The Human Brain Is Best Described as Being on a Female/Male Continuum: Evidence from a Neuroimaging Connectivity Study

Author:

Zhang Yi123,Luo Qiang24,Huang Chu-Chung5,Lo Chun-Yi Zac2,Langley Christelle36,Desrivières Sylvane7,Quinlan Erin Burke7,Banaschewski Tobias8,Millenet Sabina8,Bokde Arun L W9,Flor Herta1011,Garavan Hugh12,Gowland Penny13,Heinz Andreas14,Ittermann Bernd15,Martinot Jean-Luc1617,Artiges Eric1617,Paillère-Martinot Marie-Laure1618,Nees Frauke91019,Orfanos Dimitri Papadopoulos20,Poustka Luise2122,Fröhner Juliane H23,Smolka Michael N24,Walter Henrik14,Whelan Robert23,Tsai Shih-Jen2425,Lin Ching-Po226,Bullmore Ed3627,Schumann Gunter2829,Sahakian Barbara J236,Feng Jianfeng123031,

Affiliation:

1. Shanghai Centre for Mathematical Sciences, Fudan University, Shanghai, 200433, China

2. Institute of Science and Technology for Brain-Inspired Intelligence, Ministry of Education-Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence and Research and Research Institute of Intelligent Complex Systems, Fudan University, Shanghai, 200433, China

3. Department of Psychiatry, University of Cambridge, Cambridge, CB2 0SZ, UK

4. State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Institutes of Brain Science and National Clinical Research Center for Aging and Medicine, Huashan Hospital, Fudan University, Shanghai, 200433, China

5. Institute of Cognitive Neuroscience, School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China

6. Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, CB2 3EB, UK

7. Medical Research Council-Social, Genetic, and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology, and Neuroscience, King's College London, London, SE5 8AF, UK

8. Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, 69117, Germany

9. Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, D02 PN40, Ireland

10. Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Manheim, 69117, Germany

11. Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, 68131, Germany

12. Departments of Psychiatry and Psychology, University of Vermont, Burlington, VT 05405, USA

13. Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, NG7 2RD, UK

14. Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin, Berlin, 10117, Germany

15. Physikalisch-Technische Bundesanstalt (PTB), Abbestraße 2, 10587 Berlin, Germany

16. Institut National de la Santé et de la Recherche Médicale, INSERM U1299 ``Developmental trajectories & psychiatry''; Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli; 91190 Gif-sur-Yvette, France

17. Etablissement Public de Santé (EPS) Barthélemy Durand, 91700 Sainte-Geneviève-des-Bois, France

18. Assistance Publique—Hêpitaux de Paris, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, 75006, France

19. Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, 24118, Germany

20. Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Center Göttingen, Göttingen, 37075, Germany

21. Clinic for Child and Adolescent Psychiatry, Medical University of Vienna, Vienna, 1090 Wien, Austria

22. Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, 01087, Germany

23. School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, D02 PN40, Ireland

24. Department of Psychiatry, Taipei Veterans General Hospital, Taipei, 11217, Taiwan

25. School of Medicine, National Yang-Ming University, Taipei, 11221, Taiwan

26. Institute of Neuroscience, National Yang-Ming University, Taipei, 11221, Taiwan

27. Cambridgeshire and Peterborough National Health Service (NHS) Foundation Trust, Huntingdon, CB21 5EF, UK

28. PONS Research Group, Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charitéplatz 1, Berlin, 10117, Germany

29. PONS Centre, Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, 200433, China

30. Department of Computer Science, University of Warwick, Coventry, CV4 7AL, UK

31. Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, 200433, China

Abstract

Abstract Psychological androgyny has long been associated with greater cognitive flexibility, adaptive behavior, and better mental health, but whether a similar concept can be defined using neural features remains unknown. Using the neuroimaging data from 9620 participants, we found that global functional connectivity was stronger in the male brain before middle age but became weaker after that, when compared with the female brain, after systematic testing of potentially confounding effects. We defined a brain gender continuum by estimating the likelihood of an observed functional connectivity matrix to represent a male brain. We found that participants mapped at the center of this continuum had fewer internalizing symptoms compared with those at the 2 extreme ends. These findings suggest a novel hypothesis proposing that there exists a neuroimaging concept of androgyny using the brain gender continuum, which may be associated with better mental health in a similar way to psychological androgyny.

Funder

NIH

Science Foundation Ireland

Paris Sud University IDEX 2012

Assistance Publique Hôpitaux de Paris and INSERM

Mission Interministérielle de Lutte Contre les Drogues et les Conduites Addictives

Fondation de France, the Fondation pour la Recherche Médicale

Agence Nationale de la Recherche

Deutsche Forschungsgemeinschaft

Bundesministerium für Bildung und Forschung

National Institute for Health Research

Medical Research Council

Swedish Research Council Formas

Medical Research Council Grant

Innovative Medicine Initiative Project EU-AIMS

MATRICS

FP7 projects IMAGEMEND

BRIDGET

ERANID

Horizon 2020

European Union

Wallitt Foundation and Eton College

Zhangjiang Lab

Shanghai Municipal Science and Technology Major Project

Shanghai Science and Technology Innovation Plan

Taipei Veterans General Hospital

Taiwan National Science Council

National Natural Science Foundation of China

National Key Research and Development Program of China

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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