Meta-Analysis

. 2022 Jan;43(1):470-499.

doi: 10.1002/hbm.25204. Epub 2020 Oct 12.

Greater male than female variability in regional brain structure across the lifespan

Lara M Wierenga^{1

2}, Gaelle E Doucet^{3

4}, Danai Dima^{5

6}, Ingrid Agartz^{7

8

9}, Moji Aghajani^{10

11

12}, Theophilus N Akudjedu^{13

14}, Anton Albajes-Eizagirre^{15

16

17}, Dag Alnaes^{7

18}, Kathryn I Alpert¹⁹, Ole A Andreassen^{7

18}, Alan Anticevic²⁰, Philip Asherson²¹, Tobias Banaschewski²², Nuria Bargallo^{23

24}, Sarah Baumeister²², Ramona Baur-Streubel²⁵, Alessandro Bertolino²⁶, Aurora Bonvino²⁶, Dorret I Boomsma²⁷, Stefan Borgwardt^{28

29}, Josiane Bourque^{30

31}, Anouk den Braber^{27

32}, Daniel Brandeis^{22

33

34

35}, Alan Breier³⁶, Henry Brodaty^{37

38}, Rachel M Brouwer³⁹, Jan K Buitelaar^{40

41}, Geraldo F Busatto⁴², Vince D Calhoun⁴³, Erick J Canales-Rodríguez^{15

16}, Dara M Cannon¹³, Xavier Caseras⁴⁴, Francisco X Castellanos^{45

46}, Tiffany M Chaim-Avancini⁴², Christopher Rk Ching⁴⁷, Vincent P Clark^{48

49}, Patricia J Conrod^{31

50}, Annette Conzelmann^{51

52}, Fabrice Crivello⁵³, Christopher G Davey^{54

55}, Erin W Dickie^{56

57}, Stefan Ehrlich⁵⁸, Dennis Van't Ent²⁷, Simon E Fisher^{59

60}, Jean-Paul Fouche⁶¹, Barbara Franke^{60

62

63}, Paola Fuentes-Claramonte^{15

16}, Eco Jc de Geus²⁷, Annabella Di Giorgio⁶⁴, David C Glahn^{65

66}, Ian H Gotlib⁶⁷, Hans J Grabe^{68

69}, Oliver Gruber⁷⁰, Patricia Gruner²⁰, Raquel E Gur^{30

71}, Ruben C Gur³⁰, Tiril P Gurholt^{7

18}, Lieuwe de Haan⁷², Beathe Haatveit^{7

18}, Ben J Harrison⁷³, Catharina A Hartman⁷⁴, Sean N Hatton^{75

76}, Dirk J Heslenfeld⁷⁷, Odile A van den Heuvel^{10

78}, Ian B Hickie⁷⁵, Pieter J Hoekstra⁷⁹, Sarah Hohmann²², Avram J Holmes^{20

80

81}, Martine Hoogman^{60

62}, Norbert Hosten⁸², Fleur M Howells^{83

84}, Hilleke E Hulshoff Pol³⁹, Chaim Huyser^{85

86}, Neda Jahanshad⁴⁷, Anthony C James^{87

88}, Jiyang Jiang³⁷, Erik G Jönsson^{7

9}, John A Joska⁸⁴, Andrew J Kalnin⁸⁹; Karolinska Schizophrenia Project (KaSP) Consortium; Marieke Klein^{39

60

62}, Laura Koenders⁷², Knut K Kolskår^{18

90

91}, Bernd Krämer⁷⁰, Jonna Kuntsi²¹, Jim Lagopoulos^{92

93}, Luisa Lazaro^{16

94

95

96}, Irina S Lebedeva⁹⁷, Phil H Lee^{81

98}, Christine Lochner⁹⁹, Marise Wj Machielsen¹⁰⁰, Sophie Maingault¹⁰¹, Nicholas G Martin¹⁰², Ignacio Martínez-Zalacaín^{103

104}, David Mataix-Cols⁹, Bernard Mazoyer^{105

106}, Brenna C McDonald¹⁰⁷, Colm McDonald¹³, Andrew M McIntosh¹⁰⁸, Katie L McMahon^{109

110}, Genevieve McPhilemy¹³, Dennis van der Meer^{7

18

111}, José M Menchón^{16

103

104}, Jilly Naaijen⁴⁰, Lars Nyberg^{112

113}, Jaap Oosterlaan^{114

115}, Yannis Paloyelis⁶, Paul Pauli^{116

117}, Giulio Pergola^{26

118}, Edith Pomarol-Clotet^{15

16}, Maria J Portella^{16

119}, Joaquim Radua^{9

15

16

17

120}, Andreas Reif¹²¹, Geneviève Richard^{7

18}, Joshua L Roffman¹²², Pedro Gp Rosa⁴², Matthew D Sacchet¹²³, Perminder S Sachdev^{37

124}, Raymond Salvador^{15

16}, Salvador Sarró^{15

16}, Theodore D Satterthwaite³⁰, Andrew J Saykin^{107

125}, Mauricio H Serpa⁴², Kang Sim^{126

127}, Andrew Simmons¹²⁸, Jordan W Smoller^{81

129}, Iris E Sommer¹³⁰, Carles Soriano-Mas^{16

103

131}, Dan J Stein¹³², Lachlan T Strike¹³³, Philip R Szeszko^{3

134}, Henk S Temmingh⁸⁴, Sophia I Thomopoulos⁴⁷, Alexander S Tomyshev⁹⁷, Julian N Trollor³⁷, Anne Uhlmann^{84

