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History of suicide attempts associated with the thinning right superior temporal gyrus among individuals with schizophrenia

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Abstract

Individuals with schizophrenia have higher rates of suicide attempts than the general population. Specific cortical abnormalities (e.g., the cortical surface area and thickness) may be associated with a history of suicide attempts. We recruited 74 individuals with schizophrenia (37 suicide attempters were individually matched with 37 non-attempters on age, sex, phase of illness, and study center) and 37 healthy volunteers. The cortical surface area and thickness data were extracted from structural MRI and compared between the groups. Suicide attempters showed significantly smaller surface areas in the whole brain (p = .028, Cohen’s d = -0.54) than non-attempters. No association was found between the cortical surface area of individual brain regions and a history of suicide attempts. The mean cortical thickness did not differ significantly between the groups; however, suicide attempters demonstrated a thinner cortex in the right superior temporal gyrus (p < .001, q = 0.037, Cohen’s d = -0.88). These findings indicate that a history of suicide attempts among individuals with schizophrenia is associated with a reduction in the global cortical surface area and specific cortical thinning of the right superior temporal gyrus. The morphometric alteration of the right superior temporal gyrus may represent a biomarker of suicidal behavior in individuals with schizophrenia.

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References

  • Addington, D., Addington, J., & Maticka-Tyndale, E. (1993). Assessing depression in schizophrenia: The Calgary Depression Scale. British Journal of Psychiatry, Suppl(22), 39–44.

  • Aguilar, E. J., Garcia-Marti, G., Marti-Bonmati, L., Lull, J. J., Moratal, D., Escarti, M. J., . . . Sanjuan, J. (2008). Left orbitofrontal and superior temporal gyrus structural changes associated to suicidal behavior in patients with schizophrenia. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 32(7), 1673-1676https://doi.org/10.1016/j.pnpbp.2008.06.016

  • American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders: DSM-IV. American Psychiatric Association.

    Google Scholar 

  • Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B(Methodological), 57(1), 289–300. doi:https://doi.org/10.1111/j.2517-6161.1995.tb02031.x

  • Besteher, B., Wagner, G., Koch, K., Schachtzabel, C., Reichenbach, J. R., Schlosser, R., . . . Schultz, C. C. (2016). Pronounced prefronto-temporal cortical thinning in schizophrenia: Neuroanatomical correlate of suicidal behavior? Schizophrenia Research, 176(2-3), 151-157https://doi.org/10.1016/j.schres.2016.08.010

  • Campos, A. I., Thompson, P. M., Veltman, D. J., Pozzi, E., van Veltzen, L. S., Jahanshad, N., . . . Rentería, M. E. (2021). Brain correlates of suicide attempt in 18,925 participants across 18 international cohorts. Biological Psychiatry, 90(4), 243-252https://doi.org/10.1016/j.biopsych.2021.03.015

  • Chen, X., Liang, S., Pu, W., Song, Y., Mwansisya, T. E., Yang, Q., . . . Xue, Z. (2015). Reduced cortical thickness in right heschl's gyrus associated with auditory verbal hallucinations severity in first-episode schizophrenia. BMC Psychiatry, 15, 152https://doi.org/10.1186/s12888-015-0546-2

  • Clapham et al., 2019 Clapham, E., Boden, R., Brandt, L., Jonsson, E. G., Bahmanyar, S., Ekbom, A., . . . Reutfors, J. (2019). Suicide ideation and behavior as risk factors for subsequent suicide in schizophrenia: A nested case-control study. Suicide and Life-Threatening Behavior, 49(4), 996-1005https://doi.org/10.1111/sltb.12499

  • Coalson, T. S., Van Essen, D. C., & Glasser, M. F. (2018). The impact of traditional neuroimaging methods on the spatial localization of cortical areas. Proceedings of the National Academy of Sciences of the United States of America, 115(27), E6356–E6365. https://doi.org/10.1073/pnas.1801582115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon, M. L., Thiruchselvam, R., Todd, R., & Christoff, K. (2017). Emotion and the prefrontal cortex: An integrative review. Psychological Bulletin, 143(10), 1033–1081. https://doi.org/10.1037/bul0000096

    Article  PubMed  Google Scholar 

  • Fischl, B. (2012). FreeSurfer. Neuroimage 62, 774–781.

