Psychotic Like Experiences in Healthy Adolescents are Underpinned by Lower Fronto-Temporal Cortical Gyrification: a Study from the IMAGEN Consortium

Author:

Maitra Raka1ORCID,Horne Charlotte M1,O’Daly Owen2,Papanastasiou Evangelos13,Gaser Christian45,Banaschewski Tobias6,Barker Gareth J2,Bokde Arun L W7,Desrivières Sylvane8,Flor Herta910,Grigis Antoine11,Garavan Hugh12,Gowland Penny13ORCID,Heinz Andreas14,Brühl Rüdiger15,Martinot Jean-Luc16,Paillère Martinot Marie-Laure17ORCID,Artiges Eric18,Nees Frauke6919,Papadopoulos Orfanos Dimitri11,Lemaitre Herve1120ORCID,Paus Tomáš2122ORCID,Poustka Luise23,Hohmann Sarah6,Millenet Sabina6,Fröhner Juliane H24,Robinson Lauren25,Smolka Michael N24,Walter Henrik14,Winterer Jeanne M1426,Whelan Robert27,Burke Quinlan Erin8,Ing Alex8,Schumann Gunter8192829,Shergill Sukhi130, ,

Affiliation:

1. Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London , UK

2. Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King’s College London , UK

3. Therapeutic Area CNS, Boehringer Ingelheim International GmbH , Inghelheim , Germany

4. Departments of Neurology, Jena University Hospital , Jena , Germany

5. Departments of Psychiatry and Psychotherapy, Jena University Hospital , Jena , Germany

6. Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University , Mannheim , Germany

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

8. Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology and Neuroscience, Social, Genetic and Developmental Psychiatry Centre, King’s College London , UK

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

10. Department of Psychology, School of Social Sciences, University of Mannheim , Mannheim , Germany

11. NeuroSpin, CEA, Université Paris-Saclay , Gif-sur-Yvette , France

12. Departments of Psychiatry and Psychology, University of Vermont , Burlington, Vermont , USA

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

14. Department of Psychiatry and Psychotherapy CCM, Charité—Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health , Berlin , Germany

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

16. Institut National de la Santé et de la Recherche Médicale, INSERM U 1299 “Trajectoires développementales en psychiatrie”; Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli , Gif-sur-Yvette , France

17. Institut National de la Santé et de la Recherce Médicale, INSERM U 1299 “Trajectoires développementales and psychiatrie”, University Paris-Saclay, Ecole Normale Supérieure Paris-Saclay, CNRS; Centre Borelli, Gif-sur-Yvette, France; and AP-HP. Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital , Paris , France

18. Institut National de la Santé et de la Recherche Médicale, INSERM U 1299 “Trajectoires développementales en psychiatrie”; Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Gif-sur-Yvette; and Psychiatry Department, EPS Barthélémy Durand , Etampes , France

19. PONS Research Group, Dept of Psychiatry and Psychotherapy, Campus Charite Mitte, Humboldt University , Berlin , Germany

20. Institut des Maladies Neurodégénératives, UMR 5293, CNRS, CEA, Université de Bordeaux , Bordeaux , France

21. Departments of Psychiatry and Neuroscience, Faculty of Medicine and Centre Hospitalier Universitaire Sainte-Justine, University of Montreal , Montreal, Quebec , Canada

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

23. Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen , Göttingen , Germany

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

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

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

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

28. Leibniz Institute for Neurobiology , Magdeburg , Germany

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

30. Kent and Medway Medical School , Canterbury , UK

Abstract

Abstract Background and Hypothesis Psychotic Like Experiences (PLEs) are widely prevalent in children and adolescents and increase the risk of developing psychosis. Cortical gyrification characterizes brain development from in utero till about the first 2 years of life and can be measured in later years as static gyrification changes demonstrating neurodevelopment and dynamic gyrification changes reflecting brain maturation during adolescence. We hypothesized that PLEs would be associated with static cortical gyrification changes reflecting a neurodevelopmental abnormality. Study Design We studied 1252 adolescents recruited in the IMAGEN consortium. We used a longitudinal study design, with Magnetic Resonance Imaging measurements at age 14 years and age 19 years; measurement of PLEs using the Community Assessment of Psychic Experiences (CAPE) questionnaire at age 19 years; and clinical diagnoses at age 23 years. Study Results Our results show static gyrification changes in adolescents with elevated PLEs on 3 items of the CAPE—voice hearing, unusual experiences of receiving messages, and persecutory ideas—with lower cortical gyrification in fronto-temporal regions in the left hemisphere. This group also demonstrated dynamic gyrification changes with higher cortical gyrification in right parietal cortex in late adolescence; a finding that we replicated in an independent sample of patients with first-episode psychosis. Adolescents with high PLEs were also 5.6 times more likely to transition to psychosis in adulthood by age 23 years. Conclusions This is the largest study in adolescents that demonstrates fronto-temporal abnormality of cortical gyrification as a potential biomarker for vulnerability to PLEs and transition to psychosis.

Funder

Deutsche Forschungsgemeinschaft

Fondation de France

Interface

National Institute for Health Research

Medical Research Council

Medical Research Foundation

National Institutes of Health

Mission Interministérielle de Lutte Contre les Drogues et les Conduites Addictives

Fondation pour la Recherche Médicale

South London and Maudsley NHS Foundation Trust

King's College London

Publisher

Oxford University Press (OUP)

Subject

Psychiatry and Mental health

Reference61 articles.

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3. Genome-wide analysis of adolescent psychotic-like experiences shows genetic overlap with psychiatric disorders;Pain;Am J Med Genet.,2018

4. Developmental trajectories of psychotic-like experiences across adolescence: impact of victimization and substance use;Mackie;Psychol Med.,2011

5. Prevalence of psychotic symptoms in childhood and adolescence: a systematic review and meta-analysis of population-based studies;Kelleher;Psychol Med.,2012

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