Hostname: page-component-848d4c4894-m9kch Total loading time: 0 Render date: 2024-04-30T16:53:34.237Z Has data issue: false hasContentIssue false
  • English
  • Français

Resting-state network analysis of suicide attempt history in the UK Biobank

Published online by Cambridge University Press:  31 May 2023

Matthew F. Thompson Open the ORCID record for Matthew F. Thompson [Opens in a new window] ,
Marjan Ghahramanlou-Holloway Open the ORCID record for Marjan Ghahramanlou-Holloway [Opens in a new window] ,
Mikela A. Murphy Open the ORCID record for Mikela A. Murphy [Opens in a new window] ,
Kanchana U. Perera Open the ORCID record for Kanchana U. Perera [Opens in a new window] ,
Chelsie Benca-Bachman Open the ORCID record for Chelsie Benca-Bachman [Opens in a new window] ,
Rohan H. C. Palmer Open the ORCID record for Rohan H. C. Palmer [Opens in a new window]  and
Joshua C. Gray Open the ORCID record for Joshua C. Gray [Opens in a new window]
Matthew F. Thompson*
Affiliation:
Department of Medical & Clinical Psychology, Uniformed Services University of the Health Sciences, Bethesda, MD, USA Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., Bethesda, MD, USA
Marjan Ghahramanlou-Holloway
Affiliation:
Department of Medical & Clinical Psychology, Uniformed Services University of the Health Sciences, Bethesda, MD, USA
Mikela A. Murphy
Affiliation:
Department of Medical & Clinical Psychology, Uniformed Services University of the Health Sciences, Bethesda, MD, USA Department of Psychology, Fordham University, New York, NY, USA
Kanchana U. Perera
Affiliation:
Department of Medical & Clinical Psychology, Uniformed Services University of the Health Sciences, Bethesda, MD, USA
Chelsie Benca-Bachman
Affiliation:
Behavioral Genetics of Addiction Laboratory, Department of Psychology, Emory University, Atlanta, GA, USA
Rohan H. C. Palmer
Affiliation:
Behavioral Genetics of Addiction Laboratory, Department of Psychology, Emory University, Atlanta, GA, USA
Joshua C. Gray
Affiliation:
Department of Medical & Clinical Psychology, Uniformed Services University of the Health Sciences, Bethesda, MD, USA
*
Corresponding author: Matthew F. Thompson; Email: Matthew.Thompson.ctr@usuhs.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Prior research has identified altered brain structure and function in individuals at risk for self-directed violence thoughts and behaviors. However, these studies have largely utilized healthy controls and findings have been inconsistent. Thus, this study examined differences in resting-state functional network connectivity among individuals with lifetime suicide attempt(s) v. lifetime self-directed violence thoughts alone.

Methods

Using data from the UK Biobank, this study utilized a series of linear regressions to compare individuals with lifetime suicide attempt(s) (n = 566) v. lifetime self-directed violence thoughts alone (n = 3447) on within- and between- network resting-state functional connectivity subnetworks.

Results

There were no significant between-group differences for between-network, within-network, or whole-brain functional connectivity after adjusting for age, sex, ethnicity, and body mass index and performing statistical corrections for multiple comparisons. Resting-state network measures may not differentiate between individuals with lifetime suicide attempt(s) and lifetime self-directed violence thoughts alone.

Conclusions

Null findings diverge from results reported in smaller neuroimaging studies of suicide risk, but are consistent with null findings in other large-scale studies and meta-analyses. Strengths of the study include its large sample size and stringent control group. Future research on a wider array of imaging, genetic, and psychosocial risk factors can clarify relative contributions of individual and combined variables to suicide risk and inform scientific understanding of ideation-to-action framework.

