Abstract
Previous task-fMRI studies have reported the abnormal brain activations in major depressive disorders (MDD) with suicidal behavior. However, there is no consensus of opinion on task-fMRI imaging findings of the suicidal brain. We performed a meta-analysis to integrate the results of reported studies to find the consistent task-related alteration pattern of brain activations in MDD patients with suicidal behavior, aiming to investigate brain functional alterations in association with a vulnerability to suicidal behavior. Using the SDM (Seed-based d Mapping) method, we conducted a meta-analysis of the task-fMRI studies to compare the brain activations between major depressive disorder (MDD) patients with a history of suicidal behavior (suicide attempter, ATT) and the MDD patients without suicidal behavior (non-attempters, NAT) during tasks. Our systematic search identified 7 task-fMRI studies comprising 366 individuals, i.e., 150 ATT and 216 NAT. We found that brain activation in ATT increased in the left insula, while decreased in the bilateral fusiform gyrus compared to NAT during the fMRI tasks. We found the brain activation changes in the insula and fusiform gyrus in MDD patients with a history of suicide attempt during fMRI tasks. The brain activation changes in these regions were associated with the dysfunction of emotion regulation, processing negative information and self-awareness which may increase the vulnerability of suicidal behavior in MDD patients.
Similar content being viewed by others
References
Adolphs, R. (2003). Is the human amygdala specialized for processing social information? Annals of the New York Academy of Sciences, 985, 326–340.
Ai, H., van Tol, M. J., Marsman, J. C., Veltman, D. J., Ruhe, H. G., van der Wee, N. J. A., et al. (2018). Differential relations of suicidality in depression to brain activation during emotional and executive processing. Journal of Psychiatric Research, 105, 78–85. https://doi.org/10.1016/j.jpsychires.2018.08.018.
Baek, K., Kwon, J., Chae, J. H., Chung, Y. A., Kralik, J. D., Min, J. A., Huh, H. J., Choi, K. M., Jang, K. I., Lee, N. B., Kim, S., Peterson, B. S., & Jeong, J. (2017). Heightened aversion to risk and loss in depressed patients with a suicide attempt history. Scientific Reports, 7(1), 11228. https://doi.org/10.1038/s41598-017-10541-5.
Bostwick, J. M., & Pankratz, V. S. (2000). Affective disorders and suicide risk: a reexamination. The American Journal of Psychiatry, 157(12), 1925–1932. https://doi.org/10.1176/appi.ajp.157.12.1925.
Cao, J., Chen, J.-m., Kuang, L., Ai, M., Fang, W.-d., Gan, Y., Wang, W., Chen, X. R., Xu, X. M., Wang, H. G., & Lv, Z. (2015). Abnormal regional homogeneity in young adult suicide attempters with no diagnosable psychiatric disorder: a resting state functional magnetic imaging study. Psychiatry Research: Neuroimaging, 231(2), 95–102. https://doi.org/10.1016/j.pscychresns.2014.10.011.
Cao, J., Chen, X., Chen, J., Ai, M., Gan, Y., Wang, W., Lv, Z., Zhang, S., Zhang, S., Wang, S., Kuang, L., & Fang, W. (2016). Resting-state functional MRI of abnormal baseline brain activity in young depressed patients with and without suicidal behavior. Journal of Affective Disorders, 205, 252–263. https://doi.org/10.1016/j.jad.2016.07.002.
Chen, Z. Q., Du, M. Y., Zhao, Y. J., Huang, X. Q., Li, J., Lui, S., et al. (2015). Voxel-wise meta-analyses of brain blood flow and local synchrony abnormalities in medication-free patients with major depressive disorder. Journal of Psychiatry & Neuroscience, 40(6), 401–411.
Craig, A. D. (2009). How do you feel--now? The anterior insula and human awareness. Nature Reviews. Neuroscience, 10(1), 59–70. https://doi.org/10.1038/nrn2555.