135}, Ilya M Veer¹³⁶, Dick J Veltman¹³⁷, Aristotle Voineskos⁵⁶, Henry Völzke^{138

139

140}, Henrik Walter¹³⁶, Lei Wang¹⁹, Yang Wang¹⁴¹, Bernd Weber¹⁴², Wei Wen³⁷, John D West¹⁰⁷, Lars T Westlye^{7

18

90}, Heather C Whalley^{108

143}, Steven Cr Williams¹⁴⁴, Katharina Wittfeld^{68

69}, Daniel H Wolf³⁰, Margaret J Wright^{133

145}, Yuliya N Yoncheva¹⁴⁶, Marcus V Zanetti^{42

147}, Georg C Ziegler¹⁴⁸, Greig I de Zubicaray¹¹⁰, Paul M Thompson⁴⁷, Eveline A Crone^{1

2

149}, Sophia Frangou^{3

150}, Christian K Tamnes^{7

8

151}

Affiliations

¹ Institute of Psychology, Leiden University, Leiden, The Netherlands.
² Leiden Institute for Brain and Cognition, Leiden, The Netherlands.
³ Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, New York, USA.
⁴ Boys Town National Research Hospital, Omaha, Nebraska, USA.
⁵ Department of Psychology, School of Arts and Social Sciences, City, University of London, London, UK.
⁶ Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁷ Norwegian Centre for Mental Disorders Research (NORMENT), Division of Mental Health and Addiction, Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
⁸ Department of Psychiatric Research, Diakonhjemmet Hospital, Oslo, Norway.
⁹ Centre for Psychiatry Research, Department of Clinical Neuroscience, Karolinska Institutet, & Stockholm Health Care Services, Stockholm County Council, Stockholm, Sweden.
¹⁰ Department of Psychiatry, Amsterdam Neuroscience, Amsterdam UMC, Vrije Universiteit, Amsterdam, The Netherlands.
¹¹ Department of Research & Innovation, GGZ inGeest, Amsterdam, The Netherlands.
¹² Institute of Education and Child Studies, Forensic Family and Youth Care, Leiden University, Leiden, The Netherlands.
¹³ Centre for Neuroimaging & Cognitive Genomics (NICOG), Clinical Neuroimaging Laboratory, NCBES Galway Neuroscience Centre, College of Medicine Nursing and Health Sciences, National University of Ireland Galway, Galway, Ireland.
¹⁴ Institute of Medical Imaging & Visualisation, Faculty of Health & Social Sciences, Bournemouth University, Bournemouth, UK.
¹⁵ FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain.
¹⁶ Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Madrid, Spain.
¹⁷ Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
¹⁸ Norwegian Centre for Mental Disorders Research (NORMENT), Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.
¹⁹ Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
²⁰ Department of Psychiatry, Yale University, New Haven, Connecticut, USA.
²¹ Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
²² Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, University of Heidelberg, Medical Faculty Mannheim, Mannheim, Germany.
²³ Imaging Diagnostic Center, Hospital Clínic, Barcelona, Spain.
²⁴ Magnetic Resonance Image Core Facility, IDIBAPS, Barcelona, Spain.
²⁵ Department for Clinical Psychology, Würzburg University, Margetshöchheim, Germany.
²⁶ Department of Basic Medical Science, Neuroscience and Sense Organs, University of Bari Aldo Moro, Bari, Italy.
²⁷ Department of Biological Psychology, VU University Amsterdam, Amsterdam, The Netherlands.
²⁸ Department of Psychiatry, University of Basel, Basel, Switzerland.
²⁹ Department of Psychiatry, University of Lübeck, Lübeck, Germany.
³⁰ Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
³¹ CHU Sainte-Justine Research Center, Montreal, Quebec, Canada.
³² Alzheimer Center, Amsterdam UMC, Location VUMC, Amsterdam, The Netherlands.
³³ Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich, Switzerland.
³⁴ Zurich Center for Integrative Human Physiology, University of Zurich, Zurich, Switzerland.
³⁵ Neuroscience Centre Zurich, University and ETH Zurich, Zurich, Switzerland.
³⁶ Department of Psychiatry, Indiana University School of Medicine, Indianapolis, Indiana, USA.
³⁷ Centre for Healthy Brain Ageing, School of Psychiatry, University of New South Wales, Sydney, New South Wales, Australia.
³⁸ Dementia Centre for Research Collaboration, School of Psychiatry, University of New South Wales, Sydney, New South Wales, Australia.
³⁹ Department of Psychiatry, University Medical Center Utrecht Brain Center, Utrecht University, Utrecht, The Netherlands.
⁴⁰ Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, The Netherlands.
⁴¹ Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, The Netherlands.
⁴² Laboratory of Psychiatric Neuroimaging (LIM-21), Departamento e Instituto de Psiquiatria, Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil.
⁴³ Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State, Georgia Tech, Atlanta, Georgia, USA.
⁴⁴ MRC Centre for Neuropsychiatric Genetics and Genomics, Cardiff University, Cardiff, UK.
⁴⁵ Department of Child and Adolescent Psychiatry, NYU Grossman School of Medicine, New York, New York, USA.
⁴⁶ Nathan Kline Institute for Psychiatric Research, Orangeburg, New York, USA.
⁴⁷ Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
⁴⁸ Psychology Clinical Neuroscience Center, Department of Psychology, University of New Mexico, Albuquerque, New Mexico, USA.
