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

Molecular Psychiatry volume 28, pages 4853–4866 (2023)Cite this article

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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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Fig. 1: Schematic summary of the study design.
Fig. 2: Two significant three-way covariation models.
Fig. 3: The contribution of brain imaging phenotypes to each model.
Fig. 4: The main contributors of each model.
Fig. 5: Mediation and moderated mediation analyses for significant models.

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Code availability

Structural MRI data for VBM and SBM analyses were preprocessed separately by CAT12 (version r1364, http://dbm.neuro.uni-jena.de/cat) and FreeSurfer (version 6.0.0) (http://surfer.nmr.mgh.harvard.edu/), respectively. DTI data were preprocessed by FSL 5.0.10 (https://fsl.fmrib.ox.ac.uk/fsl/fslwiki/). rs-fMRI data were preprocessed by SPM12 (https://www.fil.ion.ucl.ac.uk/spm/software/spm12/) and Data Processing Assistant for Resting-State fMRI (http://rfmri.org/dpabi). Brain imaging phenotypes visualisation was done using MRIcroGL (https://www.nitrc.org/projects/mricrogl/) and ggseg package in R (https://github.com/ggseg/ggseg). The codes for smCCA are available on the bnaras GitHub (https://github.com/bnaras/PMA). The codes for FastICA are available at https://www.fmrib.ox.ac.uk/ukbiobank/nnpaper/ukb_NN.m.

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Acknowledgements

This work was funded by Natural Science Foundation of China (82030053), Tianjin Key Medical Discipline (Specialty) Construction Project (TJYXZDXK-001A) and Tsinghua-Toyota Joint Research Fund. No other disclosures were reported.

Author information

Author notes

  1. These authors contributed equally: Kaizhong Xue, Bo Gao, Feng Chen.

Authors and Affiliations

  1. Department of Radiology and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, Tianjin, 300052, China

    Kaizhong Xue, Wen Qin, Feng Liu, Lining Guo, Qiang Xu, Jiayuan Xu, Jilian Fu & Chunshui Yu

  2. Department of Radiology, The Affiliated Hospital of Guizhou Medical University, Guiyang, 550004, China

    Bo Gao

  3. Department of Radiology, Yantai Yuhuangding Hospital, Yantai, 264000, China

    Bo Gao

  4. Department of Radiology, Hainan General Hospital (Hainan Affiliated Hospital of Hainan Medical University), Haikou, 570311, China

    Feng Chen

  5. Department of Radiology, Henan Provincial People’s Hospital & Zhengzhou University People’s Hospital, Zhengzhou, 450003, China

    Meiyun Wang & Dapeng Shi

  6. Department of Magnetic Resonance Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, China

    Jingliang Cheng & Caihong Wang

  7. Department of Radiology, Drum Tower Hospital, Medical School of Nanjing University, Nanjing, 210008, China

    Bing Zhang

  8. Department of Radiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China

    Wenzhen Zhu

  9. Department of Medical Imaging, The First Affiliated Hospital of Guangzhou University of Traditional Chinese Medicine, Guangzhou, 510405, China

    Shijun Qiu

  10. Department of Medical Imaging, The Second Hospital of Hebei Medical University, Shijiazhuang, 050000, China

    Zuojun Geng

  11. Division of Life Science and Medicine, University of Science & Technology of China, Hefei, 230027, China

    Xiaochu Zhang

  12. Functional and Molecular Imaging Key Lab of Shaanxi Province & Department of Radiology, Tangdu Hospital, Air Force Medical University, Xi’an, 710038, China

    Guangbin Cui

  13. Department of Radiology, The First Affiliated Hospital of Anhui Medical University, Hefei, 230022, China

    Yongqiang Yu

  14. Department of Radiology, Characteristic Medical Center of Chinese People’s Armed Police Force, Tianjin, 300162, China

