Cortical profiles of numerous psychiatric disorders and normal development share a common pattern

Zhipeng Cao¹, Renata B Cupertino², Jonatan Ottino-Gonzalez², Alistair Murphy², Devarshi Pancholi², Anthony Juliano², Bader Chaarani², Matthew Albaugh², Dekang Yuan², Nathan Schwab², James Stafford³, Anna E Goudriaan⁴, Kent Hutchison⁵, Chiang-Shan R Li⁶, Maartje Luijten⁷, Martine Groefsema⁷, Reza Momenan⁸, Lianne Schmaal^{9

10}, Rajita Sinha⁶, Ruth J van Holst¹¹, Dick J Veltman¹¹, Reinout W Wiers¹², Bernice Porjesz¹³, Tristram Lett¹⁴, Tobias Banaschewski¹⁵, Arun L W Bokde¹⁶, Sylvane Desrivières¹⁷, Herta Flor^{18

19}, Antoine Grigis²⁰, Penny Gowland²¹, Andreas Heinz¹⁴, Rüdiger Brühl²², Jean-Luc Martinot²³, Marie-Laure Paillère Martinot^{23

24}, Eric Artiges^{23

25}, Frauke Nees^{15

18

26}, Dimitri Papadopoulos Orfanos²⁰, Tomáš Paus^{27

28}, Luise Poustka²⁹, Sarah Hohmann¹⁵, Sabina Millenet¹⁵, Juliane H Fröhner³⁰, Lauren Robinson³¹, Michael N Smolka³⁰, Henrik Walter¹⁴, Jeanne Winterer^{14

32}, Gunter Schumann^{17

33

34}, Robert Whelan³⁵, Ravi R Bhatt³⁶, Alyssa Zhu³⁶, Patricia Conrod³⁷, Neda Jahanshad³⁶, Paul M Thompson³⁶, Scott Mackey², Hugh Garavan²; IMAGEN Consortium; ENIGMA Addiction Working Group

Affiliations

¹ Department of Psychiatry, University of Vermont College of Medicine, Burlington, VT, 05401, USA. zhipeng30@foxmail.com.
² Department of Psychiatry, University of Vermont College of Medicine, Burlington, VT, 05401, USA.
³ Department of Neurological Sciences, University of Vermont College of Medicine, Burlington, VT, 05401, USA.
⁴ Department of Psychiatry, Amsterdam UMC, Location AMC, University of Amsterdam, Amsterdam Neuroscience and Amsterdam Institute for Addiction Research, Amsterdam, The Netherlands.
⁵ Department of Psychology and Neuroscience, University of Colorado Boulder, Boulder, CO, USA.
⁶ Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA.
⁷ Behavioural Science Institute, Radboud University, Nijmegen, The Netherlands.
⁸ Clinical NeuroImaging Research Core, Division of Intramural Clinical and Biological Research, National Institute on Alcohol Abuse and Alcoholism, Bethesda, MD, USA.
⁹ Orygen, Parkville, VIC, Australia.
¹⁰ Centre for Youth Mental Health, The University of Melbourne, Melbourne, VIC, Australia.
¹¹ Department of Psychiatry, Amsterdam UMC, Location AMC, University of Amsterdam, Amsterdam, The Netherlands.
¹² Addiction Development and Psychopathology (ADAPT)-lab, Department of Psychology and Center for Urban Mental Health, University of Amsterdam, Amsterdam, The Netherlands.
¹³ Department of Psychiatry, State University of New York Downstate Medical Center, Brooklyn, NY, 11203, USA.
¹⁴ Department of Psychiatry and Psychotherapy CCM, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 10117, Berlin, Germany.
¹⁵ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159, Mannheim, Germany.
¹⁶ Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin D2, Ireland.
¹⁷ Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology and Neuroscience, SGDP Centre, King's College London, London, SE5 8AF, UK.
¹⁸ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159, Mannheim, Germany.
¹⁹ Department of Psychology, School of Social Sciences, University of Mannheim, 68131, Mannheim, Germany.
²⁰ NeuroSpin, CEA, Université Paris-Saclay, F-91191, Gif-sur-Yvette, France.
²¹ Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, NG7 2RD, UK.
²² Physikalisch-Technische Bundesanstalt (PTB), D-10587, Braunschweig and Berlin, Germany.
²³ 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, 91191, Gif-sur-Yvette, France.
²⁴ AP-HP. Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, 75013, Paris, France.
²⁵ Psychiatry Department, EPS Barthélémy Durand, 91152, Etampes, France.
²⁶ Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, Germany.
²⁷ Departments of Psychiatry and Neuroscience and Centre Hospitalier Universitaire Sainte Justine, University of Montreal, Montreal, QC, H3T 1C5, Canada.
²⁸ Departments of Psychology and Psychiatry, University of Toronto, Toronto, ON, M6A 2E1, Canada.
²⁹ Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, 37075, Göttingen, Germany.
³⁰ Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, 01062, Dresden, Germany.
³¹ Department of Psychological Medicine, Section for Eating Disorders, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, SE5 8AF, UK.
³² Department of Education and Psychology, Freie Universität Berlin, 14195, Berlin, Germany.
³³ PONS Research Group, Department of Psychiatry and Psychotherapy, Campus Charite Mitte, Humboldt University, Berlin D-10099 and Leibniz Institute for Neurobiology, 39118, Magdeburg, Germany.
³⁴ Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, 200433, PR China.
³⁵ School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin D2, Ireland.
³⁶ Imaging Genetics Center, Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Marina del Rey, CA, 90292, USA.
³⁷ Department of Psychiatry, Université de Montreal, CHU Ste Justine Hospital, Montreal, QC, Canada.