⁴⁹ Mind Research Network, Albuquerque, New Mexico, USA.
⁵⁰ Department of Psychiatry, University of Montreal, Montreal, Canada.
⁵¹ Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University of Tübingen, Tübingen, Germany.
⁵² Department of Psychology (Clinical Psychology II), PFH - Private University of Applied Sciences, Göttingen, Germany.
⁵³ Groupe d'Imagerie Neurofonctionnelle, Institut des Maladies Neurodégénératives, Bordeaux, France.
⁵⁴ Centre for Youth Mental Health, University of Melbourne, Parkville, Victoria, Australia.
⁵⁵ Orygen, Parkville, Victoria, Australia.
⁵⁶ Campbell Family Mental Health Institute, Centre for Addiction and Mental Health, Department of Psychiatry, University of Toronto, Toronto, Canada.
⁵⁷ Department of Psychiatry, University of Toronto, Toronto, Ontario, Canada.
⁵⁸ Division of Psychological & Social Medicine and Developmental Neurosciences; Technische Universität Dresden, Faculty of Medicine, University Hospital C.G. Carus, Dresden, Germany.
⁵⁹ Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands.
⁶⁰ Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands.
⁶¹ Department of Psychiatry and Neuroscience Institute, University of Cape Town, Cape Town, Western Cape, South Africa.
⁶² Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands.
⁶³ Department of Psychiatry, Radboud University Medical Center, Nijmegen, The Netherlands.
⁶⁴ IRCCS Casa Sollievo della Sofferenza, San Giovanni Rotondo, Italy.
⁶⁵ Tommy Fuss Center for Neuropsychiatric Disease Research, Department of Psychiatry, Boston Children's Hospital and Harvard Medical School, Boston, Massachusetts, USA.
⁶⁶ Olin Center for Neuropsychiatric Research, Institute of Living, Hartford Hospital, Hartford, Connecticut, USA.
⁶⁷ Department of Psychology, Stanford University, Stanford, California, USA.
⁶⁸ Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany.
⁶⁹ German Center for Neurodegenerative Diseases (DZNE), Site Rostock/Greifswald, Greifswald, Germany.
⁷⁰ Section for Experimental Psychopathology and Neuroimaging, Department of General Psychiatry, Heidelberg University Hospital, Heidelberg, Germany.
⁷¹ Lifespan Brain Institute, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
⁷² Department of Early Psychosis, Amsterdam UMC, Amsterdam, The Netherlands.
⁷³ Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia.
⁷⁴ Interdisciplinary Center Psychopathology and Emotion regulation, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.
⁷⁵ Brain and Mind Centre, University of Sydney, Sydney, New South Wales, Australia.
⁷⁶ Department of Neurosciences, University of California San Diego, La Jolla, California, USA.
⁷⁷ Departments of Experimental and Clinical Psychology, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
⁷⁸ Department of Anatomy & Neurosciences, Amsterdam Neuroscience, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
⁷⁹ Department of Psychiatry, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.
⁸⁰ Department of Psychology, Yale University, New Haven, Connecticut, USA.
⁸¹ Department of Psychiatry, Massachusetts General Hospital, Boston, Massachusetts, USA.
⁸² Institute of Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany.
⁸³ Neuroscience Institute, University of Cape Town, Cape Town, Western Cape, South Africa.
⁸⁴ Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, Western Cape, South Africa.
⁸⁵ De Bascule, Academic center child and adolescent psychiatry, Duivendrecht, The Netherlands.
⁸⁶ Amsterdam UMC Department of Child and Adolescent Psychiatry, Amsterdam, The Netherlands.
⁸⁷ Department of Psychiatry, Warneford Hospital, Oxford, UK.
⁸⁸ Highfield Unit, Warneford Hospital, Oxford, UK.
⁸⁹ Department of Radiology, The Ohio State University College of Medicine, Columbus, Ohio, USA.
⁹⁰ Department of Psychology, University of Oslo, Oslo, Norway.
⁹¹ Sunnaas Rehabilitation Hospital HT, Nesodden, Norway.
⁹² Sunshine Coast Mind and Neuroscience Thompson Institute, Birtinya, Queensland, Australia.
⁹³ University of the Sunshine Coast, Sunshine Coast, Queensland, Australia.
⁹⁴ Department of Child and Adolescent Psychiatry and Psychology, Hospital Clínic, Barcelona, Spain.
⁹⁵ August Pi i Sunyer Biomedical Research Institut (IDIBAPS), Barcelona, Spain.
⁹⁶ Department of Medicine, University of Barcelona, Barcelona, Spain.
⁹⁷ Laboratory of Neuroimaging and Multimodal Analysis, Mental Health Research Center, Moscow, Russia.
⁹⁸ Department of Psychiatry, Harvard Medical School, Boston, Massachusetts, USA.
⁹⁹ SA MRC Unit on Risk and Resilience in Mental Disorders, Department of Psychiatry, Stellenbosch University, Cape Town, Western Cape, South Africa.
¹⁰⁰ Department of Psychiatry, Academic Medical Center, Amsterdam, The Netherlands.
¹⁰¹ Institut des maladies neurodégénératives, Université de Bordeaux, Bordeaux, France.
¹⁰² Genetic Epidemiology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
