Covariation of preadult environmental exposures, adult brain imaging phenotypes, and adult personality traits

Kaizhong Xue^#¹, Bo Gao^#^{2

3}, Feng Chen^#⁴, Meiyun Wang⁵, Jingliang Cheng⁶, Bing Zhang⁷, Wenzhen Zhu⁸, Shijun Qiu⁹, Zuojun Geng¹⁰, Xiaochu Zhang¹¹, Guangbin Cui¹², Yongqiang Yu¹³, Quan Zhang¹⁴, Weihua Liao^{15

16

17}, Hui Zhang¹⁸, Xiaojun Xu¹⁹, Tong Han²⁰, Wen Qin¹, Feng Liu¹, Meng Liang²¹, Lining Guo¹, Qiang Xu¹, Jiayuan Xu¹, Jilian Fu¹, Peng Zhang²², Wei Li²², Dapeng Shi⁵, Caihong Wang⁶, Su Lui²³, Zhihan Yan²⁴, Jing Zhang^{25

26}, Jiance Li²⁷, Dawei Wang²⁸, Junfang Xian²⁹, Kai Xu³⁰, Xi-Nian Zuo^{31

32}, Longjiang Zhang³³, Zhaoxiang Ye²², Tobias Banaschewski³⁴, Gareth J Barker³⁵, Arun L W Bokde³⁶, Sylvane Desrivières³⁷, Herta Flor^{38

39}, Antoine Grigis⁴⁰, Hugh Garavan⁴¹, Penny Gowland⁴², Andreas Heinz⁴³, Rüdiger Brühl⁴⁴, Jean-Luc Martinot⁴⁵, Marie-Laure Paillère Martinot^{45

46}, Eric Artiges^{45

47}, Frauke Nees^{34

38

48}, Dimitri Papadopoulos Orfanos⁴⁰, Herve Lemaitre^{40

49}, Luise Poustka⁵⁰, Sarah Hohmann⁵¹, Nathalie Holz³⁴, Juliane H Fröhner⁵², Michael N Smolka⁵², Nilakshi Vaidya⁵³, Henrik Walter⁴³, Robert Whelan⁵⁴, Wen Shen⁵⁵, Yanwei Miao⁵⁶, Chunshui Yu^{57