  • Fradkin, Y., Khadka, S., Bessette, K. L., & Stevens, M. C. (2017). The relationship of impulsivity and cortical thickness in depressed and non-depressed adolescents. Brain Imaging and Behavior, 11(5), 1515–1525. https://doi.org/10.1007/s11682-016-9612-8

    Article  PubMed  Google Scholar 

  • Giakoumatos, C. I., Tandon, N., Shah, J., Mathew, I. T., Brady, R. O., Clementz, B. A., . . . Keshavan, M. S. (2013). Are structural brain abnormalities associated with suicidal behavior in patients with psychotic disorders? Journal of Psychiatric Research, 47(10), 1389-1395https://doi.org/10.1016/j.jpsychires.2013.06.011

  • Grasby, K. L., Jahanshad, N., Painter, J. N., Colodro-Conde, L., Bralten, J., Hibar, D. P., . . . Medland, S. E. (2020). The genetic architecture of the human cerebral cortex. Science, 367(6484), eaay6690. doi:https://doi.org/10.1126/science.aay6690

  • Hibar, D. P., Westlye, L. T., Doan, N. T., Jahanshad, N., Cheung, J. W., Ching, C. R. K., . . . Andreassen, O. A. (2018). Cortical abnormalities in bipolar disorder: An MRI analysis of 6503 individuals from the ENIGMA bipolar disorder working group. Molecular Psychiatry, 23(4), 932-942https://doi.org/10.1038/mp.2017.73

  • Hjorthøj, C. D., Stürup, A. E. M. D., McGrath, J. J. P., & Nordentoft, M. P. (2017). Years of potential life lost and life expectancy in schizophrenia: A systematic review and meta-analysis. Lancet Psychiatry, 4(4), 295–301. https://doi.org/10.1016/S2215-0366(17)30078-0

    Article  PubMed  Google Scholar 

  • Hu, S., Ide, J. S., Zhang, S., & Li, C. R. (2016). The right superior frontal gyrus and individual variation in proactive control of impulsive response. Journal of Neuroscience, 36(50), 12688–12696. https://doi.org/10.1523/JNEUROSCI.1175-16.2016

    Article  CAS  PubMed  Google Scholar 

  • Hu, S., Ide, J. S., Zhang, S., & Li, C. S. (2015). Anticipating conflict: Neural correlates of a Bayesian belief and its motor consequence. NeuroImage, 119, 286–295. https://doi.org/10.1016/j.neuroimage.2015.06.032

    Article  PubMed  Google Scholar 

  • Kang, S., Cho, S., Na, K., Lee, J. S., Joo, S. W., Cho, S., . . . Lee, Y. J. (2020). Differences in brain surface area and cortical volume between suicide attempters and non-attempters with major depressive disorder. Psychiatry Research: Neuroimaging, 297https://doi.org/10.1016/j.pscychresns.2020.111032

  • Kay, S. R., Fiszbein, A., & Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13(2), 261–276. https://doi.org/10.1093/schbul/13.2.261

    Article  CAS  PubMed  Google Scholar 

  • Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31(3), 968-980https://doi.org/10.1016/j.neuroimage.2006.01.021

  • Liu, H., Zhang, H., Xiao, W., Liu, Q., Fu, P., Chen, J., . . . Li, L. (2009). Scales for evaluating depressive symptoms in Chinese patients with schizophrenia. Journal of Nervous and Mental Disease, 197(2), 140-142https://doi.org/10.1097/NMD.0b013e31819636a5

  • Lu, L., Dong, M., Zhang, L., Zhu, X. M., Ungvari, G. S., Ng, C. H., . . . Xiang, Y. T. (2019). Prevalence of suicide attempts in individuals with schizophrenia: A meta-analysis of observational studies. Epidemiology and Psychiatric Sciences, 29, e39https://doi.org/10.1017/S2045796019000313

  • Manza, P., Hu, S., Chao, H. H., Zhang, S., Leung, H. C., & Li, C. R. (2016). A dual but asymmetric role of the dorsal anterior cingulate cortex in response inhibition and switching from a non-salient to salient action. NeuroImage, 134, 466–474. https://doi.org/10.1016/j.neuroimage.2016.04.055

    Article  PubMed  Google Scholar 

  • McLellan, Q., Wilkes, T. C., Swansburg, R., Jaworska, N., Langevin, L. M., & MacMaster, F. P. (2018). History of suicide attempt and right superior temporal gyrus volume in youth with treatment-resistant major depressive disorder. Journal of Affective Disorders, 239, 291–294. https://doi.org/10.1016/j.jad.2018.07.030

    Article  PubMed  Google Scholar 

  • Minzenberg, M. J., Lesh, T., Niendam, T., Yoon, J. H., Cheng, Y., Rhoades, R., & Carter, C. S. (2015a). Conflict-related anterior cingulate functional connectivity is associated with past suicidal ideation and behavior in recent-onset schizophrenia. Journal of Psychiatric Research, 65, 95–101. https://doi.org/10.1016/j.jpsychires.2015.04.002

