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Prefrontal cortical thinning links to negative symptoms in schizophrenia via the ENIGMA consortium

Published online by Cambridge University Press:  26 May 2017

E. Walton ,
D. P. Hibar ,
T. G. M. van Erp ,
S. G. Potkin ,
R. Roiz-Santiañez ,
B. Crespo-Facorro ,
P. Suarez-Pinilla ,
N. E. M. van Haren ,
S. M. C. de Zwarte  and
R. S. Kahn
...Show all authors
E. Walton
Affiliation:
Department of Psychology, Georgia State University, Atlanta, GA 30302, USA Division of Psychological and Social Medicine and Developmental Neurosciences, Faculty of Medicine, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany Department of Psychology, Institute of Psychology, Psychiatry and Neuroscience, King's College London, London, SE5 8AF, UK
D. P. Hibar
Affiliation:
Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging & Informatics, University of Southern California, Marina del Rey, CA, USA
T. G. M. van Erp
Affiliation:
Department of Psychiatry and Human Behavior, University of California, Irvine, California
S. G. Potkin
Affiliation:
Department of Psychiatry and Human Behavior, University of California, Irvine, California
R. Roiz-Santiañez
Affiliation:
Department of Psychiatry, University Hospital Marqués de Valdecilla, School of Medicine, University of Cantabria–IDIVAL, Avda. Valdecilla s/n, 39008, Santander, Spain Cibersam (Centro Investigación Biomédica en Red Salud Mental), Avda. Valdecilla s/n, 39008, Santander, Spain
B. Crespo-Facorro
Affiliation:
Department of Psychiatry, University Hospital Marqués de Valdecilla, School of Medicine, University of Cantabria–IDIVAL, Avda. Valdecilla s/n, 39008, Santander, Spain Cibersam (Centro Investigación Biomédica en Red Salud Mental), Avda. Valdecilla s/n, 39008, Santander, Spain
P. Suarez-Pinilla
Affiliation:
Department of Psychiatry, University Hospital Marqués de Valdecilla, School of Medicine, University of Cantabria–IDIVAL, Avda. Valdecilla s/n, 39008, Santander, Spain Cibersam (Centro Investigación Biomédica en Red Salud Mental), Avda. Valdecilla s/n, 39008, Santander, Spain
N. E. M. van Haren
Affiliation:
Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
S. M. C. de Zwarte
Affiliation:
Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
R. S. Kahn
Affiliation:
Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
W. Cahn
Affiliation:
Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
N. T. Doan
Affiliation:
NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, University of Oslo, P.O. Box 4956 Nydalen, 0424 Oslo, Norway
K. N. Jørgensen
Affiliation:
NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, University of Oslo, P.O. Box 4956 Nydalen, 0424 Oslo, Norway Department of Psychiatric Research, Diakonhjemmet Hospital, P.O. Box 85 Vinderen, 0319 Oslo, Norway
T. P. Gurholt
Affiliation:
NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, University of Oslo, P.O. Box 4956 Nydalen, 0424 Oslo, Norway
I. Agartz
Affiliation:
NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, University of Oslo, P.O. Box 4956 Nydalen, 0424 Oslo, Norway Department of Psychiatric Research, Diakonhjemmet Hospital, P.O. Box 85 Vinderen, 0319 Oslo, Norway Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden
O. A. Andreassen
Affiliation:
NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, University of Oslo, P.O. Box 4956 Nydalen, 0424 Oslo, Norway NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital, P.O. Box 4956 Nydalen, 0424, Oslo, Norway
L. T. Westlye
Affiliation:
NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital, P.O. Box 4956 Nydalen, 0424, Oslo, Norway
I. Melle
Affiliation:
NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, University of Oslo, P.O. Box 4956 Nydalen, 0424 Oslo, Norway NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital, P.O. Box 4956 Nydalen, 0424, Oslo, Norway
A. O. Berg
Affiliation:
NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, University of Oslo, P.O. Box 4956 Nydalen, 0424 Oslo, Norway
L. Morch-Johnsen
Affiliation:
NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, University of Oslo, P.O. Box 4956 Nydalen, 0424 Oslo, Norway Department of Psychiatric Research, Diakonhjemmet Hospital, P.O. Box 85 Vinderen, 0319 Oslo, Norway
A. Færden
Affiliation:
Division of Mental Health and Addiction, Oslo University Hospital, P.O. Box 4956 Nydalen, 0424, Oslo, Norway
L. Flyckt
Affiliation:
Department of Clinical Neuroscience, Karolinska Institutet, Centre for Psychiatry Research, Norra Stationsgatan 69, 113 64 Stockholm, Sweden
H. Fatouros-Bergman
Affiliation:
Department of Clinical Neuroscience, Karolinska Institutet, Centre for Psychiatry Research, Norra Stationsgatan 69, 113 64 Stockholm, Sweden
E. G. Jönsson
Affiliation:
NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, University of Oslo, P.O. Box 4956 Nydalen, 0424 Oslo, Norway Department of Clinical Neuroscience, Karolinska Institutet, 171 77 Stockholm, Sweden
R. Hashimoto
Affiliation:
Molecular Research Center for Children's Mental Development, United Graduate School of Child Development, Osaka University, D3, 2-2, Yamadaoka, Suita, Osaka, 565-0871, Japan Department of Psychiatry, Osaka University Graduate School of Medicine D3, 2-2, Yamadaoka, Suita, Osaka, 565-0871, Japan