¹⁰³ Department of Psychiatry, Bellvitge University Hospital, Bellvitge Biomedical Research Institute-IDIBELL, Barcelona, Spain.
¹⁰⁴ Department of Clinical Sciences, University of Barcelona, Barcelona, Spain.
¹⁰⁵ University of Bordeaux, Bordeaux, France.
¹⁰⁶ Bordeaux University Hospital, Bordeaux, France.
¹⁰⁷ Department of Radiology and Imaging Sciences, Indiana University School of Medicine, Indianapolis, Indiana, USA.
¹⁰⁸ Division of Psychiatry, University of Edinburgh, Edinburgh, UK.
¹⁰⁹ Herston Imaging Research Facility and School of Clinical Sciences, Queensland University of Technology (QUT), Brisbane, Queensland, Australia.
¹¹⁰ Faculty of Health, Institute of Health and Biomedical Innovation, Queensland University of Technology (QUT), Brisbane, Queensland, Australia.
¹¹¹ School of Mental Health and Neuroscience, Faculty of Health, Medicine and Life Sciences, Maastricht University, Maastricht, The Netherlands.
¹¹² Department of Radiation Sciences, Umeå University, Umeå, Sweden.
¹¹³ Department of Integrative Medical Biology, Umeå University, Umeå, Sweden.
¹¹⁴ Emma Children's Hospital, Amsterdam UMC University of Amsterdam and Vrije Universiteit Amsterdam, Emma Neuroscience Group, Department of Pediatrics, Amsterdam Reproduction & Development, Amsterdam, The Netherlands.
¹¹⁵ Clinical Neuropsychology Section, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
¹¹⁶ Department of Psychology, University of Würzburg, Würzburg, Germany.
¹¹⁷ Centre of Mental Health, Medical Faculty, University of Würzburg, Würzburg, Germany.
¹¹⁸ Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, Mary Land, USA.
¹¹⁹ Department of Psychiatry, Institut d'Investigació Biomèdica Sant Pau, Barcelona, Spain.
¹²⁰ Early Psychosis: Interventions and Clinical-detection (EPIC) lab, Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹²¹ Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfur am Maint, Germany.
¹²² Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts, USA.
¹²³ Center for Depression, Anxiety, and Stress Research, McLean Hospital, Harvard Medical School, Belmont, Massachusetts, USA.
¹²⁴ Neuropsychiatric Institute, The Prince of Wales Hospital, Randwick, New South Wales, Australia.
¹²⁵ Indiana Alzheimer Disease Center, Indianapolis, Indiana, USA.
¹²⁶ West Region, Institute of Mental Health, Singapore, Singapore.
¹²⁷ Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
¹²⁸ Department of Neuroimaging, Institute of Psychiatry, Psychology and Neurology, King's College London, London, UK.
¹²⁹ Psychiatric and Neurodevelopmental Genetics Unit, Center for Genomic Medicine, Massachusetts General Hospital, Boston, Massachusetts, USA.
¹³⁰ Department of Biomedical Sciences of Cells and Systems, Rijksuniversiteit Groningen, University Medical Center Groningen, Groningen, The Netherlands.
¹³¹ Department of Psychobiology and Methodology in Health Sciences, Universitat Autònoma de Barcelona, Barcelona, Spain.
¹³² SAMRC Unit on Risk & Resilience in Mental Disorders, Dept of Psychiatry & Neuroscience Institute, University of Cape Town, Cape Town, Western Cape, South Africa.
¹³³ Queensland Brain Institute, University of Queensland, Brisbane, Queensland, Australia.
¹³⁴ Mental Illness Research, Education and Clinical Center (MIRECC), James J. Peters VA Medical Center, New York, New York, USA.
¹³⁵ Department of Child and Adolescent Psychiatry and Psychotherapy, Faculty of Medicine Carl Gustav Carus of TU Dresden, Dresden, Germany.
¹³⁶ Department of Psychiatry and Psychotherapy CCM, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
¹³⁷ Department of Psychiatry & Amsterdam Neuroscience, Amsterdam UMC, location VUMC, Amsterdam, The Netherlands.
¹³⁸ Institute for Community Medicine, University Medicine Greifswald, Greifswald, Germany.
¹³⁹ DZHK (German Centre for Cardiovascular Research), partner site Greifswald, Greifswald, Germany.
¹⁴⁰ DZD (German Center for Diabetes Research), partner site Greifswald, Greifswald, Germany.
¹⁴¹ Department of Radiology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.
¹⁴² Institute for Experimental Epileptology and Cognition Research, University Hospital Bonn, Bonn, Germany.
¹⁴³ Division of Psychiatry, Royal Edinburgh Hospital, Edinburgh, UK.
¹⁴⁴ Department of Neuroimaging, King's College London, London, UK.
¹⁴⁵ Centre for Advanced Imaging, University of Queensland, Brisbane, Queensland, Australia.
¹⁴⁶ Department of Child and Adolescent Psychiatry, NYU Child Study Center, Hassenfeld Children's Hospital at NYU Langone, New York, New York, USA.
¹⁴⁷ Instituto de Ensino e Pesquisa, Hospital Sírio-Libanês, São Paulo, Brazil.
¹⁴⁸ Division of Molecular Psychiatry, Center of Mental Health, University of Würzburg, Würzburg, Germany.
¹⁴⁹ Department of Psychology, Education and Child Studies (DPECS), Erasmus School of Social and Behavioral Sciences, Erasmus University Rotterdam, The Netherlands.
¹⁵⁰ Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada.
¹⁵¹ PROMENTA Research Center, Department of Psychology, University of Oslo, Oslo, Norway.