    Article  PubMed  Google Scholar 

  • Minzenberg, M. J., Lesh, T., Niendam, T., Yoon, J. H., Cheng, Y. A., Rhoades, R. N., & Carter, C. S. (2015b). Frontal motor cortex activity during reactive control is associated with past suicidal behavior in recent-onset schizophrenia. Crisis-the Journal of Crisis Intervention and Suicide Prevention, 36(5), 363–370. https://doi.org/10.1027/0227-5910/a000335

    Article  Google Scholar 

  • Minzenberg, M. J., Lesh, T. A., Niendam, T. A., Yoon, J. H., Rhoades, R. N., & Carter, C. S. (2014). Frontal cortex control dysfunction related to long-term suicide risk in recent-onset schizophrenia. Schizophrenia Research, 157(1–3), 19–25. https://doi.org/10.1016/j.schres.2014.05.039

    Article  PubMed  Google Scholar 

  • Olfson, M., Gerhard, T., Huang, C., Crystal, S., & Stroup, T. S. (2015). Premature mortality among adults with schizophrenia in the United States. JAMA Psychiatry, 72(12), 1172–1181. https://doi.org/10.1001/jamapsychiatry.2015.1737

    Article  PubMed  Google Scholar 

  • Olfson, M., Stroup, T. S., Huang, C., Wall, M. M., Crystal, S., & Gerhard, T. (2021). Suicide risk in medicare patients with schizophrenia across the life span. JAMA Psychiatry. https://doi.org/10.1001/jamapsychiatry.2021.0841

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan, L. A., Ramos, L., Segreti, A., Brent, D. A., & Phillips, M. L. (2015). Right superior temporal gyrus volume in adolescents with a history of suicide attempt. British Journal of Psychiatry, 206(4), 339–340. https://doi.org/10.1192/bjp.bp.114.151316

    Article  Google Scholar 

  • Price, C. J. (2012). A review and synthesis of the first 20 years of pet and fMRI studies of heard speech, spoken language and reading. NeuroImage, 62(2), 816–847. https://doi.org/10.1016/j.neuroimage.2012.04.062

    Article  PubMed  Google Scholar 

  • Rusch, N., Spoletini, I., Wilke, M., Martinotti, G., Bria, P., Trequattrini, A., . . . Spalletta, G. (2008). Inferior frontal white matter volume and suicidality in schizophrenia. Psychiatry Research, 164(3), 206-214https://doi.org/10.1016/j.pscychresns.2007.12.011

  • Schmaal, L., Hibar, D. P., Samann, P. G., Hall, G. B., Baune, B. T., Jahanshad, N., . . . Veltman, D. J. (2017). Cortical abnormalities in adults and adolescents with major depression based on brain scans from 20 cohorts worldwide in the ENIGMA major depressive disorder working group. Molecular Psychiatry, 22(6), 900-909https://doi.org/10.1038/mp.2016.60

  • Schmaal, L., van Harmelen, A. L., Chatzi, V., Lippard, E. T. C., Toenders, Y. J., Averill, L. A., . . . Blumberg, H. P. (2020). Imaging suicidal thoughts and behaviors: A comprehensive review of 2 decades of neuroimaging studies. Molecular Psychiatry, 25(2), 408-427https://doi.org/10.1038/s41380-019-0587-x

  • Sliwinska, M. W., & Pitcher, D. (2018). TMS demonstrates that both right and left superior temporal sulci are important for facial expression recognition. NeuroImage, 183, 394–400. https://doi.org/10.1016/j.neuroimage.2018.08.025

    Article  PubMed  Google Scholar 

  • Soloff, P. H., Pruitt, P., Sharma, M., Radwan, J., White, R., & Diwadkar, V. A. (2012). Structural brain abnormalities and suicidal behavior in borderline personality disorder. Journal of Psychiatric Research, 46(4), 516–525. https://doi.org/10.1016/j.jpsychires.2012.01.003

    Article  PubMed  PubMed Central  Google Scholar 

  • StataCorp. (2017). Stata statistical software: Release 15. StataCorp LLC. www.stata.com

  • Sudol, K., & Mann, J. J. (2017). Biomarkers of suicide attempt behavior: Towards a biological model of risk. Current Psychiatry Reports, 19(6), 31. https://doi.org/10.1007/s11920-017-0781-y

    Article  PubMed  Google Scholar 

  • Tanskanen, A., Tiihonen, J., & Taipale, H. (2018). Mortality in schizophrenia: 30-year nationwide follow-up study. Acta Psychiatrica Scandinavica, 138(6), 492–499. https://doi.org/10.1111/acps.12913

    Article  CAS  PubMed  Google Scholar 

  • The Math Works, Inc. (2019). MATLAB. Version 2019b. The Math Works, Inc. https://ww2.mathworks.cn/