H. Yamamori
Affiliation:
Department of Psychiatry, Osaka University Graduate School of Medicine D3, 2-2, Yamadaoka, Suita, Osaka, 565-0871, Japan
M. Fukunaga
Affiliation:
Division of Cerebral Integration, National Institute for Physiological Sciences, 38 Nishigonaka Myodaiji, Okazaki, Aichi, 444-8585, Japan
N. Jahanshad
Affiliation:
Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging & Informatics, University of Southern California, Marina del Rey, CA, USA
P. De Rossi
Affiliation:
NESMOS Department (Neurosciences, Mental Health and Sensory Functions), School of Medicine and Psychology, Sapienza University, Rome, Italy Department of Clinical and Behavioural Neurology, IRCCS Santa Lucia Foundation, 00179, Rome, Italy Department of Neurology and Psychiatry, Sapienza University of Rome, Rome, Italy
F. Piras
Affiliation:
Department of Clinical and Behavioural Neurology, IRCCS Santa Lucia Foundation, 00179, Rome, Italy Centro Fermi - Museo Storico della Fisica e Centro Studi e Ricerche “Enrico Fermi”, Rome, Italy
N. Banaj
Affiliation:
Department of Clinical and Behavioural Neurology, IRCCS Santa Lucia Foundation, 00179, Rome, Italy
G. Spalletta
Affiliation:
Department of Clinical and Behavioural Neurology, IRCCS Santa Lucia Foundation, 00179, Rome, Italy Beth K. and Stuart C. Yudofsky Division of Neuropsychiatry Menninger, Department of Psychiatry and Behavioral Sciences Baylor College of Medicine Houston, TX, USA
R. E. Gur
Affiliation:
Brain Behavior Laboratory, University of Pennsylvania, Philadelphia, PA 19104, USA
R. C. Gur
Affiliation:
Brain Behavior Laboratory, University of Pennsylvania, Philadelphia, PA 19104, USA
D. H. Wolf
Affiliation:
Brain Behavior Laboratory, University of Pennsylvania, Philadelphia, PA 19104, USA
T. D. Satterthwaite
Affiliation:
Brain Behavior Laboratory, University of Pennsylvania, Philadelphia, PA 19104, USA
L. M. Beard
Affiliation:
Brain Behavior Laboratory, University of Pennsylvania, Philadelphia, PA 19104, USA
I. E. Sommer
Affiliation:
Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
S. Koops
Affiliation:
Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
O. Gruber
Affiliation:
Department of Psychiatry and Psychotherapy, Center for Translational Research in Systems Neuroscience and Psychiatry, University Medical Center Göttingen, Von-Siebold-Str. 5, 37075 Göttingen, Germany
A. Richter
Affiliation:
Department of Psychiatry and Psychotherapy, Center for Translational Research in Systems Neuroscience and Psychiatry, University Medical Center Göttingen, Von-Siebold-Str. 5, 37075 Göttingen, Germany
B. Krämer
Affiliation:
Department of Psychiatry and Psychotherapy, Center for Translational Research in Systems Neuroscience and Psychiatry, University Medical Center Göttingen, Von-Siebold-Str. 5, 37075 Göttingen, Germany
S. Kelly
Affiliation:
Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging & Informatics, University of Southern California, Marina del Rey, CA, USA Trinity College, Dublin, Ireland
G. Donohoe
Affiliation:
Centre for Neuroimaging and Cognitive Genomics (NICOG), NCBES Galway Neuroscience Centre, National University of Ireland Galway, Galway, Ireland
C. McDonald
Affiliation:
Centre for Neuroimaging and Cognitive Genomics (NICOG), NCBES Galway Neuroscience Centre, National University of Ireland Galway, Galway, Ireland
D. M. Cannon
Affiliation:
Centre for Neuroimaging and Cognitive Genomics (NICOG), NCBES Galway Neuroscience Centre, National University of Ireland Galway, Galway, Ireland
A. Corvin
Affiliation:
Trinity College, Dublin, Ireland
M. Gill
Affiliation:
Trinity College, Dublin, Ireland
A. Di Giorgio
Affiliation:
Section of Psychiatry and Psychology, IRCCS Casa Sollievo della Sofferenza, S.G. Rotondo (FG), 71013, Italy
A. Bertolino
Affiliation:
Psychiatric Neuroscience Group, University of Bari ‘Aldo Moro’, Bari, 70124, Italy
S. Lawrie
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Morningside, Edinburgh, EH10 5HF, UK
T. Nickson
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Morningside, Edinburgh, EH10 5HF, UK
H. C. Whalley
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Morningside, Edinburgh, EH10 5HF, UK
E. Neilson
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Morningside, Edinburgh, EH10 5HF, UK
V. D. Calhoun
Affiliation:
The Mind Research Network, Albuquerque, NM 87106, USA Department of Electrical and Computer Engineering, University of New Mexico, Albuquerque, NM 87131, USA
P. M. Thompson
Affiliation:
Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging & Informatics, University of Southern California, Marina del Rey, CA, USA
J. A. Turner
Affiliation:
Department of Psychology and Neuroscience Institute, Georgia State University, Atlanta, GA 30302, USA
S. Ehrlich*
Affiliation:
Division of Psychological and Social Medicine and Developmental Neurosciences, Faculty of Medicine, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany
*
*Address for correspondence: S. Ehrlich, M.D., Division of Psychological and Social Medicine and Developmental Neurosciences, Faculty of Medicine, Technische Universität Dresden, Fetscherstr. 74, 01307 Dresden, Germany. (Email: [email protected])
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Abstract