58}; IMAGEN Consortium; CHIMGEN Consortium

Affiliations

¹ Department of Radiology and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, Tianjin, 300052, China.
² Department of Radiology, The Affiliated Hospital of Guizhou Medical University, Guiyang, 550004, China.
³ Department of Radiology, Yantai Yuhuangding Hospital, Yantai, 264000, China.
⁴ Department of Radiology, Hainan General Hospital (Hainan Affiliated Hospital of Hainan Medical University), Haikou, 570311, China.
⁵ Department of Radiology, Henan Provincial People's Hospital & Zhengzhou University People's Hospital, Zhengzhou, 450003, China.
⁶ Department of Magnetic Resonance Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, China.
⁷ Department of Radiology, Drum Tower Hospital, Medical School of Nanjing University, Nanjing, 210008, China.
⁸ Department of Radiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China.
⁹ Department of Medical Imaging, The First Affiliated Hospital of Guangzhou University of Traditional Chinese Medicine, Guangzhou, 510405, China.
¹⁰ Department of Medical Imaging, The Second Hospital of Hebei Medical University, Shijiazhuang, 050000, China.
¹¹ Division of Life Science and Medicine, University of Science & Technology of China, Hefei, 230027, China.
¹² Functional and Molecular Imaging Key Lab of Shaanxi Province & Department of Radiology, Tangdu Hospital, Air Force Medical University, Xi'an, 710038, China.
¹³ Department of Radiology, The First Affiliated Hospital of Anhui Medical University, Hefei, 230022, China.
¹⁴ Department of Radiology, Characteristic Medical Center of Chinese People's Armed Police Force, Tianjin, 300162, China.
¹⁵ Department of Radiology, Xiangya Hospital, Central South University, Changsha, 410008, China.
¹⁶ Molecular Imaging Research Center of Central South University, Changsha, 410008, China.
¹⁷ National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, 410008, China.
¹⁸ Department of Radiology, The First Hospital of Shanxi Medical University, Taiyuan, 030001, China.
¹⁹ Department of Radiology, The Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, 310009, China.
²⁰ Department of Radiology, Tianjin Huanhu Hospital, Tianjin, 300350, China.
²¹ School of Medical Imaging and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University, Tianjin, 300203, China.
²² Department of Radiology, Tianjin Medical University Cancer Institute and Hospital, Tianjin, 300060, China.
²³ Department of Radiology, the Center for Medical Imaging, West China Hospital of Sichuan University, Chengdu, 610041, China.
²⁴ Department of Radiology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, 325027, China.
²⁵ Department of Magnetic Resonance, Lanzhou University Second Hospital, Lanzhou, 730030, China.
²⁶ Gansu Province Clinical Research Center for Functional and Molecular Imaging, Lanzhou, 730030, China.
²⁷ Department of Radiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, 325000, China.
²⁸ Department of Radiology, Qilu Hospital of Shandong University, Jinan, 250012, China.
²⁹ Department of Radiology, Beijing Tongren Hospital, Capital Medical University, Beijing, 100730, China.
³⁰ Department of Radiology, The Affiliated Hospital of Xuzhou Medical University, Xuzhou, 221006, China.
³¹ IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China.
³² Institute of Psychology, Chinese Academy of Sciences, Beijing, 100101, China.
³³ Department of Medical Imaging, Jinling Hospital, Medical School of Nanjing University, Nanjing, 210002, China.
³⁴ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159, Mannheim, Germany.
³⁵ Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, United Kingdom.
³⁶ Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
³⁷ Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King's College London, London, United Kingdom.
³⁸ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany.
³⁹ Department of Psychology, School of Social Sciences, University of Mannheim, 68131, Mannheim, Germany.
⁴⁰ NeuroSpin, CEA, Université Paris-Saclay, F-91191, Gif-sur-Yvette, France.
⁴¹ Departments of Psychiatry and Psychology, University of Vermont, Burlington, VT, 05405, USA.
⁴² Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom.
⁴³ 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.
⁴⁴ Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Germany.
⁴⁵ Institut National de la Santé et de la Recherche Médicale, INSERM U 1299 "Trajectoires développementales & psychiatrie", University Paris-Saclay, CNRS; Ecole Normale Supérieure Paris-Saclay, Centre Borelli, Gif-sur-Yvette, France.
⁴⁶ AP-HP. Sorbonne University, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France.
⁴⁷ Psychiatry Department, EPS Barthélémy Durand, Etampes, France.
⁴⁸ Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, Germany.
⁴⁹ Institut des Maladies Neurodégénératives, UMR 5293, CNRS, CEA, Université de Bordeaux, 33076, Bordeaux, France.
⁵⁰ Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, 37075, Göttingen, Germany.
⁵¹ Department of Child and Adolescent Psychiatry, Psychotherapy and Psychosomatics, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁵² Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
⁵³ Centre for Population Neuroscience and Stratified Medicine (PONS), Department of Psychiatry and Neuroscience, Charité Universitätsmedizin Berlin, Berlin, Germany.
⁵⁴ School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland.
⁵⁵ Department of Radiology, Tianjin First Center Hospital, Tianjin, 300192, China. shenwen66happy@163.com.
⁵⁶ Department of Radiology, The First Affiliated Hospital of Dalian Medical University, Dalian, 116011, China. ywmiao716@163.com.
⁵⁷ Department of Radiology and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, Tianjin, 300052, China. chunshuiyu@tmu.edu.cn.
⁵⁸ CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, 200031, China. chunshuiyu@tmu.edu.cn.

^# Contributed equally.

