche, and Takeda. He received conference support or speaker’s fee by Medice and Takeda. He has been involved in clinical trials conducted by Shire & Viforpharma. He received royalties from Hogrefe, Kohlhammer, CIP Medien, and Oxford University Press. He has been involved in clinical trials conducted by Shire & Viforpharma. GB has received honoraria from General Electric Healthcare for teaching on scanner programming courses. LP 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 commercial relationships or conflicts of interest.

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Marchitelli, R., Paillère Martinot, ML., Trouvé, A. et al. Coupled changes between ruminating thoughts and resting-state brain networks during the transition into adulthood. Mol Psychiatry (2024). https://doi.org/10.1038/s41380-024-02610-9

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  • DOI: https://doi.org/10.1038/s41380-024-02610-9

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