PMID: 33044802
PMCID: PMC8675415
DOI: 10.1002/hbm.25204

Meta-Analysis

Greater male than female variability in regional brain structure across the lifespan

Lara M Wierenga et al. Hum Brain Mapp. 2022 Jan.

. 2022 Jan;43(1):470-499.

doi: 10.1002/hbm.25204. Epub 2020 Oct 12.

Authors

Affiliations

¹ Institute of Psychology, Leiden University, Leiden, The Netherlands.
² Leiden Institute for Brain and Cognition, Leiden, The Netherlands.
³ Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, New York, USA.
⁴ Boys Town National Research Hospital, Omaha, Nebraska, USA.
⁵ Department of Psychology, School of Arts and Social Sciences, City, University of London, London, UK.
⁶ Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁷ Norwegian Centre for Mental Disorders Research (NORMENT), Division of Mental Health and Addiction, Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
⁸ Department of Psychiatric Research, Diakonhjemmet Hospital, Oslo, Norway.
⁹ Centre for Psychiatry Research, Department of Clinical Neuroscience, Karolinska Institutet, & Stockholm Health Care Services, Stockholm County Council, Stockholm, Sweden.
¹⁰ Department of Psychiatry, Amsterdam Neuroscience, Amsterdam UMC, Vrije Universiteit, Amsterdam, The Netherlands.
¹¹ Department of Research & Innovation, GGZ inGeest, Amsterdam, The Netherlands.
¹² Institute of Education and Child Studies, Forensic Family and Youth Care, Leiden University, Leiden, The Netherlands.
¹³ Centre for Neuroimaging & Cognitive Genomics (NICOG), Clinical Neuroimaging Laboratory, NCBES Galway Neuroscience Centre, College of Medicine Nursing and Health Sciences, National University of Ireland Galway, Galway, Ireland.
¹⁴ Institute of Medical Imaging & Visualisation, Faculty of Health & Social Sciences, Bournemouth University, Bournemouth, UK.
¹⁵ FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain.
¹⁶ Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Madrid, Spain.
¹⁷ Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
¹⁸ Norwegian Centre for Mental Disorders Research (NORMENT), Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.
¹⁹ Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
²⁰ Department of Psychiatry, Yale University, New Haven, Connecticut, USA.
²¹ Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
²² Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, University of Heidelberg, Medical Faculty Mannheim, Mannheim, Germany.
²³ Imaging Diagnostic Center, Hospital Clínic, Barcelona, Spain.
²⁴ Magnetic Resonance Image Core Facility, IDIBAPS, Barcelona, Spain.
²⁵ Department for Clinical Psychology, Würzburg University, Margetshöchheim, Germany.
²⁶ Department of Basic Medical Science, Neuroscience and Sense Organs, University of Bari Aldo Moro, Bari, Italy.
²⁷ Department of Biological Psychology, VU University Amsterdam, Amsterdam, The Netherlands.
²⁸ Department of Psychiatry, University of Basel, Basel, Switzerland.
²⁹ Department of Psychiatry, University of Lübeck, Lübeck, Germany.
³⁰ Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
³¹ CHU Sainte-Justine Research Center, Montreal, Quebec, Canada.
³² Alzheimer Center, Amsterdam UMC, Location VUMC, Amsterdam, The Netherlands.
³³ Department of Child and Adolescent Psychiatry and Psychotherapy, Psychiatric Hospital, University of Zurich, Zurich, Switzerland.
³⁴ Zurich Center for Integrative Human Physiology, University of Zurich, Zurich, Switzerland.
³⁵ Neuroscience Centre Zurich, University and ETH Zurich, Zurich, Switzerland.
³⁶ Department of Psychiatry, Indiana University School of Medicine, Indianapolis, Indiana, USA.
³⁷ Centre for Healthy Brain Ageing, School of Psychiatry, University of New South Wales, Sydney, New South Wales, Australia.
³⁸ Dementia Centre for Research Collaboration, School of Psychiatry, University of New South Wales, Sydney, New South Wales, Australia.
³⁹ Department of Psychiatry, University Medical Center Utrecht Brain Center, Utrecht University, Utrecht, The Netherlands.
⁴⁰ Department of Cognitive Neuroscience, Radboud University Medical Centre, Nijmegen, The Netherlands.
⁴¹ Karakter Child and Adolescent Psychiatry University Centre, Nijmegen, The Netherlands.
⁴² Laboratory of Psychiatric Neuroimaging (LIM-21), Departamento e Instituto de Psiquiatria, Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, Brazil.
⁴³ Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State, Georgia Tech, Atlanta, Georgia, USA.
⁴⁴ MRC Centre for Neuropsychiatric Genetics and Genomics, Cardiff University, Cardiff, UK.
⁴⁵ Department of Child and Adolescent Psychiatry, NYU Grossman School of Medicine, New York, New York, USA.
⁴⁶ Nathan Kline Institute for Psychiatric Research, Orangeburg, New York, USA.
⁴⁷ Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
⁴⁸ Psychology Clinical Neuroscience Center, Department of Psychology, University of New Mexico, Albuquerque, New Mexico, USA.
⁴⁹ Mind Research Network, Albuquerque, New Mexico, USA.