Keywords

fMRIresting-stateself-directed violencesuicideUK Biobank
Type
Original Article
Information
Psychological Medicine , Volume 53 , Issue 16 , December 2023 , pp. 7591 - 7600
Copyright
Copyright © Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., 2023. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ai, H., van Tol, M. J., Marsman, J. C., Veltman, D. J., Ruhe, H. G., van der Wee, N. J. A., … Aleman, A. (2018). Differential relations of suicidality in depression to brain activation during emotional and executive processing. Journal of Psychiatric Research, 105, 78–85. doi: 10.1016/j.jpsychires.2018.08.018CrossRefGoogle ScholarPubMed
Alfaro-Almagro, F., Jenkinson, M., Bangerter, N. K., Andersson, J. L. R., Griffanti, L., Douaud, G., … Smith, S. M. (2018). Image processing and Quality Control for the first 10,000 brain imaging datasets from UK Biobank. NeuroImage, 166, 400–424. doi: 10.1016/j.neuroimage.2017.10.034CrossRefGoogle Scholar
Alfaro-Almagro, F., McCarthy, P., Afyouni, S., Andersson, J. L. R., Bastiani, M., Miller, K. L., … Smith, S. M. (2021). Confound modelling in UK Biobank brain imaging. NeuroImage, 224, 117002. doi: 10.1016/j.neuroimage.2020.117002CrossRefGoogle ScholarPubMed
Andersson, J. L., Jenkinson, M., & Smith, S. (2007). Non-linear registration aka Spatial normalisation FMRIB Technial Report TR07JA2. FMRIB Analysis Group of the University of Oxford.Google Scholar
Balcioglu, Y. H., & Kose, S. (2018). Neural substrates of suicide and suicidal behaviour: From a neuroimaging perspective. Psychiatry and Clinical Psychopharmacology, 28(3), 314–328.CrossRefGoogle Scholar
Barredo, J., Bozzay, M., Primack, J., Schatten, H., Armey, M., Carpenter, L. L., & Philip, N. S. (2021). Translating interventional neuroscience to suicide–it's about time. Biological Psychiatry, 89(11), 1073–1083.CrossRefGoogle ScholarPubMed
Boisseau, C. L., Yen, S., Markowitz, J. C., Grilo, C. M., Sanislow, C. A., Shea, M. T., … Morey, L. C. (2013). Individuals with single versus multiple suicide attempts over 10 years of prospective follow-up. Comprehensive Psychiatry, 54(3), 238–242.CrossRefGoogle Scholar
Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The brain's default network: Anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124, 1–38. doi: 10.1196/annals.1440.011CrossRefGoogle ScholarPubMed
Buckner, R. L., & DiNicola, L. M. (2019). The brain's default network: Updated anatomy, physiology and evolving insights. Nature Reviews Neuroscience, 20(10), 593–608. doi: 10.1038/s41583-019-0212-7CrossRefGoogle ScholarPubMed
Button, K. S., Ioannidis, J. P., Mokrysz, C., Nosek, B. A., Flint, J., Robinson, E. S., & Munafo, M. R. (2013). Power failure: Why small sample size undermines the reliability of neuroscience. Nature Reviews Neuroscience, 14(5), 365–376. doi: 10.1038/nrn3475CrossRefGoogle ScholarPubMed
Cao, J., Ai, M., Chen, X., Chen, J., Wang, W., & Kuang, L. (2020). Altered resting-state functional network connectivity is associated with suicide attempt in young depressed patients. Psychiatry Research, 285, 112713.CrossRefGoogle ScholarPubMed
Cao, J., Chen, J.-M., Kuang, L., Ai, M., Fang, W.-D., Gan, Y., … Wang, H.-G. (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.CrossRefGoogle ScholarPubMed
Chase, H. W., Segreti, A. M., Keller, T. A., Cherkassky, V. L., Just, M. A., Pan, L. A., & Brent, D. A. (2017). Alterations of functional connectivity and intrinsic activity within the cingulate cortex of suicidal ideators. Journal of Affective Disorders, 212, 78–85.CrossRefGoogle ScholarPubMed
Chen, C. F., Chen, W. N., & Zhang, B. (2021). Functional alterations of the suicidal brain: A coordinate-based meta-analysis of functional imaging studies. Brain Imaging and Behavior, 16(1), 291–304. doi: 10.1007/s11682-021-00503-x.CrossRefGoogle Scholar
Cole, M. W., Repovs, G., & Anticevic, A. (2014). The frontoparietal control system: A central role in mental health. Neuroscientist, 20(6), 652–664. doi: 10.1177/1073858414525995CrossRefGoogle ScholarPubMed