PMID: 37737484
DOI: 10.1038/s41380-023-02261-2

Covariation of preadult environmental exposures, adult brain imaging phenotypes, and adult personality traits

Kaizhong Xue et al. Mol Psychiatry. 2023 Nov.

. 2023 Nov;28(11):4853-4866.

doi: 10.1038/s41380-023-02261-2. Epub 2023 Sep 22.

Authors

Affiliations

¹ Department of Radiology and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, Tianjin, 300052, China.
² Department of Radiology, The Affiliated Hospital of Guizhou Medical University, Guiyang, 550004, China.
³ Department of Radiology, Yantai Yuhuangding Hospital, Yantai, 264000, China.
⁴ Department of Radiology, Hainan General Hospital (Hainan Affiliated Hospital of Hainan Medical University), Haikou, 570311, China.
⁵ Department of Radiology, Henan Provincial People's Hospital & Zhengzhou University People's Hospital, Zhengzhou, 450003, China.
⁶ Department of Magnetic Resonance Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, China.
⁷ Department of Radiology, Drum Tower Hospital, Medical School of Nanjing University, Nanjing, 210008, China.
⁸ Department of Radiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China.
⁹ Department of Medical Imaging, The First Affiliated Hospital of Guangzhou University of Traditional Chinese Medicine, Guangzhou, 510405, China.
¹⁰ Department of Medical Imaging, The Second Hospital of Hebei Medical University, Shijiazhuang, 050000, China.
¹¹ Division of Life Science and Medicine, University of Science & Technology of China, Hefei, 230027, China.
¹² Functional and Molecular Imaging Key Lab of Shaanxi Province & Department of Radiology, Tangdu Hospital, Air Force Medical University, Xi'an, 710038, China.
¹³ Department of Radiology, The First Affiliated Hospital of Anhui Medical University, Hefei, 230022, China.
¹⁴ Department of Radiology, Characteristic Medical Center of Chinese People's Armed Police Force, Tianjin, 300162, China.
¹⁵ Department of Radiology, Xiangya Hospital, Central South University, Changsha, 410008, China.
¹⁶ Molecular Imaging Research Center of Central South University, Changsha, 410008, China.
¹⁷ National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, 410008, China.
¹⁸ Department of Radiology, The First Hospital of Shanxi Medical University, Taiyuan, 030001, China.
¹⁹ Department of Radiology, The Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, 310009, China.
²⁰ Department of Radiology, Tianjin Huanhu Hospital, Tianjin, 300350, China.
²¹ School of Medical Imaging and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University, Tianjin, 300203, China.
²² Department of Radiology, Tianjin Medical University Cancer Institute and Hospital, Tianjin, 300060, China.
²³ Department of Radiology, the Center for Medical Imaging, West China Hospital of Sichuan University, Chengdu, 610041, China.
²⁴ Department of Radiology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou, 325027, China.
²⁵ Department of Magnetic Resonance, Lanzhou University Second Hospital, Lanzhou, 730030, China.
²⁶ Gansu Province Clinical Research Center for Functional and Molecular Imaging, Lanzhou, 730030, China.
²⁷ Department of Radiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, 325000, China.
²⁸ Department of Radiology, Qilu Hospital of Shandong University, Jinan, 250012, China.
²⁹ Department of Radiology, Beijing Tongren Hospital, Capital Medical University, Beijing, 100730, China.
³⁰ Department of Radiology, The Affiliated Hospital of Xuzhou Medical University, Xuzhou, 221006, China.
³¹ IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China.
³² Institute of Psychology, Chinese Academy of Sciences, Beijing, 100101, China.
³³ Department of Medical Imaging, Jinling Hospital, Medical School of Nanjing University, Nanjing, 210002, China.
³⁴ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159, Mannheim, Germany.
³⁵ Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, United Kingdom.
³⁶ Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
³⁷ Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King's College London, London, United Kingdom.
³⁸ Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany.
³⁹ Department of Psychology, School of Social Sciences, University of Mannheim, 68131, Mannheim, Germany.
⁴⁰ NeuroSpin, CEA, Université Paris-Saclay, F-91191, Gif-sur-Yvette, France.
⁴¹ Departments of Psychiatry and Psychology, University of Vermont, Burlington, VT, 05405, USA.
⁴² Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom.
⁴³ 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.
⁴⁴ Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Germany.
⁴⁵ Institut National de la Santé et de la Recherche Médicale, INSERM U 1299 "Trajectoires développementales & psychiatrie", University Paris-Saclay, CNRS; Ecole Normale Supérieure Paris-Saclay, Centre Borelli, Gif-sur-Yvette, France.
⁴⁶ AP-HP. Sorbonne University, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France.
⁴⁷ Psychiatry Department, EPS Barthélémy Durand, Etampes, France.
⁴⁸ Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig Holstein, Kiel University, Kiel, Germany.
⁴⁹ Institut des Maladies Neurodégénératives, UMR 5293, CNRS, CEA, Université de Bordeaux, 33076, Bordeaux, France.
⁵⁰ Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, 37075, Göttingen, Germany.
⁵¹ Department of Child and Adolescent Psychiatry, Psychotherapy and Psychosomatics, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁵² Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
⁵³ Centre for Population Neuroscience and Stratified Medicine (PONS), Department of Psychiatry and Neuroscience, Charité Universitätsmedizin Berlin, Berlin, Germany.
⁵⁴ School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland.
⁵⁵ Department of Radiology, Tianjin First Center Hospital, Tianjin, 300192, China. shenwen66happy@163.com.
⁵⁶ Department of Radiology, The First Affiliated Hospital of Dalian Medical University, Dalian, 116011, China. ywmiao716@163.com.
⁵⁷ Department of Radiology and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, Tianjin, 300052, China. chunshuiyu@tmu.edu.cn.
⁵⁸ CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, 200031, China. chunshuiyu@tmu.edu.cn.