⁵⁰ Department of Psychiatry, University of Montreal, Montreal, Canada.
⁵¹ Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University of Tübingen, Tübingen, Germany.
⁵² Department of Psychology (Clinical Psychology II), PFH - Private University of Applied Sciences, Göttingen, Germany.
⁵³ Groupe d'Imagerie Neurofonctionnelle, Institut des Maladies Neurodégénératives, Bordeaux, France.
⁵⁴ Centre for Youth Mental Health, University of Melbourne, Parkville, Victoria, Australia.
⁵⁵ Orygen, Parkville, Victoria, Australia.
⁵⁶ Campbell Family Mental Health Institute, Centre for Addiction and Mental Health, Department of Psychiatry, University of Toronto, Toronto, Canada.
⁵⁷ Department of Psychiatry, University of Toronto, Toronto, Ontario, Canada.
⁵⁸ Division of Psychological & Social Medicine and Developmental Neurosciences; Technische Universität Dresden, Faculty of Medicine, University Hospital C.G. Carus, Dresden, Germany.
⁵⁹ Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands.
⁶⁰ Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands.
⁶¹ Department of Psychiatry and Neuroscience Institute, University of Cape Town, Cape Town, Western Cape, South Africa.
⁶² Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands.
⁶³ Department of Psychiatry, Radboud University Medical Center, Nijmegen, The Netherlands.
⁶⁴ IRCCS Casa Sollievo della Sofferenza, San Giovanni Rotondo, Italy.
⁶⁵ Tommy Fuss Center for Neuropsychiatric Disease Research, Department of Psychiatry, Boston Children's Hospital and Harvard Medical School, Boston, Massachusetts, USA.
⁶⁶ Olin Center for Neuropsychiatric Research, Institute of Living, Hartford Hospital, Hartford, Connecticut, USA.
⁶⁷ Department of Psychology, Stanford University, Stanford, California, USA.
⁶⁸ Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany.
⁶⁹ German Center for Neurodegenerative Diseases (DZNE), Site Rostock/Greifswald, Greifswald, Germany.
⁷⁰ Section for Experimental Psychopathology and Neuroimaging, Department of General Psychiatry, Heidelberg University Hospital, Heidelberg, Germany.
⁷¹ Lifespan Brain Institute, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
⁷² Department of Early Psychosis, Amsterdam UMC, Amsterdam, The Netherlands.
⁷³ Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia.
⁷⁴ Interdisciplinary Center Psychopathology and Emotion regulation, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.
⁷⁵ Brain and Mind Centre, University of Sydney, Sydney, New South Wales, Australia.
⁷⁶ Department of Neurosciences, University of California San Diego, La Jolla, California, USA.
⁷⁷ Departments of Experimental and Clinical Psychology, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
⁷⁸ Department of Anatomy & Neurosciences, Amsterdam Neuroscience, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
⁷⁹ Department of Psychiatry, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.
⁸⁰ Department of Psychology, Yale University, New Haven, Connecticut, USA.
⁸¹ Department of Psychiatry, Massachusetts General Hospital, Boston, Massachusetts, USA.
⁸² Institute of Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany.
⁸³ Neuroscience Institute, University of Cape Town, Cape Town, Western Cape, South Africa.
⁸⁴ Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, Western Cape, South Africa.
⁸⁵ De Bascule, Academic center child and adolescent psychiatry, Duivendrecht, The Netherlands.
⁸⁶ Amsterdam UMC Department of Child and Adolescent Psychiatry, Amsterdam, The Netherlands.
⁸⁷ Department of Psychiatry, Warneford Hospital, Oxford, UK.
⁸⁸ Highfield Unit, Warneford Hospital, Oxford, UK.
⁸⁹ Department of Radiology, The Ohio State University College of Medicine, Columbus, Ohio, USA.
⁹⁰ Department of Psychology, University of Oslo, Oslo, Norway.
⁹¹ Sunnaas Rehabilitation Hospital HT, Nesodden, Norway.
⁹² Sunshine Coast Mind and Neuroscience Thompson Institute, Birtinya, Queensland, Australia.
⁹³ University of the Sunshine Coast, Sunshine Coast, Queensland, Australia.
⁹⁴ Department of Child and Adolescent Psychiatry and Psychology, Hospital Clínic, Barcelona, Spain.
⁹⁵ August Pi i Sunyer Biomedical Research Institut (IDIBAPS), Barcelona, Spain.
⁹⁶ Department of Medicine, University of Barcelona, Barcelona, Spain.
⁹⁷ Laboratory of Neuroimaging and Multimodal Analysis, Mental Health Research Center, Moscow, Russia.
⁹⁸ Department of Psychiatry, Harvard Medical School, Boston, Massachusetts, USA.
⁹⁹ SA MRC Unit on Risk and Resilience in Mental Disorders, Department of Psychiatry, Stellenbosch University, Cape Town, Western Cape, South Africa.
¹⁰⁰ Department of Psychiatry, Academic Medical Center, Amsterdam, The Netherlands.
¹⁰¹ Institut des maladies neurodégénératives, Université de Bordeaux, Bordeaux, France.
¹⁰² Genetic Epidemiology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
¹⁰³ Department of Psychiatry, Bellvitge University Hospital, Bellvitge Biomedical Research Institute-IDIBELL, Barcelona, Spain.