Background

Our understanding of the complex relationship between schizophrenia symptomatology and etiological factors can be improved by studying brain-based correlates of schizophrenia. Research showed that impairments in value processing and executive functioning, which have been associated with prefrontal brain areas [particularly the medial orbitofrontal cortex (MOFC)], are linked to negative symptoms. Here we tested the hypothesis that MOFC thickness is associated with negative symptom severity.

Methods

This study included 1985 individuals with schizophrenia from 17 research groups around the world contributing to the ENIGMA Schizophrenia Working Group. Cortical thickness values were obtained from T1-weighted structural brain scans using FreeSurfer. A meta-analysis across sites was conducted over effect sizes from a model predicting cortical thickness by negative symptom score (harmonized Scale for the Assessment of Negative Symptoms or Positive and Negative Syndrome Scale scores).

Results

Meta-analytical results showed that left, but not right, MOFC thickness was significantly associated with negative symptom severity (βstd = −0.075; p = 0.019) after accounting for age, gender, and site. This effect remained significant (p = 0.036) in a model including overall illness severity. Covarying for duration of illness, age of onset, antipsychotic medication or handedness weakened the association of negative symptoms with left MOFC thickness. As part of a secondary analysis including 10 other prefrontal regions further associations in the left lateral orbitofrontal gyrus and pars opercularis emerged.

Conclusions

Using an unusually large cohort and a meta-analytical approach, our findings point towards a link between prefrontal thinning and negative symptom severity in schizophrenia. This finding provides further insight into the relationship between structural brain abnormalities and negative symptoms in schizophrenia.

Keywords

Cortical thicknessENIGMAFreeSurfermedial orbitofrontal cortexMRInegative symptomsPANSSSANSschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 48 , Issue 1 , January 2018 , pp. 82 - 94
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

†

Members of Karolinska Schizophrenia Project (KaSP) are listed at the end of the article as collaborators.

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