Du, M., Liu, J., Chen, Z., Huang, X., Li, J., Kuang, W., et al. (2014). Brain grey matter volume alterations in late-life depression. Journal of Psychiatry & Neuroscience, 39(6), 397–406.
Fairhall, S. L., & Ishai, A. (2007). Effective connectivity within the distributed cortical network for face perception. Cerebral Cortex, 17(10), 2400–2406. https://doi.org/10.1093/cercor/bhl148.
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.
Frank, D. W., Dewitt, M., Hudgens-Haney, M., Schaeffer, D. J., Ball, B. H., Schwarz, N. F., Hussein, A. A., Smart, L. M., & Sabatinelli, D. (2014). Emotion regulation: quantitative meta-analysis of functional activation and deactivation. Neuroscience and Biobehavioral Reviews, 45, 202–211. https://doi.org/10.1016/j.neubiorev.2014.06.010.
Giakoumatos, C. I., Tandon, N., Shah, J., Mathew, I. T., Brady, R. O., Clementz, B. A., Pearlson, G. D., Thaker, G. K., Tamminga, C. A., Sweeney, J. A., & Keshavan, M. S. (2013). Are structural brain abnormalities associated with suicidal behavior in patients with psychotic disorders? Journal of Psychiatric Research, 47(10), 1389–1395. https://doi.org/10.1016/j.jpsychires.2013.06.011.
Grill-Spector, K., Knouf, N., & Kanwisher, N. (2004). The fusiform face area subserves face perception, not generic within-category identification. Nature Neuroscience, 7(5), 555–562. https://doi.org/10.1038/nn1224.
Han, D., Li, M., Mei, M., & Sun, X. (2018). The functional and structural characteristics of the emotion network in alexithymia. Neuropsychiatric Disease and Treatment, 14, 991–998. https://doi.org/10.2147/ndt.S154601.
Hwang, J.-P., Lee, T.-W., Tsai, S.-J., Chen, T.-J., Yang, C.-H., Lirng, J.-F., & Tsai, C. F. (2010). Cortical and subcortical abnormalities in late-onset depression with history of suicide attempts investigated with MRI and voxel-based morphometry. Journal of Geriatric Psychiatry and Neurology, 23(3), 171–184. https://doi.org/10.1177/0891988710363713.
Jabbi, M., Kohn, P. D., Nash, T., Ianni, A., Coutlee, C., Holroyd, T., Carver, F. W., Chen, Q., Cropp, B., Kippenhan, J. S., Robinson, S. E., Coppola, R., & Berman, K. F. (2015). Convergent BOLD and Beta-Band activity in superior temporal sulcus and Frontolimbic circuitry underpins human emotion cognition. Cerebral Cortex, 25(7), 1878–1888. https://doi.org/10.1093/cercor/bht427.
Jollant, F., Lawrence, N. S., Giampietro, V., Brammer, M. J., Fullana, M. A., Drapier, D., et al. (2008). Orbitofrontal cortex response to angry faces in men with histories of suicide attempts. The American Journal of Psychiatry, 165(6), 740–748. https://doi.org/10.1176/appi.ajp.2008.07081239.
Jollant, F., Lawrence, N. S., Olie, E., O'Daly, O., Malafosse, A., Courtet, P., & Phillips, M. L. (2010). Decreased activation of lateral orbitofrontal cortex during risky choices under uncertainty is associated with disadvantageous decision-making and suicidal behavior. Neuroimage, 51(3), 1275–1281. https://doi.org/10.1016/j.neuroimage.2010.03.027.
Kang, S. G., Na, K. S., Choi, J. W., Kim, J. H., Son, Y. D., & Lee, Y. J. (2017). Resting-state functional connectivity of the amygdala in suicide attempters with major depressive disorder. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 77, 222–227. https://doi.org/10.1016/j.pnpbp.2017.04.029.
Karnath, H. O., Baier, B., & Nagele, T. (2005). Awareness of the functioning of one's own limbs mediated by the insular cortex? The Journal of Neuroscience, 25(31), 7134–7138. https://doi.org/10.1523/jneurosci.1590-05.2005.