    Quan Zhang

  15. Department of Radiology, Xiangya Hospital, Central South University, Changsha, 410008, China

    Weihua Liao

  16. Molecular Imaging Research Center of Central South University, Changsha, 410008, China

    Weihua Liao

  17. National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, 410008, China

    Weihua Liao

  18. Department of Radiology, The First Hospital of Shanxi Medical University, Taiyuan, 030001, China

    Hui Zhang

  19. Department of Radiology, The Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, 310009, China

    Xiaojun Xu

  20. Department of Radiology, Tianjin Huanhu Hospital, Tianjin, 300350, China

    Tong Han

  21. School of Medical Imaging and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University, Tianjin, 300203, China

    Meng Liang

  22. Department of Radiology, Tianjin Medical University Cancer Institute and Hospital, Tianjin, 300060, China

    Peng Zhang, Wei Li & Zhaoxiang Ye

  23. Department of Radiology, the Center for Medical Imaging, West China Hospital of Sichuan University, Chengdu, 610041, China

    Su Lui

  24. Department of Radiology, The Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, 325027, China

    Zhihan Yan

  25. Department of Magnetic Resonance, Lanzhou University Second Hospital, Lanzhou, 730030, China

    Jing Zhang

  26. Gansu Province Clinical Research Center for Functional and Molecular Imaging, Lanzhou, 730030, China

    Jing Zhang

  27. Department of Radiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, 325000, China

    Jiance Li

  28. Department of Radiology, Qilu Hospital of Shandong University, Jinan, 250012, China

    Dawei Wang

  29. Department of Radiology, Beijing Tongren Hospital, Capital Medical University, Beijing, 100730, China

    Junfang Xian

  30. Department of Radiology, The Affiliated Hospital of Xuzhou Medical University, Xuzhou, 221006, China

    Kai Xu

  31. IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China

    Xi-Nian Zuo

  32. Institute of Psychology, Chinese Academy of Sciences, Beijing, 100101, China

    Xi-Nian Zuo

  33. Department of Medical Imaging, Jinling Hospital, Medical School of Nanjing University, Nanjing, 210002, China

    Longjiang Zhang

  34. Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, 68159, Mannheim, Germany

    Tobias Banaschewski, Frauke Nees & Nathalie Holz

  35. Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom

    Gareth J. Barker

  36. Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland

    Arun L. W. Bokde

  37. Centre for Population Neuroscience and Precision Medicine (PONS), Institute of Psychiatry, Psychology & Neuroscience, SGDP Centre, King’s College London, London, United Kingdom

    Sylvane Desrivières

  38. Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Square J5, Mannheim, Germany

    Herta Flor & Frauke Nees

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

    Herta Flor

  40. NeuroSpin, CEA, Université Paris-Saclay, F-91191, Gif-sur-Yvette, France

    Antoine Grigis, Dimitri Papadopoulos Orfanos & Herve Lemaitre

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

    Hugh Garavan

  42. Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom

    Penny Gowland

  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

    Andreas Heinz & Henrik Walter

  44. Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Germany

    Rüdiger Brühl

  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

    Jean-Luc Martinot, Marie-Laure Paillère Martinot & Eric Artiges

  46. AP-HP. Sorbonne University, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France

    Marie-Laure Paillère Martinot

  47. Psychiatry Department, EPS Barthélémy Durand, Etampes, France

    Eric Artiges

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

    Frauke Nees

  49. Institut des Maladies Neurodégénératives, UMR 5293, CNRS, CEA, Université de Bordeaux, 33076, Bordeaux, France

    Herve Lemaitre

  50. Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str. 5, 37075, Göttingen, Germany

    Luise Poustka

  51. Department of Child and Adolescent Psychiatry, Psychotherapy and Psychosomatics, University Medical Center Hamburg-Eppendorf, Hamburg, Germany

    Sarah Hohmann

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

    Juliane H. Fröhner & Michael N. Smolka

  53. Centre for Population Neuroscience and Stratified Medicine (PONS), Department of Psychiatry and Neuroscience, Charité Universitätsmedizin Berlin, Berlin, Germany