PMID: 36380235
DOI: 10.1038/s41380-022-01855-6

Cortical profiles of numerous psychiatric disorders and normal development share a common pattern

Zhipeng Cao et al. Mol Psychiatry. 2023 Feb.

. 2023 Feb;28(2):698-709.

doi: 10.1038/s41380-022-01855-6. Epub 2022 Nov 15.

Authors

Affiliations

¹ Department of Psychiatry, University of Vermont College of Medicine, Burlington, VT, 05401, USA. zhipeng30@foxmail.com.
² Department of Psychiatry, University of Vermont College of Medicine, Burlington, VT, 05401, USA.
³ Department of Neurological Sciences, University of Vermont College of Medicine, Burlington, VT, 05401, USA.
⁴ Department of Psychiatry, Amsterdam UMC, Location AMC, University of Amsterdam, Amsterdam Neuroscience and Amsterdam Institute for Addiction Research, Amsterdam, The Netherlands.
⁵ Department of Psychology and Neuroscience, University of Colorado Boulder, Boulder, CO, USA.
⁶ Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA.
⁷ Behavioural Science Institute, Radboud University, Nijmegen, The Netherlands.
⁸ Clinical NeuroImaging Research Core, Division of Intramural Clinical and Biological Research, National Institute on Alcohol Abuse and Alcoholism, Bethesda, MD, USA.
⁹ Orygen, Parkville, VIC, Australia.
¹⁰ Centre for Youth Mental Health, The University of Melbourne, Melbourne, VIC, Australia.
¹¹ Department of Psychiatry, Amsterdam UMC, Location AMC, University of Amsterdam, Amsterdam, The Netherlands.
¹² Addiction Development and Psychopathology (ADAPT)-lab, Department of Psychology and Center for Urban Mental Health, University of Amsterdam, Amsterdam, The Netherlands.
¹³ Department of Psychiatry, State University of New York Downstate Medical Center, Brooklyn, NY, 11203, USA.
¹⁴ Department of Psychiatry and Psychotherapy CCM, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 10117, Berlin, Germany.
¹⁵ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159, Mannheim, Germany.
¹⁶ Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin D2, Ireland.
¹⁷ Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology and Neuroscience, SGDP Centre, King's College London, London, SE5 8AF, UK.
¹⁸ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159, Mannheim, Germany.
¹⁹ Department of Psychology, School of Social Sciences, University of Mannheim, 68131, Mannheim, Germany.
²⁰ NeuroSpin, CEA, Université Paris-Saclay, F-91191, Gif-sur-Yvette, France.
²¹ Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, NG7 2RD, UK.
²² Physikalisch-Technische Bundesanstalt (PTB), D-10587, Braunschweig and Berlin, Germany.
²³ 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, 91191, Gif-sur-Yvette, France.
²⁴ AP-HP. Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, 75013, Paris, France.
²⁵ Psychiatry Department, EPS Barthélémy Durand, 91152, Etampes, France.
²⁶ Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, Germany.
²⁷ Departments of Psychiatry and Neuroscience and Centre Hospitalier Universitaire Sainte Justine, University of Montreal, Montreal, QC, H3T 1C5, Canada.
²⁸ Departments of Psychology and Psychiatry, University of Toronto, Toronto, ON, M6A 2E1, Canada.
²⁹ Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, 37075, Göttingen, Germany.
³⁰ Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, 01062, Dresden, Germany.
³¹ Department of Psychological Medicine, Section for Eating Disorders, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, SE5 8AF, UK.
³² Department of Education and Psychology, Freie Universität Berlin, 14195, Berlin, Germany.
³³ PONS Research Group, Department of Psychiatry and Psychotherapy, Campus Charite Mitte, Humboldt University, Berlin D-10099 and Leibniz Institute for Neurobiology, 39118, Magdeburg, Germany.
³⁴ Institute for Science and Technology of Brain-inspired Intelligence (ISTBI), Fudan University, Shanghai, 200433, PR China.
³⁵ School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin D2, Ireland.
³⁶ Imaging Genetics Center, Stevens Institute for Neuroimaging and Informatics, Keck School of Medicine, University of Southern California, Marina del Rey, CA, 90292, USA.
³⁷ Department of Psychiatry, Université de Montreal, CHU Ste Justine Hospital, Montreal, QC, Canada.

