Novel Gyrification Networks Reveal Links with Psychiatric Risk Factors in Early Illness

PRONIA Consortium

doi:10.1093/cercor/bhab288

Novel Gyrification Networks Reveal Links with Psychiatric Risk Factors in Early Illness

PRONIA Consortium

Department of Psychiatry and Psychotherapy, Ludwig-Maximilian University, Munich, 80336, Germany,Max Planck School of Cognition, Leipzig, 04103, Germany
Department of Psychiatry and Psychotherapy, Ludwig-Maximilian University, Munich, 80336, Germany
Department of Psychiatry and Psychotherapy, Ludwig-Maximilian University, Munich, 80336, Germany,Department of Basic Medical Science, Neuroscience and Sense Organs, University of Bari Aldo Moro, Bari, 70124, Italy
Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital, University of Cologne, Cologne, 50937, Germany
Department of Radiology and Institute of Informatics, Washington University in St. Luis, st. Luis, MO63110, USA
Department of Psychiatry and Psychotherapy, Ludwig-Maximilian University, Munich, 80336, Germany,Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital, University of Cologne, Cologne, 50937, Germany
Max Planck School of Cognition, Leipzig, 04103, Germany
Medical Faculty, University of Basel, Basel, 4051, Switzerland
Department of Psychiatry and Psychotherapy, Ludwig-Maximilian University, Munich, 80336, Germany,Max-Planck Institute of Psychiatry, Munich, 80804, Germany
Melbourne Neuropsychiatry Centrem University of Melbourne & Melbourne Health, Melbourne, 3053, Australia
Department of Psychiatry, University of Turku, Turku, 20700, Finland
Department of Psychiatry and Psychotherapy, University of Münster, Münster, 48149, Germany,Department of Psychiatry and Psychotherapy, University of Lübeck, Lübeck, 23538, Germany
Department of Basic Medical Science, Neuroscience and Sense Organs, University of Bari Aldo Moro, Bari, 70124, Italy
Department of Psychiatry and Psychotherapy, Medical Faculty, Heinrich-Heine University, Düsseldorf, 40629, Germany
Department of Psychiatry and Psychotherapy, University of Lübeck, Lübeck, 23538, Germany,Department of Psychiatry (Psychiatric University Hospital, UPK), University of Basel, Basel, 4002, Switzerland
Department of Neurosciences and Mental Health, Fondazione IRCCS Ca' Grande Ospedale Maggiore Policlinico, Milano, 20122, Italy,Department of Pathophysiology and Transplantation, University of Milan, Milan, 20122, Italy
Centre for Youth Mental Health, University of Melbourne, Melbourne, 3052, Australia,Orygen, Melbourne, 3052, Australia,School of Psychology, University of Birmingham, Birmingham, B15 2TT, UK
Institute for Mental Health, University of Birmingham, Birmingham, B15 2TT, UK,Early Intervention Service, Birmingham Women’s and Children’s NHS foundation Trust, Birmingham, B4 6NH, UK
Department of Psychiatry and Psychotherapy, Medical Faculty, Heinrich-Heine University, Düsseldorf, 40629, Germany,Department of Psychology and Mental Health, Faculty of Psychology, Airlangga University, Surubaya, 60286, Indonesia,University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bern, 3000, Switzerland
Department of Psychiatry and Psychotherapy, Ludwig-Maximilian University, Munich, 80336, Germany,Max-Planck Institute of Psychiatry, Munich, 80804, Germany,Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, SE5 8AF, UK

Research output: Contribution to journal › Article › peer-review

6 Citations (Scopus)

Abstract

Adult gyrification provides a window into coordinated early neurodevelopment when disruptions predispose individuals to psychiatric illness. We hypothesized that the echoes of such disruptions should be observed within structural gyrification networks in early psychiatric illness that would demonstrate associations with developmentally relevant variables rather than specific psychiatric symptoms. We employed a new data-driven method (Orthogonal Projective Non-Negative Matrix Factorization) to delineate novel gyrification-based networks of structural covariance in 308 healthy controls. Gyrification within the networks was then compared to 713 patients with recent onset psychosis or depression, and at clinical high-risk. Associations with diagnosis, symptoms, cognition, and functioning were investigated using linear models. Results demonstrated 18 novel gyrification networks in controls as verified by internal and external validation. Gyrification was reduced in patients in temporal-insular, lateral occipital, and lateral fronto-parietal networks (pFDR < 0.01) and was not moderated by illness group. Higher gyrification was associated with better cognitive performance and lifetime role functioning, but not with symptoms. The findings demonstrated that gyrification can be parsed into novel brain networks that highlight generalized illness effects linked to developmental vulnerability. When combined, our study widens the window into the etiology of psychiatric risk and its expression in adulthood.