Kenny, E. R., O’Brien, J. T., Cousins, D. A., Richardson, J., Thomas, A. J., Firbank, M. J., & Blamire, A. M. (2010). Functional connectivity in late-life depression using resting-state functional magnetic resonance imaging. The American Journal of Geriatric Psychiatry, 18(7), 643–651. https://doi.org/10.1097/JGP.0b013e3181cabd0e.
Kim, B., Kim, M. K., Yoo, E., Lee, J. Y., Choe, A. Y., Yook, K. H., Lee, K. S., Choi, T. K., & Lee, S. H. (2013). Comparison of panic disorder with and without comorbid major depression by using brain structural magnetic resonance imaging. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 43, 188–196. https://doi.org/10.1016/j.pnpbp.2012.12.022.
Koenigs, M., & Grafman, J. (2009). The functional neuroanatomy of depression: distinct roles for ventromedial and dorsolateral prefrontal cortex. Behavioural Brain Research, 201(2), 239–243. https://doi.org/10.1016/j.bbr.2009.03.004.
Kressel, H. Y. (2017). Setting sail: 2017. Radiology, 282(1), 4–6. https://doi.org/10.1148/radiol.2016162471.
Li, G., Ma, X., Bian, H., Sun, X., Zhai, N., Yao, M., Qu, H., Ji, S., Tian, H., & Zhuo, C. (2016). A pilot fMRI study of the effect of stressful factors on the onset of depression in female patients. Brain Imaging and Behavior, 10(1), 195–202. https://doi.org/10.1007/s11682-015-9382-8.
Lui, S., Zhou, X. J., Sweeney, J. A., & Gong, Q. (2016). Psychoradiology: the frontier of neuroimaging in psychiatry. Radiology, 281(2), 357–372.
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.
Morawetz, C., Bode, S., Derntl, B., & Heekeren, H. R. (2017). The effect of strategies, goals and stimulus material on the neural mechanisms of emotion regulation: a meta-analysis of fMRI studies. Neuroscience and Biobehavioral Reviews, 72, 111–128. https://doi.org/10.1016/j.neubiorev.2016.11.014.
Narumoto, J., Okada, T., Sadato, N., Fukui, K., & Yonekura, Y. (2001). Attention to emotion modulates fMRI activity in human right superior temporal sulcus. Brain Research. Cognitive Brain Research, 12(2), 225–231.
Nock, M. K., Borges, G., Bromet, E. J., Alonso, J., Angermeyer, M., Beautrais, A., Bruffaerts, R., Chiu, W. T., de Girolamo, G., Gluzman, S., de Graaf, R., Gureje, O., Haro, J. M., Huang, Y., Karam, E., Kessler, R. C., Lepine, J. P., Levinson, D., Medina-Mora, M. E., Ono, Y., Posada-Villa, J., & Williams, D. (2008). Cross-national prevalence and risk factors for suicidal ideation, plans and attempts. The British Journal of Psychiatry, 192(2), 98–105. https://doi.org/10.1192/bjp.bp.107.040113.
Olie, E., Ding, Y., Le Bars, E., de Champfleur, N. M., Mura, T., Bonafe, A., et al. (2015). Processing of decision-making and social threat in patients with history of suicidal attempt: a neuroimaging replication study. Psychiatry Research, 234(3), 369–377. https://doi.org/10.1016/j.pscychresns.2015.09.020.
Olie, E., Jollant, F., Deverdun, J., de Champfleur, N. M., Cyprien, F., Le Bars, E., et al. (2017). The experience of social exclusion in women with a history of suicidal acts: a neuroimaging study. Scientific Reports, 7(1), 89. https://doi.org/10.1038/s41598-017-00211-x.