  • van Erp, T. G. M., Walton, E., Hibar, D. P., Schmaal, L., Jiang, W., Glahn, D. C., . . . Turner, J. A. (2018). Cortical brain abnormalities in 4474 individuals with schizophrenia and 5098 control subjects via the enhancing neuro imaging genetics through meta analysis (ENIGMA) consortium. Biological Psychiatry, 84(9), 644-654https://doi.org/10.1016/j.biopsych.2018.04.023

  • van Tol, M. J., van der Meer, L., Bruggeman, R., Modinos, G., Knegtering, H., & Aleman, A. (2014). Voxel-based gray and white matter morphometry correlates of hallucinations in schizophrenia: The superior temporal gyrus does not stand alone. Neuroimage: Clinical, 4, 249–257. doi:https://doi.org/10.1016/j.nicl.2013.12.008

  • Walton, E., Hibar, D. P., van Erp, T. G., Potkin, S. G., Roiz-Santianez, R., Crespo-Facorro, B., . . . Ehrlich, S. (2017). Positive symptoms associate with cortical thinning in the superior temporal gyrus via the ENIGMA schizophrenia consortium. Acta Psychiatrica Scandinavica, 135(5), 439-447https://doi.org/10.1111/acps.12718

  • Wang, W., Hu, S., Ide, J. S., Zhornitsky, S., Zhang, S., Yu, A. J., & Li, C. R. (2018). Motor preparation disrupts proactive control in the stop signal task. Frontiers in Human Neuroscience, 12, 151. https://doi.org/10.3389/fnhum.2018.00151

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, W., Zhornitsky, S., Chao, H. H., Levy, I., Joormann, J., & Li, C. R. (2020). The effects of age on cerebral responses to self-initiated actions during social interactions: An exploratory study. Behavioural Brain Research, 378, 112301. https://doi.org/10.1016/j.bbr.2019.112301

    Article  PubMed  Google Scholar 

  • Wang, W., Zhornitsky, S., Li, C. S., Zhang, S., Ide, J. S., Joormann, J., & Li, C. R. (2019). Cerebral responses to self-initiated action during social interactions. Cognitive, Affective & Behavioral Neuroscience, 19(6), 1521–1535. https://doi.org/10.3758/s13415-019-00711-5

    Article  CAS  Google Scholar 

  • Winkler, A. M., Greve, D. N., Bjuland, K. J., Nichols, T. E., Sabuncu, M. R., Haberg, A. K., . . . Rimol, L. M. (2018). Joint analysis of cortical area and thickness as a replacement for the analysis of the volume of the cerebral cortex. Cerebral Cortex, 28(2), 738-749https://doi.org/10.1093/cercor/bhx308

  • Yi, H. G., Leonard, M. K., & Chang, E. F. (2019). The encoding of speech sounds in the superior temporal gyrus. Neuron, 102(6), 1096–1110. https://doi.org/10.1016/j.neuron.2019.04.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Contributions

Author contributions included conception and study design (Y. Tan and L.E. Hong), data collection or acquisition (J. Tong, J. Huang, and S. Chen), statistical analysis (Y. Yin, F. Fan), interpretation of results (Y. Yin, Y. Tan), drafting the manuscript work (Y. Yin, Y. Tan), revising it critically for important intellectual content (B. Tian, S. Tan, Z. Wang, F. Yang, Y. Tong, P. Kochunov, N. Jahanshad, C. R. Li, and L. E. Hong) and approval of final version to be published and agreement to be accountable for the integrity and accuracy of all aspects of the work (All authors).

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Correspondence to Yunlong Tan.

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This work was supported by the National Natural Science Foundation of China (Y. Tan, 81761128021, 81771452), Beijing Natural Science Foundation (Y. Tan, 7151005), the National Institutes of Health (L. E. Hong, R01MH112180). Funders have no roles in data analysis, interpretation of the findings, or decision to publish the findings.

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008. The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional guides on the care and use of laboratory animals.

Conflict of interest

Dr. Hong has received or is planning to receive research funding or consulting fees from Mitsubishi, Your Energy Systems LLC, Neuralstem, Taisho, Heptares, Pfizer, Sound Pharma, Luye Pharma, Takeda, and Regeneron. None was involved in the design, analysis, or outcomes of the study. Other authors declare that the research was conducted without any relationships that could be interpreted as a potential conflict of interest or financial conflict.

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Yin, Y., Tong, J., Huang, J. et al. History of suicide attempts associated with the thinning right superior temporal gyrus among individuals with schizophrenia. Brain Imaging and Behavior 16, 1893–1901 (2022). https://doi.org/10.1007/s11682-021-00624-3

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