Original language	English
Pages (from-to)	1625-1636
Journal	Cerebral Cortex
Volume	32
Issue number	8
Early online date	14 Sept 2021
DOIs	https://doi.org/10.1093/cercor/bhab288
Publication status	Published - 15 Apr 2022

Bibliographical note

Funding: This work was supported by PRONIA: a Collaboration Project funded by the European Union under the 7th Framework Program under grant agreement number 602152. BMBF and Max Planck Society (grant agreement number M526300) funded R.S. Structural European Funding of the Italian Minister of Education (Attraction and International Mobility—AIM—action, grant agreement No 1859959) funded L.A.A. NIH/NIA supported A.S. (grant R01AG06710). National Health and Medical Research Council Senior Principal Research Fellowship (grants 628386 and 1105825) and European Union–National Health and Medical Research Council (grant 1075379) supported C.P., S.R., A.R-R., and N.K. reported receiving grants from the European Union (EU) during the conduct of the study.

Keywords

clinical high risk
cortical folding
depression
psychosis
structural covariance

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10.1093/cercor/bhab288

Cite this

@article{a17f5f20bbf74ca89048403a12a8df57,

title = "Novel Gyrification Networks Reveal Links with Psychiatric Risk Factors in Early Illness",

abstract = "Adult gyrification provides a window into coordinated early neurodevelopment when disruptions predispose individuals to psychiatric illness. We hypothesized that the echoes of such disruptions should be observed within structural gyrification networks in early psychiatric illness that would demonstrate associations with developmentally relevant variables rather than specific psychiatric symptoms. We employed a new data-driven method (Orthogonal Projective Non-Negative Matrix Factorization) to delineate novel gyrification-based networks of structural covariance in 308 healthy controls. Gyrification within the networks was then compared to 713 patients with recent onset psychosis or depression, and at clinical high-risk. Associations with diagnosis, symptoms, cognition, and functioning were investigated using linear models. Results demonstrated 18 novel gyrification networks in controls as verified by internal and external validation. Gyrification was reduced in patients in temporal-insular, lateral occipital, and lateral fronto-parietal networks (pFDR < 0.01) and was not moderated by illness group. Higher gyrification was associated with better cognitive performance and lifetime role functioning, but not with symptoms. The findings demonstrated that gyrification can be parsed into novel brain networks that highlight generalized illness effects linked to developmental vulnerability. When combined, our study widens the window into the etiology of psychiatric risk and its expression in adulthood.",

keywords = "clinical high risk, cortical folding, depression, psychosis, structural covariance",

author = "Rachele Sanfelici and Anne Ruef and Antonucci, \{Linda A\} and Nora Penzel and Aristeidis Sotiras and Dong, \{Mark Sen\} and Maria Urquijo-Castro and Julian Wenzel and Lana Kambeitz-Ilankovic and Hettwer, \{Meike D\} and Stephan Ruhrmann and Katharine Chisholm and Anita Riecher-R{\"o}ssler and Peter Falkai and Christos Pantelis and Salokangas, \{Raimo K R\} and Rebekka Lencer and Alessandro Bertolino and Joseph Kambeitz and Eva Meisenzahl and Stefan Borgwardt and Paolo Brambilla and Wood, \{Stephen J\} and Rachel Upthegrove and Frauke Schultze-Lutter and Nikolaos Koutsouleris and Dwyer, \{Dominic B\} and \{PRONIA Consortium\}",

note = "Funding: This work was supported by PRONIA: a Collaboration Project funded by the European Union under the 7th Framework Program under grant agreement number 602152. BMBF and Max Planck Society (grant agreement number M526300) funded R.S. Structural European Funding of the Italian Minister of Education (Attraction and International Mobility—AIM—action, grant agreement No 1859959) funded L.A.A. NIH/NIA supported A.S. (grant R01AG06710). National Health and Medical Research Council Senior Principal Research Fellowship (grants 628386 and 1105825) and European Union–National Health and Medical Research Council (grant 1075379) supported C.P., S.R., A.R-R., and N.K. reported receiving grants from the European Union (EU) during the conduct of the study.",

year = "2022",

month = apr,

day = "15",

doi = "10.1093/cercor/bhab288",

language = "English",

volume = "32",

pages = "1625--1636",

journal = "Cerebral Cortex",

issn = "1047-3211",

publisher = "Oxford University Press",

number = "8",

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TY - JOUR

T1 - Novel Gyrification Networks Reveal Links with Psychiatric Risk Factors in Early Illness