    Nilakshi Vaidya

  54. School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland

    Robert Whelan

  55. Department of Radiology, Tianjin First Center Hospital, Tianjin, 300192, China

    Wen Shen

  56. Department of Radiology, The First Affiliated Hospital of Dalian Medical University, Dalian, 116011, China

    Yanwei Miao

  57. CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, 200031, China

    Chunshui Yu

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  1. Kaizhong Xue
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  2. Bo Gao
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  3. Feng Chen
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  4. Meiyun Wang
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  5. Jingliang Cheng
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  6. Bing Zhang
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  15. Hui Zhang
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  16. Xiaojun Xu
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  17. Tong Han
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  18. Wen Qin
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  19. Feng Liu
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Consortia

IMAGEN Consortium

  • Tobias Banaschewski
  • , Gareth J. Barker
  • , Arun L. W. Bokde
  • , Sylvane Desrivières
  • , Herta Flor
  • , Antoine Grigis
  • , Hugh Garavan
  • , Penny Gowland
  • , Andreas Heinz
  • , Rüdiger Brühl
  • , Jean-Luc Martinot
  • , Marie-Laure Paillère Martinot
  • , Eric Artiges
  • , Frauke Nees
  • , Dimitri Papadopoulos Orfanos
  • , Herve Lemaitre
  • , Luise Poustka
  • , Sarah Hohmann
  • , Nathalie Holz
  • , Juliane H. Fröhner
  • , Michael N. Smolka
  • , Nilakshi Vaidya
  • , Henrik Walter
  •  & Robert Whelan

CHIMGEN Consortium

  • Kaizhong Xue
  • , Bo Gao
  • , Feng Chen
  • , Meiyun Wang
  • , Jingliang Cheng
  • , Bing Zhang
  • , Wenzhen Zhu
  • , Shijun Qiu
  • , Zuojun Geng
  • , Xiaochu Zhang
  • , Guangbin Cui
  • , Yongqiang Yu
  • , Quan Zhang
  • , Weihua Liao
  • , Hui Zhang
  • , Xiaojun Xu
  • , Tong Han
  • , Wen Qin
  • , Feng Liu
  • , Meng Liang
  • , Lining Guo
  • , Qiang Xu
  • , Jiayuan Xu
  • , Jilian Fu
  • , Peng Zhang
  • , Wei Li
  • , Dapeng Shi
  • , Caihong Wang
  • , Su Lui
  • , Zhihan Yan
  • , Jing Zhang
  • , Jiance Li
  • , Dawei Wang
  • , Junfang Xian
  • , Kai Xu
  • , Xi-Nian Zuo
  • , Longjiang Zhang
  • , Zhaoxiang Ye
  • , Wen Shen
  • , Yanwei Miao
  •  & Chunshui Yu

Contributions

KX, WS, YM, and CY conceptualised the study. KX conducted the analysis, and wrote the first version of the manuscript. BG, FC helped analyse data and revise the manuscript. MW, JC, BZ, WZ, SQ, XZ, ZG, GC, YY, WL, HZ, XX, TH, WQ, FL, ML, LG, QX, JX, JF, PZ, WL, DS, CW, ZY, JZ, JL, DW, JX, KX, X-NZ, LZ, ZY, WS, YM, and CY collected imaging data. TB, GJB, ALWB, SD, HF, AG, HG, PG, AH, RB, J-LM, M-LPM, EA, FN, DPO, HL, LP, SH, NH, JHF, MNS, NV, HW and RW acquired the data. WS, YM, and CY provided critical comments on the manuscript and approved the final version of the manuscript. All authors contributed to the manuscript. The authors read and approved the final manuscript.

Corresponding authors

Correspondence to Wen Shen, Yanwei Miao or Chunshui Yu.

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Xue, K., Gao, B., Chen, F. et al. Covariation of preadult environmental exposures, adult brain imaging phenotypes, and adult personality traits. Mol Psychiatry 28, 4853–4866 (2023). https://doi.org/10.1038/s41380-023-02261-2

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  • DOI: https://doi.org/10.1038/s41380-023-02261-2

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