¹⁰⁴ Department of Clinical Sciences, University of Barcelona, Barcelona, Spain.
¹⁰⁵ University of Bordeaux, Bordeaux, France.
¹⁰⁶ Bordeaux University Hospital, Bordeaux, France.
¹⁰⁷ Department of Radiology and Imaging Sciences, Indiana University School of Medicine, Indianapolis, Indiana, USA.
¹⁰⁸ Division of Psychiatry, University of Edinburgh, Edinburgh, UK.
¹⁰⁹ Herston Imaging Research Facility and School of Clinical Sciences, Queensland University of Technology (QUT), Brisbane, Queensland, Australia.
¹¹⁰ Faculty of Health, Institute of Health and Biomedical Innovation, Queensland University of Technology (QUT), Brisbane, Queensland, Australia.
¹¹¹ School of Mental Health and Neuroscience, Faculty of Health, Medicine and Life Sciences, Maastricht University, Maastricht, The Netherlands.
¹¹² Department of Radiation Sciences, Umeå University, Umeå, Sweden.
¹¹³ Department of Integrative Medical Biology, Umeå University, Umeå, Sweden.
¹¹⁴ Emma Children's Hospital, Amsterdam UMC University of Amsterdam and Vrije Universiteit Amsterdam, Emma Neuroscience Group, Department of Pediatrics, Amsterdam Reproduction & Development, Amsterdam, The Netherlands.
¹¹⁵ Clinical Neuropsychology Section, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
¹¹⁶ Department of Psychology, University of Würzburg, Würzburg, Germany.
¹¹⁷ Centre of Mental Health, Medical Faculty, University of Würzburg, Würzburg, Germany.
¹¹⁸ Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, Mary Land, USA.
¹¹⁹ Department of Psychiatry, Institut d'Investigació Biomèdica Sant Pau, Barcelona, Spain.
¹²⁰ Early Psychosis: Interventions and Clinical-detection (EPIC) lab, Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹²¹ Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfur am Maint, Germany.
¹²² Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, Massachusetts, USA.
¹²³ Center for Depression, Anxiety, and Stress Research, McLean Hospital, Harvard Medical School, Belmont, Massachusetts, USA.
¹²⁴ Neuropsychiatric Institute, The Prince of Wales Hospital, Randwick, New South Wales, Australia.
¹²⁵ Indiana Alzheimer Disease Center, Indianapolis, Indiana, USA.
¹²⁶ West Region, Institute of Mental Health, Singapore, Singapore.
¹²⁷ Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
¹²⁸ Department of Neuroimaging, Institute of Psychiatry, Psychology and Neurology, King's College London, London, UK.
¹²⁹ Psychiatric and Neurodevelopmental Genetics Unit, Center for Genomic Medicine, Massachusetts General Hospital, Boston, Massachusetts, USA.
¹³⁰ Department of Biomedical Sciences of Cells and Systems, Rijksuniversiteit Groningen, University Medical Center Groningen, Groningen, The Netherlands.
¹³¹ Department of Psychobiology and Methodology in Health Sciences, Universitat Autònoma de Barcelona, Barcelona, Spain.
¹³² SAMRC Unit on Risk & Resilience in Mental Disorders, Dept of Psychiatry & Neuroscience Institute, University of Cape Town, Cape Town, Western Cape, South Africa.
¹³³ Queensland Brain Institute, University of Queensland, Brisbane, Queensland, Australia.
¹³⁴ Mental Illness Research, Education and Clinical Center (MIRECC), James J. Peters VA Medical Center, New York, New York, USA.
¹³⁵ Department of Child and Adolescent Psychiatry and Psychotherapy, Faculty of Medicine Carl Gustav Carus of TU Dresden, Dresden, Germany.
¹³⁶ Department of Psychiatry and Psychotherapy CCM, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.
¹³⁷ Department of Psychiatry & Amsterdam Neuroscience, Amsterdam UMC, location VUMC, Amsterdam, The Netherlands.
¹³⁸ Institute for Community Medicine, University Medicine Greifswald, Greifswald, Germany.
¹³⁹ DZHK (German Centre for Cardiovascular Research), partner site Greifswald, Greifswald, Germany.
¹⁴⁰ DZD (German Center for Diabetes Research), partner site Greifswald, Greifswald, Germany.
¹⁴¹ Department of Radiology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.
¹⁴² Institute for Experimental Epileptology and Cognition Research, University Hospital Bonn, Bonn, Germany.
¹⁴³ Division of Psychiatry, Royal Edinburgh Hospital, Edinburgh, UK.
¹⁴⁴ Department of Neuroimaging, King's College London, London, UK.
¹⁴⁵ Centre for Advanced Imaging, University of Queensland, Brisbane, Queensland, Australia.
¹⁴⁶ Department of Child and Adolescent Psychiatry, NYU Child Study Center, Hassenfeld Children's Hospital at NYU Langone, New York, New York, USA.
¹⁴⁷ Instituto de Ensino e Pesquisa, Hospital Sírio-Libanês, São Paulo, Brazil.
¹⁴⁸ Division of Molecular Psychiatry, Center of Mental Health, University of Würzburg, Würzburg, Germany.
¹⁴⁹ Department of Psychology, Education and Child Studies (DPECS), Erasmus School of Social and Behavioral Sciences, Erasmus University Rotterdam, The Netherlands.
¹⁵⁰ Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada.
¹⁵¹ PROMENTA Research Center, Department of Psychology, University of Oslo, Oslo, Norway.