Pan, L. A., Batezati-Alves, S. C., Almeida, J. R., Segreti, A., Akkal, D., Hassel, S., et al. (2011). Dissociable patterns of neural activity during response inhibition in depressed adolescents with and without suicidal behavior. Journal of the American Academy of Child and Adolescent Psychiatry, 50(6), 602–611.e603. https://doi.org/10.1016/j.jaac.2011.03.018.
Pan, L. A., Hassel, S., Segreti, A. M., Nau, S. A., Brent, D. A., & Phillips, M. L. (2013a). Differential patterns of activity and functional connectivity in emotion processing neural circuitry to angry and happy faces in adolescents with and without suicide attempt. Psychological Medicine, 43(10), 2129–2142. https://doi.org/10.1017/s0033291712002966.
Pan, L., Segreti, A., Almeida, J., Jollant, F., Lawrence, N., Brent, D., & Phillips, M. (2013b). Preserved hippocampal function during learning in the context of risk in adolescent suicide attempt. Psychiatry Research, 211(2), 112–118. https://doi.org/10.1016/j.pscychresns.2012.07.008.
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. The British Journal of Psychiatry, 206(4), 339–340. https://doi.org/10.1192/bjp.bp.114.151316.
Peng, D., Shi, F., Li, G., Fralick, D., Shen, T., Qiu, M., Liu, J., Jiang, K., Shen, D., & Fang, Y. (2015). Surface vulnerability of cerebral cortex to major depressive disorder. PLoS One, 10(3), e0120704. https://doi.org/10.1371/journal.pone.0120704.
Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage, 16(2), 331–348. https://doi.org/10.1006/nimg.2002.1087.
Port, J. D. (2018). Diagnosis of attention deficit hyperactivity disorder by using MR imaging and radiomics: a potential tool for clinicians. Radiology, 287(2), 631–632.
Posner, K., Brown, G. K., Stanley, B., Brent, D. A., Yershova, K. V., Oquendo, M. A., Currier, G. W., Melvin, G. A., Greenhill, L., Shen, S., & Mann, J. J. (2011). The Columbia-suicide severity rating scale: initial validity and internal consistency findings from three multisite studies with adolescents and adults. The American Journal of Psychiatry, 168(12), 1266–1277. https://doi.org/10.1176/appi.ajp.2011.10111704.
Powell, T. R., De Jong, S., Breen, G., Lewis, C. M., & Dima, D. (2018). Telomere length as a predictor of emotional processing in the brain. Human Brain Mapping. https://doi.org/10.1002/hbm.24487.
Radua, J., & Mataix-Cols, D. (2009). Voxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. The British Journal of Psychiatry, 195(5), 393–402. https://doi.org/10.1192/bjp.bp.108.055046.
Radua, J., Phillips, M. L., Russell, T., Lawrence, N., Marshall, N., Kalidindi, S., el-Hage, W., McDonald, C., Giampietro, V., Brammer, M. J., David, A. S., & Surguladze, S. A. (2010). Neural response to specific components of fearful faces in healthy and schizophrenic adults. Neuroimage, 49(1), 939–946. https://doi.org/10.1016/j.neuroimage.2009.08.030.
Radua, J., Mataix-Cols, D., Phillips, M. L., El-Hage, W., Kronhaus, D. M., Cardoner, N., et al. (2012). A new meta-analytic method for neuroimaging studies that combines reported peak coordinates and statistical parametric maps. European Psychiatry, 27(8), 605–611. https://doi.org/10.1016/j.eurpsy.2011.04.001.
Richard-Devantoy, S., Ding, Y., Lepage, M., Turecki, G., & Jollant, F. (2016). Cognitive inhibition in depression and suicidal behavior: a neuroimaging study. Psychological Medicine, 46(5), 933–944. https://doi.org/10.1017/s0033291715002421.
Selimbegovic, L., & Chatard, A. (2013). The mirror effect: self-awareness alone increases suicide thought accessibility. Consciousness and Cognition, 22(3), 756–764. https://doi.org/10.1016/j.concog.2013.04.014.