AU - Sanfelici, Rachele

AU - Ruef, Anne

AU - Antonucci, Linda A

AU - Penzel, Nora

AU - Sotiras, Aristeidis

AU - Dong, Mark Sen

AU - Urquijo-Castro, Maria

AU - Wenzel, Julian

AU - Kambeitz-Ilankovic, Lana

AU - Hettwer, Meike D

AU - Ruhrmann, Stephan

AU - Chisholm, Katharine

AU - Riecher-Rössler, Anita

AU - Falkai, Peter

AU - Pantelis, Christos

AU - Salokangas, Raimo K R

AU - Lencer, Rebekka

AU - Bertolino, Alessandro

AU - Kambeitz, Joseph

AU - Meisenzahl, Eva

AU - Borgwardt, Stefan

AU - Brambilla, Paolo

AU - Wood, Stephen J

AU - Upthegrove, Rachel

AU - Schultze-Lutter, Frauke

AU - Koutsouleris, Nikolaos

AU - Dwyer, Dominic B

AU - PRONIA Consortium

N1 - Funding: This work was supported by PRONIA: a Collaboration Project funded by the European Union under the 7th Framework Program under grant agreement number 602152. BMBF and Max Planck Society (grant agreement number M526300) funded R.S. Structural European Funding of the Italian Minister of Education (Attraction and International Mobility—AIM—action, grant agreement No 1859959) funded L.A.A. NIH/NIA supported A.S. (grant R01AG06710). National Health and Medical Research Council Senior Principal Research Fellowship (grants 628386 and 1105825) and European Union–National Health and Medical Research Council (grant 1075379) supported C.P., S.R., A.R-R., and N.K. reported receiving grants from the European Union (EU) during the conduct of the study.

PY - 2022/4/15

Y1 - 2022/4/15

N2 - Adult gyrification provides a window into coordinated early neurodevelopment when disruptions predispose individuals to psychiatric illness. We hypothesized that the echoes of such disruptions should be observed within structural gyrification networks in early psychiatric illness that would demonstrate associations with developmentally relevant variables rather than specific psychiatric symptoms. We employed a new data-driven method (Orthogonal Projective Non-Negative Matrix Factorization) to delineate novel gyrification-based networks of structural covariance in 308 healthy controls. Gyrification within the networks was then compared to 713 patients with recent onset psychosis or depression, and at clinical high-risk. Associations with diagnosis, symptoms, cognition, and functioning were investigated using linear models. Results demonstrated 18 novel gyrification networks in controls as verified by internal and external validation. Gyrification was reduced in patients in temporal-insular, lateral occipital, and lateral fronto-parietal networks (pFDR < 0.01) and was not moderated by illness group. Higher gyrification was associated with better cognitive performance and lifetime role functioning, but not with symptoms. The findings demonstrated that gyrification can be parsed into novel brain networks that highlight generalized illness effects linked to developmental vulnerability. When combined, our study widens the window into the etiology of psychiatric risk and its expression in adulthood.

AB - Adult gyrification provides a window into coordinated early neurodevelopment when disruptions predispose individuals to psychiatric illness. We hypothesized that the echoes of such disruptions should be observed within structural gyrification networks in early psychiatric illness that would demonstrate associations with developmentally relevant variables rather than specific psychiatric symptoms. We employed a new data-driven method (Orthogonal Projective Non-Negative Matrix Factorization) to delineate novel gyrification-based networks of structural covariance in 308 healthy controls. Gyrification within the networks was then compared to 713 patients with recent onset psychosis or depression, and at clinical high-risk. Associations with diagnosis, symptoms, cognition, and functioning were investigated using linear models. Results demonstrated 18 novel gyrification networks in controls as verified by internal and external validation. Gyrification was reduced in patients in temporal-insular, lateral occipital, and lateral fronto-parietal networks (pFDR < 0.01) and was not moderated by illness group. Higher gyrification was associated with better cognitive performance and lifetime role functioning, but not with symptoms. The findings demonstrated that gyrification can be parsed into novel brain networks that highlight generalized illness effects linked to developmental vulnerability. When combined, our study widens the window into the etiology of psychiatric risk and its expression in adulthood.

KW - clinical high risk

KW - cortical folding

KW - depression

KW - psychosis

KW - structural covariance

UR - https://academic.oup.com/cercor/advance-article/doi/10.1093/cercor/bhab288/6369971

U2 - 10.1093/cercor/bhab288

DO - 10.1093/cercor/bhab288

M3 - Article

SN - 1047-3211

VL - 32

SP - 1625

EP - 1636

JO - Cerebral Cortex

JF - Cerebral Cortex

IS - 8

ER -

Novel Gyrification Networks Reveal Links with Psychiatric Risk Factors in Early Illness

Abstract

Bibliographical note

Keywords

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