PMID: 33044802
PMCID: PMC8675415
DOI: 10.1002/hbm.25204

Abstract

For many traits, males show greater variability than females, with possible implications for understanding sex differences in health and disease. Here, the ENIGMA (Enhancing Neuro Imaging Genetics through Meta-Analysis) Consortium presents the largest-ever mega-analysis of sex differences in variability of brain structure, based on international data spanning nine decades of life. Subcortical volumes, cortical surface area and cortical thickness were assessed in MRI data of 16,683 healthy individuals 1-90 years old (47% females). We observed significant patterns of greater male than female between-subject variance for all subcortical volumetric measures, all cortical surface area measures, and 60% of cortical thickness measures. This pattern was stable across the lifespan for 50% of the subcortical structures, 70% of the regional area measures, and nearly all regions for thickness. Our findings that these sex differences are present in childhood implicate early life genetic or gene-environment interaction mechanisms. The findings highlight the importance of individual differences within the sexes, that may underpin sex-specific vulnerability to disorders.

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Conflict of interest statement

The authors declare the following competing interests: OAA: Speaker's honorarium from Lundbeck, Consultant of HealthLyti; PA: Received payments for consultancy to Shire/Takeda, Medic, educational/research awards from Shire/Takeda, GW Pharma, Janssen‐Cila, speaker at sponsored events for Shire, Flynn Pharma, Medic; TB: advisory or consultancy role for Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, Shire, and Infectopharm, conference support or speaker's fee by Lilly, Medice, and Shire, received royalities from Hogrefe, Kohlhammer, CIP Medien, Oxford University Press ‐ the present work is unrelated to the above grants and relationship; DB: serves as an unpaid scientific consultant for an EU‐funded neurofeedback trial that is unrelated to the present work; HB: Advisory Board, Nutricia Australi; CRKC: received partial research support from Biogen, Inc. (Boston, USA) for work unrelated to the topic of this manuscript; BF: received educational speaking fees from Medice; HJG: received travel grants and speakers honoraria from Fresenius Medical Care, Neuraxpharm, Servier and Janssen Cilag as well as research funding from Fresenius Medical Care; NJ and PMT: MPI of a research related grant from Biogen, Inc., for research unrelated to the contents of this manuscript; JK: given talks at educational events sponsored by Medic; all funds are received by King's College London and used for studies of ADHD; DM‐C: receives fees from UpToDate, Inc and Elsevier, all unrelated to the current work; AMM: received research support from Eli Lilly, Janssen, and the Sackler Foundation, and speaker fees from Illumina and Janssen; DJS: received research grants and/or honoraria from Lundbeck and Sun. The remaining authors declare no competing interests.

Figures

**FIGURE 1**
Sex differences in volumetric measures of subcortical volumes (left), cortical surface area (center), and cortical thickness (right). Shown are effect sizes (Cohen's d‐value) of FDR corrected mean sex differences. Greater mean values for males are displayed in blue, greater mean values for females are displayed in red. Darker colors indicate larger effect sizes

**FIGURE 2**
Sex differences in variance ratio for subcortical volumes (Left), cortical surface area (center), and cortical thickness (right). Shown are log transformed variance ratios, where significant larger variance ratio for males than females is displayed in blue ranging from 0 to 1. Darker colors indicate a larger variance ratio

**FIGURE 3**
Jittered marginal distribution scatterplots are displayed together with their shift function for the top three variance ratio effects of subcortical volumes (top), cortical surface area (middle) and cortical thickness (right). The central, darkest line on each distribution is the median, note that main sex effects are removed. The other lines mark the deciles of each distribution. The shift values are included, which refer to the number of units that the male (upper) distribution would have to be shifted to match the female (lower) distribution. Confidence intervals are included for each of these shift values

**FIGURE 4**
Regions where sex differences in variability of brain structure interacted with age displayed for subcortical volumes (left), cortical surface area (center), and cortical thickness (right)

**FIGURE 5**
Sex differences in variability interacted with age in 50% of the subcortical volumes, 30% of the surface area measures, and only one thickness measure. Three representative results are shown: right thalamus volume (top left), surface area of the right parahippocampal gyrus (top right) and thickness of the left insula (bottom center). Absolute residual values are modeled across the age range. Effects showed larger male than female variance in the younger age group, this effect attenuated with increasing age

**FIGURE 6**
(a–c) Stronger anatomical correlations for males than females are indicated in blue (larger homogeneity in males than females), while stronger correlations for females are displayed in red (larger homogeneity in females than males). The bottom left half shows the significant variance ratio's only, using two sided permutation testing. Results are displayed for subcortical volumes (a), surface area (b), and cortical thickness (c). Cortical regions are ordered by lobe and hemisphere (left frontal, left occipital, left parietal, left temporal, right frontal, right occipital, right parietal, right temporal)

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Greater male than female variability in regional brain structure across the lifespan

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Greater male than female variability in regional brain structure across the lifespan

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