PMID: 36380235
DOI: 10.1038/s41380-022-01855-6

Abstract

The neurobiological bases of the association between development and psychopathology remain poorly understood. Here, we identify a shared spatial pattern of cortical thickness (CT) in normative development and several psychiatric and neurological disorders. Principal component analysis (PCA) was applied to CT of 68 regions in the Desikan-Killiany atlas derived from three large-scale datasets comprising a total of 41,075 neurotypical participants. PCA produced a spatially broad first principal component (PC1) that was reproducible across datasets. Then PC1 derived from healthy adult participants was compared to the pattern of CT differences associated with psychiatric and neurological disorders comprising a total of 14,886 cases and 20,962 controls from seven ENIGMA disease-related working groups, normative maturation and aging comprising a total of 17,697 scans from the ABCD Study® and the IMAGEN developmental study, and 17,075 participants from the ENIGMA Lifespan working group, as well as gene expression maps from the Allen Human Brain Atlas. Results revealed substantial spatial correspondences between PC1 and widespread lower CT observed in numerous psychiatric disorders. Moreover, the PC1 pattern was also correlated with the spatial pattern of normative maturation and aging. The transcriptional analysis identified a set of genes including KCNA2, KCNS1 and KCNS2 with expression patterns closely related to the spatial pattern of PC1. The gene category enrichment analysis indicated that the transcriptional correlations of PC1 were enriched to multiple gene ontology categories and were specifically over-represented starting at late childhood, coinciding with the onset of significant cortical maturation and emergence of psychopathology during the prepubertal-to-pubertal transition. Collectively, the present study reports a reproducible latent pattern of CT that captures interregional profiles of cortical changes in both normative brain maturation and a spectrum of psychiatric disorders. The pubertal timing of the expression of PC1-related genes implicates disrupted neurodevelopment in the pathogenesis of the spectrum of psychiatric diseases emerging during adolescence.

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Cortical profiles of numerous psychiatric disorders and normal development share a common pattern

Affiliations

Cortical profiles of numerous psychiatric disorders and normal development share a common pattern

Authors

Affiliations

Abstract

References

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LinkOut - more resources

Full Text Sources

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Medical

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