Crosby, A., Gfroerer, J., Han, B., Ortega, L., & Parks, S. E. (2011a). Suicidal thoughts and behaviors among adults aged> ̲18 years – United States, 2008–2009. Atlanta, GA: Centers for Disease Control and Prevention.Google ScholarPubMed
Crosby, A., Ortega, L., & Melanson, C. (2011b). Self-directed violence surveillance: Uniform definitions and recommended data elements. Atlanta, GA: Centers for Disease Control and Prevention.Google Scholar
David, S. P., Ware, J. J., Chu, I. M., Loftus, P. D., Fusar-Poli, P., Radua, J., … Ioannidis, J. P. (2013). Potential reporting bias in fMRI studies of the brain. PLoS One, 8(7), e70104. doi: 10.1371/journal.pone.0070104CrossRefGoogle ScholarPubMed
Desmyter, S., van Heeringen, C., & Audenaert, K. (2011). Structural and functional neuroimaging studies of the suicidal brain. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 35(4), 796–808. doi: 10.1016/j.pnpbp.2010.12.026CrossRefGoogle ScholarPubMed
Dutt, R. K., Hannon, K., Easley, T. O., Griffis, J. C., Zhang, W., & Bijsterbosch, J. D. (2022). Mental health in the UK Biobank: A roadmap to self-report measures and neuroimaging correlates. Human Brain Mapping, 43(2), 816–832. doi: 10.1002/hbm.25690CrossRefGoogle ScholarPubMed
Fornito, A., Zalesky, A., & Breakspear, M. (2015). The connectomics of brain disorders. Nature Reviews Neuroscience, 16(3), 159–172. doi: 10.1038/nrn3901CrossRefGoogle ScholarPubMed
Fox, M. D., Zhang, D., Snyder, A. Z., & Raichle, M. E. (2009). The global signal and observed anticorrelated resting state brain networks. Journal of Neurophysiology, 101(6), 3270–3283. doi: 10.1152/jn.90777.2008CrossRefGoogle ScholarPubMed
Franklin, J. C., Ribeiro, J. D., Fox, K. R., Bentley, K. H., Kleiman, E. M., Huang, X., … Nock, M. K. (2017). Risk factors for suicidal thoughts and behaviors: A meta-analysis of 50 years of research. Psychological Bulletin, 143(2), 187–232. doi: 10.1037/bul0000084CrossRefGoogle ScholarPubMed
Gallyer, A. J., Dougherty, S. P., Burani, K., Albanese, B. J., Joiner, T. E., & Hajcak, G. (2021). Suicidal thoughts, behaviors, and event-related potentials: A systematic review and meta-analysis. Psychophysiology, 58(12), e13939. doi: 10.1111/psyp.13939CrossRefGoogle ScholarPubMed
Gratton, C., Nelson, S. M., & Gordon, E. M. (2022). Brain-behavior correlations: Two paths toward reliability. Neuron, 110(9), 1446–1449. doi: 10.1016/j.neuron.2022.04.018CrossRefGoogle ScholarPubMed
Griffanti, L., Douaud, G., Bijsterbosch, J., Evangelisti, S., Alfaro-Almagro, F., Glasser, M. F., … Smith, S. M. (2017). Hand classification of fMRI ICA noise components. NeuroImage, 154, 188–205. doi: 10.1016/j.neuroimage.2016.12.036CrossRefGoogle ScholarPubMed
Huang, X., Rootes-Murdy, K., Bastidas, D. M., Nee, D. E., & Franklin, J. C. (2020). Brain differences associated with self-injurious thoughts and behaviors: A meta-analysis of neuroimaging studies. Scientific Reports, 10(1), 2404. doi: 10.1038/s41598-020-59490-6CrossRefGoogle ScholarPubMed
Hyatt, C. S., Owens, M. M., Crowe, M. L., Carter, N. T., Lynam, D. R., & Miller, J. D. (2020). The quandary of covarying: A brief review and empirical examination of covariate use in structural neuroimaging studies on psychological variables. NeuroImage, 205, 116225. doi: 10.1016/j.neuroimage.2019.116225CrossRefGoogle ScholarPubMed
Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17(2), 825–841. doi: 10.1016/s1053-8119(02)91132-8CrossRefGoogle ScholarPubMed
Jiao, Z., Lai, Y., Kang, J., Gong, W., Ma, L., Jia, T., … Feng, J. (2022). A model-based approach to assess reproducibility for large-scale high-throughput MRI-based studies. NeuroImage, 255, 119166. doi: 10.1016/j.neuroimage.2022.119166CrossRefGoogle ScholarPubMed
Jollant, F., Lawrence, N. L., Olie, E., Guillaume, S., & Courtet, P. (2011). The suicidal mind and brain: A review of neuropsychological and neuroimaging studies. The World Journal of Biological Psychiatry, 12(5), 319–339. doi: 10.3109/15622975.2011.556200CrossRefGoogle ScholarPubMed
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 and Biological Psychiatry, 77, 222–227. doi: 10.1016/j.pnpbp.2017.04.029CrossRefGoogle ScholarPubMed