Shepherd, A. M., Matheson, S. L., Laurens, K. R., Carr, V. J., & Green, M. J. (2012). Systematic meta-analysis of insula volume in schizophrenia. Biological Psychiatry, 72(9), 775–784. https://doi.org/10.1016/j.biopsych.2012.04.020.
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.
Sublette, M. E., Milak, M. S., Galfalvy, H. C., Oquendo, M. A., Malone, K. M., & Mann, J. J. (2013). Regional brain glucose uptake distinguishes suicide attempters from non-attempters in major depression. Archives of Suicide Research, 17(4), 434–447. https://doi.org/10.1080/13811118.2013.801813.
Sun, H., Chen, Y., Huang, Q., Lui, S., Huang, X., Shi, Y., Xu, X., Sweeney, J. A., & Gong, Q. (2018). Psychoradiologic utility of MR imaging for diagnosis of attention deficit hyperactivity disorder: a radiomics analysis. Radiology, 287(2), 620–630.
van Beek, E. J. R., Kuhl, C., Anzai, Y., Desmond, P., Ehman, R. L., Gong, Q., et al. (2018). Value of MRI in medicine: more than just another test? Journal of Magnetic Resonance Imaging. https://doi.org/10.1002/jmri.26211.
van Heeringen, K., Bijttebier, S., Desmyter, S., Vervaet, M., & Baeken, C. (2014). Is there a neuroanatomical basis of the vulnerability to suicidal behavior? A coordinate-based meta-analysis of structural and functional MRI studies. Frontiers in Human Neuroscience, 8, 824. https://doi.org/10.3389/fnhum.2014.00824.
Vanyukov, P. M., Szanto, K., Siegle, G. J., Hallquist, M. N., Reynolds, C. F., 3rd, Aizenstein, H. J., et al. (2015). Impulsive traits and unplanned suicide attempts predict exaggerated prefrontal response to angry faces in the elderly. The American Journal of Geriatric Psychiatry, 23(8), 829–839. https://doi.org/10.1016/j.jagp.2014.10.004.
Vanyukov, P. M., Szanto, K., Hallquist, M. N., Siegle, G. J., Reynolds, C. F., 3rd, Forman, S. D., Aizenstein, H. J., & Dombrovski, A. Y. (2016). Paralimbic and lateral prefrontal encoding of reward value during intertemporal choice in attempted suicide. Psychological Medicine, 46(2), 381–391. https://doi.org/10.1017/s0033291715001890.
Vilares, I., Howard, J. D., Fernandes, H. L., Gottfried, J. A., & Kording, K. P. (2012). Differential representations of prior and likelihood uncertainty in the human brain. Current Biology, 22(18), 1641–1648. https://doi.org/10.1016/j.cub.2012.07.010.
Wiles, N., Thomas, L., Abel, A., Ridgway, N., Turner, N., Campbell, J., Garland, A., Hollinghurst, S., Jerrom, B., Kessler, D., Kuyken, W., Morrison, J., Turner, K., Williams, C., Peters, T., & Lewis, G. (2013). Cognitive behavioural therapy as an adjunct to pharmacotherapy for primary care based patients with treatment resistant depression: results of the CoBalT randomised controlled trial. Lancet, 381(9864), 375–384. https://doi.org/10.1016/s0140-6736(12)61552-9.
Acknowledgments
This study was supported by the National Natural Science Foundation (Grant Nos. 81771812, 81621003, 81571637, 81801681), the Sichuan Science and Technology Program (2018SZ0391). Q.G. received the support from Changjiang Scholar Professorship Award (Award No. T2014190) of China and the CMB Distinguished Professorship Award (Award No. F510000/G16916411) administered by the Institute of International Education, USA.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Li, H., Chen, Z., Gong, Q. et al. Voxel-wise meta-analysis of task-related brain activation abnormalities in major depressive disorder with suicide behavior. Brain Imaging and Behavior 14, 1298–1308 (2020). https://doi.org/10.1007/s11682-019-00045-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-019-00045-3