A shared neural basis underlying psychiatric comorbidity

Chao Xie; Shitong Xiang; Chun Shen; Xuerui Peng; Jujiao Kang; Yuzhu Li; Wei Cheng; Shiqi He; Marina Bobou; M John Broulidakis; Betteke Maria van Noort; Zuo Zhang; Lauren Robinson; Nilakshi Vaidya; Jeanne Winterer; Yuning Zhang; Sinead King; Tobias Banaschewski; Gareth J Barker; Arun L W Bokde; Uli Bromberg; Christian Büchel; Herta Flor; Antoine Grigis; Hugh Garavan; Penny Gowland; Andreas Heinz; Bernd Ittermann; Hervé Lemaître; Jean-Luc Martinot; Marie-Laure Paillère Martinot; Frauke Nees; Dimitri Papadopoulos Orfanos; Tomáš Paus; Luise Poustka; Juliane H Fröhner; Ulrike Schmidt; Julia Sinclair; Michael N Smolka; Argyris Stringaris; Henrik Walter; Robert Whelan; Sylvane Desrivières; Barbara J Sahakian; Trevor W Robbins; Gunter Schumann; Tianye Jia; Jianfeng Feng; IMAGEN Consortium; STRATIFY/ESTRA Consortium; ZIB Consortium

doi:10.1038/s41591-023-02317-4

A shared neural basis underlying psychiatric comorbidity

Nat Med. 2023 May;29(5):1232-1242. doi: 10.1038/s41591-023-02317-4. Epub 2023 Apr 24.

Authors

Chao Xie^{1

2}, Shitong Xiang^{1

2}, Chun Shen^{1

2}, Xuerui Peng³, Jujiao Kang^{1

2}, Yuzhu Li^{1

2}, Wei Cheng^{1

2}, Shiqi He^{1

4}, Marina Bobou⁵, M John Broulidakis⁶, Betteke Maria van Noort⁷, Zuo Zhang⁵, Lauren Robinson^{8

9}, Nilakshi Vaidya¹⁰, Jeanne Winterer^{10

11}, Yuning Zhang¹², Sinead King^{5

13}, Tobias Banaschewski¹⁴, Gareth J Barker¹⁵, Arun L W Bokde¹⁶, Uli Bromberg¹⁷, Christian Büchel¹⁷, Herta Flor^{18

19}, Antoine Grigis²⁰, Hugh Garavan²¹, Penny Gowland²², Andreas Heinz¹⁰, Bernd Ittermann²³, Hervé Lemaître²⁴, Jean-Luc Martinot²⁵, Marie-Laure Paillère Martinot^{25

26}, Frauke Nees^{14

18

27}, Dimitri Papadopoulos Orfanos²⁰, Tomáš Paus²⁸, Luise Poustka²⁹, Juliane H Fröhner³⁰, Ulrike Schmidt^{8

9}, Julia Sinclair⁶, Michael N Smolka³⁰, Argyris Stringaris³¹, Henrik Walter¹⁰, Robert Whelan³², Sylvane Desrivières⁵, Barbara J Sahakian^{1

33}, Trevor W Robbins^#^{1

34}, Gunter Schumann^#^{1

10

35

36}, Tianye Jia^#^{37

38

39}, Jianfeng Feng^#^{1

2

40

41

42}; IMAGEN Consortium; STRATIFY/ESTRA Consortium; ZIB Consortium

Collaborator

Betteke Maria van Noort

Affiliations

¹ Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China.
² Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, Shanghai, China.
³ Faculty of Psychology, Technische Universität Dresden, Dresden, Germany.
⁴ School of Health Sciences, The University of Manchester, Manchester, UK.
⁵ Social Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁶ Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, UK.
⁷ Department of Psychology, MSB Medical School Berlin, Berlin, Germany.
⁸ Department of Psychological Medicine, Section for Eating Disorders, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁹ South London and Maudsley NHS Foundation Trust, London, UK.
¹⁰ Department of Psychiatry and Neurosciences, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
¹¹ Department of Education and Psychology, Freie Universität Berlin, Berlin, Germany.
¹² Psychology Department, University of Southampton, Southampton, UK.
¹³ School of Medicine, Center for Neuroimaging, Cognition and Genomics, National University of Ireland (NUI) Galway, Galway, Ireland.
¹⁴ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹⁵ Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹⁶ Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
¹⁷ University Medical Centre Hamburg-Eppendorf, Hamburg, Germany.
¹⁸ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹⁹ Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, Germany.
²⁰ NeuroSpin, C.E.A., Université Paris-Saclay, Gif-sur-Yvette, France.
²¹ Departments of Psychiatry and Psychology, University of Vermont, Burlington, VT, USA.
²² Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, Nottingham, UK.
²³ Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Germany.
²⁴ Institut des Maladies Neurodégénératives, UMR 5293, CNRS, CEA, Université de Bordeaux, Bordeaux, France.
²⁵ Institut National de la Santé et de la Recherche Médicale, INSERM U1299 'Trajectoires développementales en psychiatrie', Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS UMR9010, Centre Borelli, Gif-sur-Yvette, France.
²⁶ AP-HP, Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France.
²⁷ Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig-Holstein, Kiel University, Kiel, Germany.
²⁸ Department of Psychiatry and Neuroscience and Centre Hospitalier Universitaire Sainte-Justine, University of Montreal, Quebec, Canada.
²⁹ Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, Göttingen, Germany.
³⁰ Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
³¹ Division of Psychiatry and Department of Clinical, Educational & Health Psychology, University College London, London, UK.
³² School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland.
³³ Department of Psychiatry and Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UK.
³⁴ Department of Psychology and Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UK.
³⁵ Department of Sports and Health Sciences, University of Potsdam, Potsdam, Germany.
³⁶ PONS Centre, Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, China.
³⁷ Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China. tianyejia@fudan.edu.cn.
³⁸ Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, Shanghai, China. tianyejia@fudan.edu.cn.
³⁹ Social Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK. tianyejia@fudan.edu.cn.
⁴⁰ School of Mathematical Sciences and Centre for Computational Systems Biology, Fudan University, Shanghai, China.
⁴¹ Department of Computer Science, University of Warwick, Coventry, UK.
⁴² Fudan ISTBI-ZJNU Algorithm Centre for Brain-inspired Intelligence, Zhejiang Normal University, Jinhua, China.

^# Contributed equally.

Abstract

Recent studies proposed a general psychopathology factor underlying common comorbidities among psychiatric disorders. However, its neurobiological mechanisms and generalizability remain elusive. In this study, we used a large longitudinal neuroimaging cohort from adolescence to young adulthood (IMAGEN) to define a neuropsychopathological (NP) factor across externalizing and internalizing symptoms using multitask connectomes. We demonstrate that this NP factor might represent a unified, genetically determined, delayed development of the prefrontal cortex that further leads to poor executive function. We also show this NP factor to be reproducible in multiple developmental periods, from preadolescence to early adulthood, and generalizable to the resting-state connectome and clinical samples (the ADHD-200 Sample and the Stratify Project). In conclusion, we identify a reproducible and general neural basis underlying symptoms of multiple mental health disorders, bridging multidimensional evidence from behavioral, neuroimaging and genetic substrates. These findings may help to develop new therapeutic interventions for psychiatric comorbidities.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Adolescent
Comorbidity
Humans
Mental Disorders* / diagnostic imaging
Mental Disorders* / epidemiology
Mental Disorders* / psychology
Neuroimaging
Psychopathology
Young Adult

Abstract

Publication types

MeSH terms

Grants and funding