Klinitzke, G., Steinig, J., Bluher, M., Kersting, A., & Wagner, B. (2013). Obesity and suicide risk in adults--A systematic review. Journal of Affective Disorders, 145(3), 277–284. doi: 10.1016/j.jad.2012.07.010CrossRefGoogle ScholarPubMed
Klonsky, E. D., & May, A. M. (2015). The three-step theory (3ST): A new theory of suicide rooted in the “ideation-to-action” framework. International Journal of Cognitive Therapy, 8(2), 114–129.CrossRefGoogle Scholar
Klonsky, E. D., Qiu, T., & Saffer, B. Y. (2017). Recent advances in differentiating suicide attempters from suicide ideators. Current Opinions in Psychiatry, 30(1), 15–20. doi: 10.1097/YCO.0000000000000294CrossRefGoogle ScholarPubMed
Klonsky, E. D., Saffer, B. Y., & Bryan, C. J. (2018). Ideation-to-action theories of suicide: A conceptual and empirical update. Current Opinion in Psychology, 22, 38–43. doi: 10.1016/j.copsyc.2017.07.020CrossRefGoogle ScholarPubMed
Kullmann, S., Heni, M., Veit, R., Ketterer, C., Schick, F., Haring, H. U., … Preissl, H. (2012). The obese brain: Association of body mass index and insulin sensitivity with resting state network functional connectivity. Human Brain Mapping, 33(5), 1052–1061. doi: 10.1002/hbm.21268CrossRefGoogle ScholarPubMed
Malhi, G. S., Das, P., Outhred, T., Bryant, R. A., Calhoun, V., & Mann, J. J. (2020). Default mode dysfunction underpins suicidal activity in mood disorders. Psychological Medicine, 50(7), 1214–1223. doi: 10.1017/S0033291719001132CrossRefGoogle ScholarPubMed
Malhi, G. S., Das, P., Outhred, T., Gessler, D., John Mann, J., & Bryant, R. (2019). Cognitive and emotional impairments underpinning suicidal activity in patients with mood disorders: An fMRI study. Acta Psychiatrica Scanddinavica, 139(5), 454–463. doi: 10.1111/acps.13022CrossRefGoogle ScholarPubMed
Marek, S., Tervo-Clemmens, B., Calabro, F. J., Montez, D. F., Kay, B. P., Hatoum, A. S., … Hendrickson, T. J. (2022). Reproducible brain-wide association studies require thousands of individuals. Nature, 603(7902), 654–660.CrossRefGoogle ScholarPubMed
May, A. M., & Klonsky, E. D. (2016). What distinguishes suicide attempters from suicide ideators? A meta-analysis of potential factors. Clinical Psychology: Science and Practice, 23(1), 5–20.Google Scholar
Menon, V. (2011). Large-scale brain networks and psychopathology: A unifying triple network model. Trends in Cognitive Sciences, 15(10), 483–506. doi: 10.1016/j.tics.2011.08.003CrossRefGoogle ScholarPubMed
Miller, K. L., Alfaro-Almagro, F., Bangerter, N. K., Thomas, D. L., Yacoub, E., Xu, J., … Smith, S. M. (2016). Multimodal population brain imaging in the UK Biobank prospective epidemiological study. Nature Neuroscience, 19(11), 1523–1536. doi: 10.1038/nn.4393CrossRefGoogle ScholarPubMed
Minzenberg, M. J., Lesh, T. A., Niendam, T. A., Cheng, Y., & Carter, C. S. (2016). Conflict-related anterior cingulate functional connectivity is associated with past suicidal ideation and behavior in recent-onset psychotic major mood disorders. The Journal of Neuropsychiatry and Clinical Neurosciences, 28(4), 299–305.CrossRefGoogle ScholarPubMed
Minzenberg, M. J., Lesh, T. A., Niendam, T. A., Yoon, J. H., Cheng, Y., Rhoades, R. N., & Carter, C. S. (2015). Control-related frontal-striatal function is associated with past suicidal ideation and behavior in patients with recent-onset psychotic major mood disorders. Journal of Affective Disorders, 188, 202–209.CrossRefGoogle ScholarPubMed
Nock, M. K., Borges, G., Bromet, E. J., Alonso, J., Angermeyer, M., Beautrais, A., … Williams, D. (2008). Cross-national prevalence and risk factors for suicidal ideation, plans and attempts. The British Journal of Psychiatry, 192(2), 98–105. doi: 10.1192/bjp.bp.107.040113CrossRefGoogle ScholarPubMed
Ordaz, S. J., Goyer, M. S., Ho, T. C., Singh, M. K., & Gotlib, I. H. (2018). Network basis of suicidal ideation in depressed adolescents. Journal of Affective Disorders, 226, 92–99. doi: 10.1016/j.jad.2017.09.021CrossRefGoogle ScholarPubMed