^# Contributed equally.

PMID: 37737484
DOI: 10.1038/s41380-023-02261-2

Abstract

Exposure to preadult environmental exposures may have long-lasting effects on mental health by affecting the maturation of the brain and personality, two traits that interact throughout the developmental process. However, environment-brain-personality covariation patterns and their mediation relationships remain unclear. In 4297 healthy participants (aged 18-30 years), we combined sparse multiple canonical correlation analysis with independent component analysis to identify the three-way covariation patterns of 59 preadult environmental exposures, 760 adult brain imaging phenotypes, and five personality traits, and found two robust environment-brain-personality covariation models with sex specificity. One model linked greater stress and less support to weaker functional connectivity and activity in the default mode network, stronger activity in subcortical nuclei, greater thickness and volume in the occipital, parietal and temporal cortices, and lower agreeableness, consciousness and extraversion as well as higher neuroticism. The other model linked higher urbanicity and better socioeconomic status to stronger functional connectivity and activity in the sensorimotor network, smaller volume and surface area and weaker functional connectivity and activity in the medial prefrontal cortex, lower white matter integrity, and higher openness to experience. We also conducted mediation analyses to explore the potential bidirectional mediation relationships between adult brain imaging phenotypes and personality traits with the influence of preadult environmental exposures and found both environment-brain-personality and environment-personality-brain pathways. We finally performed moderated mediation analyses to test the potential interactions between macro- and microenvironmental exposures and found that one category of exposure moderated the mediation pathways of another category of exposure. These results improve our understanding of the effects of preadult environmental exposures on the adult brain and personality traits and may facilitate the design of targeted interventions to improve mental health by reducing the impact of adverse environmental exposures.

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Covariation of preadult environmental exposures, adult brain imaging phenotypes, and adult personality traits

Affiliations

Covariation of preadult environmental exposures, adult brain imaging phenotypes, and adult personality traits

Authors

Affiliations

Abstract

References

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources