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Brain structural and functional signatures of multi-generational family history of suicidal behaviors in preadolescent children

Molecular Psychiatry (2023)Cite this article

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Abstract

Parent-child transmission of suicidal behaviors has been extensively studied, but the investigation of a three-generation family suicide risk paradigm remains limited. In this study, we aimed to explore the behavioral and brain signatures of multi-generational family history of suicidal behaviors (FHoS) in preadolescents, utilizing a longitudinal design and the dataset from Adolescent Brain and Cognitive DevelopmentSM Study (ABCD Study®), which comprised 4 years of data and includes a total of 9,653 preadolescents. Our findings revealed that multi-generational FHoS was significantly associated with an increased risk of problematic behaviors and suicidal behaviors (suicide ideation and suicide attempt) in offspring. Interestingly, the problematic behaviors were further identified as a mediator in the multi-generational transmission of suicidal behaviors. Additionally, we observed alterations in brain structure within superior temporal gyrus (STG), precentral/postcentral cortex, posterior parietal cortex (PPC), cingulate cortex (CC), and planum temporale (PT), as well as disrupted functional connectivity of default mode network (DMN), ventral attention network (VAN), dorsal attention network (DAN), fronto-parietal network (FPN), and cingulo-opercular network (CON) among preadolescents with FHoS. These results provide compelling longitudinal evidence at the population level, highlighting the associations between multi-generational FHoS and maladaptive behavioral and neurodevelopmental outcomes in offspring. These findings underscore the need for early preventive measures aimed at mitigating the familial transmission of suicide risk and reducing the global burden of deaths among children and adolescents.

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Fig. 1: Trends of problematic behaviors in preadolescent children grouped by family history of suicidal behaviors.
Fig. 2: Trends of suicidal behaviors in preadolescent children grouped by family history of suicidal behaviors.
Fig. 3: Role of problematic behaviors in explaining the multi-generational transmission of suicidal behaviors.
Fig. 4: Representative regions with significantly different volumes in preadolescent children grouped by family history of suicidal behaviors.
Fig. 5: Representative brain networks with significantly different functional connectivities in preadolescent children grouped by family history of suicidal behaviors.

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Data availability

Data is from the Adolescent Brain and Cognitive DevelopmentSM Study (ABCD Study®). Access to ABCD study data is restricted to protect participants’ privacy. Users must create an account through the National Institute of Mental Health (NIMH) Data Archive and they may then complete the necessary steps to gain access (https://data-archive.nimh.nih.gov/abcd). Processed data from this study (including the MRI and rsfMRI) have been uploaded to the NIMH Data Archive (NDA). Information on how to access ABCD data through the NDA is available on the ABCD study data sharing webpage: https://abcdstudy.org/scientists_data_sharing.html. The ABCD data used in this report came from ABCD release 4.0 (https://doi.org/10.15154/1523041). All variables included in the current study are listed and described in Supplementary Table S1.

Code availability

Scripts that support the findings of this study are available from the corresponding author upon reasonable request (E-mail: runsenchen@tsinghua.edu.cn).

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Acknowledgements

D.Q. was supported by the Shuimu Tsinghua Scholar Program of Tsinghua University. We thank the Adolescent Brain Cognitive Development (ABCD) participants and their families for their time and dedication to this project. Data used in the preparation of this article were obtained from the ABCD Study (https://abcdstudy.org) and are held in the NIMH Data Archive (NDA). This is a multisite, longitudinal study designed to recruit more than 10,000 children aged 9–10 and follow them over 10 years into early adulthood. The ABCD Study is supported by the National Institutes of Health (NIH)and additional federal partners under award numbers U01DA0401048, U01DA050989, U01DA051016, U01DA041022, U01DA051018, U01DA051037, U01DA050987, U01DA041174, U01DA041106, U01DA041117, U01DA041028, U01DA041134, U01DA050988, U01DA051039, U01DA041156, U01DA041025, U01DA041120, U01DA051038, U01DA041148, U01DA041093, U01DA041089, U24DA041123, U24DA041147. A full list of supporters is available at https://abcdstudy.org/federal-partners.html. A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/principal-investigators/. ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in the analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators. The ABCD repository grows and changes over time. The ABCD data used in this report came from ABCD release 4.0 (https://doi.org/10.15154/1523041). DOIs can be found at nda.nih.gov.

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  1. These authors contributed equally: Xue Wen, Diyang Qu.

Authors and Affiliations

  1. Vanke School of Public Health, Tsinghua University, Beijing, China

    Xue Wen, Diyang Qu, Dongyu Liu & Runsen Chen

  2. Institute for Healthy China, Tsinghua University, Beijing, China

    Xue Wen, Diyang Qu, Dongyu Liu & Runsen Chen

  3. Chinese Institute for Brain Research, Beijing, China

    Yinuo Shu, Shaoling Zhao, Guowei Wu & Zaixu Cui

  4. Key Laboratory of Brain, Cognition and Education Sciences; School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, China

    Yuanyuan Wang

  5. Wulituo Hospital of Shijingshan District, Beijing, China

    Xiaoqian Zhang

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Contributions

XW formulated the research questions, analyzed the data, interpreted the data, made the tables and figures, wrote the first draft of the manuscript, and revised the manuscript. DQ assisted in formulating the research questions, double-checking the data analyses, interpreting the data, writing the first draft of the manuscript, and revising the manuscript. RC assisted in formulating the research questions, interpreting data, supervision, and revising the manuscript critically. ZC, XZ, and YW assisted in formulating the research questions, interpreting data, and revising the manuscript critically. DL, SZ, and YS assisted in double-checking the data analyses. DL and GW assisted in revising the manuscript. All the authors contributed feedback and approved the final manuscript.

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Correspondence to Zaixu Cui, Xiaoqian Zhang or Runsen Chen.

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Wen, X., Qu, D., Liu, D. et al. Brain structural and functional signatures of multi-generational family history of suicidal behaviors in preadolescent children. Mol Psychiatry (2023). https://doi.org/10.1038/s41380-023-02342-2

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