Piscopo, K., Lipari, R. N., Cooney, J., & Glasheen, C. (2016). Suicidal thoughts and behavior among adults: Results from the 2015 national survey on drug use and health. NSDUH Data Review, 9, 1–15.Google Scholar
Pruim, R. H. R., Mennes, M., van Rooij, D., Llera, A., Buitelaar, J. K., & Beckmann, C. F. (2015). ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data. NeuroImage, 112, 267–277. doi: 10.1016/j.neuroimage.2015.02.064CrossRefGoogle ScholarPubMed
Ren, Y., You, J., Zhang, X., Huang, J., Conner, B. T., Sun, R., … Lin, M. P. (2019). Differentiating suicide attempters from suicide ideators: The role of capability for suicide. Archives of Suicide Research, 23(1), 64–81. doi: 10.1080/13811118.2018.1426507CrossRefGoogle ScholarPubMed
Ritchie, S. J., Cox, S. R., Shen, X., Lombardo, M. V., Reus, L. M., Alloza, C., … Deary, I. J. (2018). Sex differences in the adult human brain: Evidence from 5216 UK Biobank participants. Cerebral Cortex, 28(8), 2959–2975. doi: 10.1093/cercor/bhy109CrossRefGoogle ScholarPubMed
Rudd, M. D. (2000). The suicidal mode: A cognitive-behavioral model of suicidality. Suicide and Life-Threatening Behavior, 30(1), 18–33.CrossRefGoogle Scholar
Schaefer, A., Kong, R., Gordon, E. M., Laumann, T. O., Zuo, X. N., Holmes, A. J., … Yeo, B. T. T. (2018). Local-global parcellation of the human cerebral cortex from intrinsic functional connectivity MRI. Cerebral Cortex, 28(9), 3095–3114. doi: 10.1093/cercor/bhx179CrossRefGoogle ScholarPubMed
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), 408–427. doi: 10.1038/s41380-019-0587-xCrossRefGoogle ScholarPubMed
Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., … Greicius, M. D. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience, 27(9), 2349–2356. doi: 10.1523/JNEUROSCI.5587-06.2007CrossRefGoogle ScholarPubMed
Serafini, G., Pardini, M., Pompili, M., Girardi, P., & Amore, M. (2016). Understanding suicidal behavior: The contribution of recent resting-state fMRI techniques. Frontiers in Psychiatry, 7(69), 69. doi: 10.3389/fpsyt.2016.00069CrossRefGoogle ScholarPubMed
Shen, X., Cox, S. R., Adams, M. J., Howard, D. M., Lawrie, S. M., Ritchie, S. J., … Whalley, H. C. (2018). Resting-state connectivity and its association with cognitive performance, educational attainment, and household income in the UK Biobank. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3(10), 878–886. doi: 10.1016/j.bpsc.2018.06.007Google ScholarPubMed
Smith, S. M., & Nichols, T. E. (2018). Statistical challenges in “big data” human neuroimaging. Neuron, 97(2), 263–268.CrossRefGoogle ScholarPubMed
Smith, S. M., Nichols, T. E., Vidaurre, D., Winkler, A. M., Behrens, T. E., Glasser, M. F., … Miller, K. L. (2015). A positive-negative mode of population covariation links brain connectivity, demographics and behavior. Nature Neuroscience, 18(11), 1565–1567. doi: 10.1038/nn.4125CrossRefGoogle ScholarPubMed
Szucs, D., & Ioannidis, J. P. (2020). Sample size evolution in neuroimaging research: An evaluation of highly-cited studies (1990–2012) and of latest practices (2017–2018) in high-impact journals. NeuroImage, 221, 117164. doi: 10.1016/j.neuroimage.2020.117164CrossRefGoogle Scholar
Uddin, L. Q., Yeo, B. T. T., & Spreng, R. N. (2019). Towards a universal taxonomy of macro-scale functional human brain networks. Brain Topography, 32(6), 926–942. doi: 10.1007/s10548-019-00744-6CrossRefGoogle ScholarPubMed
van Heeringen, K., & Mann, J. J. (2014). The neurobiology of suicide. The Lancet. Psychiatry, 1(1), 63–72. doi: 10.1016/S2215-0366(14)70220-2CrossRefGoogle ScholarPubMed
Yeo, B. T., Krienen, F. M., Sepulcre, J., Sabuncu, M. R., Lashkari, D., Hollinshead, M., … Buckner, R. L. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106(3), 1125–1165. doi: 10.1152/jn.00338.2011Google ScholarPubMed
Zhang, Y., Brady, M., & Smith, S. (2001). Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Transactions on Medical Imaging, 20(1), 45–57.CrossRefGoogle ScholarPubMed
Supplementary material: File

Thompson et al. supplementary material
Download undefined(File)
File 931.5 KB