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

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

doi:10.1038/s41380-024-02610-9

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

Mol Psychiatry. 2024 Jul 2. doi: 10.1038/s41380-024-02610-9. Online ahead of print.

Authors

Rocco Marchitelli¹, Marie-Laure Paillère Martinot^{1

2}, Alain Trouvé¹, Tobias Banaschewski³, Arun L W Bokde⁴, Sylvane Desrivières⁵, Herta Flor^{6

7}, Hugh Garavan⁸, Penny Gowland⁹, Andreas Heinz¹⁰, Rüdiger Brühl¹¹, Frauke Nees^{3

6

12}, Dimitri Papadopoulos Orfanos¹³, Tomáš Paus¹⁴, Luise Poustka¹⁵, Sarah Hohmann³, Nathalie Holz³, Nilakshi Vaidya¹⁶, Juliane H Fröhner¹⁷, Michael N Smolka¹⁷, Henrik Walter¹⁰, Robert Whelan¹⁸, Gunter Schumann^{19

20}, Jean-Luc Martinot^#^{21

22}, Eric Artiges^#^{1

23}; IMAGEN consortium

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.
² AP-HP Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France.
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.
⁴ Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
⁵ Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
⁶ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany.
⁷ Department of Psychology, School of Social Sciences, University of Mannheim, 68131, Mannheim, Germany.
⁸ Departments of Psychiatry and Psychology, University of Vermont, Burlington, VT, 05405, USA.
⁹ Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, UK.
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.
¹¹ Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Berlin, Germany.
¹² Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, Germany.
¹³ NeuroSpin, CEA, Université Paris-Saclay, F-91191, Gif-sur-Yvette, France.
¹⁴ Department of Psychiatry and Neuroscience, Faculty of Medicine, CHU Sainte-Justine Research Center, Population Neuroscience Laboratory, University of Montreal, Montreal, QC, Canada.
¹⁵ Department of Child and Adolescent Psychiatry, Center for Psychosocial Medicine, University Hospital Heidelberg, Heidelberg, Germany.
¹⁶ Centre for Population Neuroscience and Stratified Medicine (PONS), Department of Psychiatry and Neuroscience, Charité Universitätsmedizin Berlin, Berlin, Germany.
¹⁷ Department of Psychiatry and Psychotherapy, Medical Faculty, Technische Universität Dresden, Dresden, Germany.
¹⁸ School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland.
¹⁹ Centre for Population Neuroscience and Stratified Medicine (PONS), ISTBI Fudan University, Shanghai, China.
²⁰ Department of Psychiatry and Neuroscience, Charité University Medicine, Berlin, Germany.
²¹ Ecole Normale Supérieure Paris-Saclay, University Paris-Saclay, University Paris-City, INSERM U1299 "Developmental Trajectories & Psychiatry, Centre Borelli CNRS UMR9010, Gif-sur-Yvette, France. jean-luc.martinot@inserm.fr.
²² Department of Psychiatry, Lab-D-PSY, EPS Barthélémy Durand, Etampes, France. jean-luc.martinot@inserm.fr.
²³ Department of Psychiatry, Lab-D-PSY, EPS Barthélémy Durand, Etampes, France.

^# Contributed equally.

PMID: 38956372
DOI: 10.1038/s41380-024-02610-9

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.