Abstract
Relative to the general population, criminal offenders have a higher risk of suicide. Neurobiological deficits related to suicidal behavior have been identified in the general population, but unexamined in offenders to date. We examined the association between brain morphology and suicidal behavior in adult male criminal offenders. Brain morphology was examined using voxel-based morphometry (VBM) and source-based morphometry (SBM), a multivariate alternative to VBM which analyzes brain volume in between-subject spatially independent networks. Results showed that offenders with past suicide attempts (n = 19), relative to offenders without past suicide attempts (n = 19) and non-offenders (n = 26), had reduced gray matter in an SBM component that comprised the posterior cingulate, dorsal prefrontal cortex, and amygdala. The SBM source weights were significantly associated with suicide attempts independent of other suicide risk variables (e.g., depression). VBM results were similar to the SBM results but less robust. The results reveal a potential neurobiological marker of vulnerability to suicidal behavior among criminal offenders and illustrate the utility of multivariate methods of gray matter analyses.
Similar content being viewed by others
Notes
Drug use disorder could not be analyzed due to (quasi) separation: nearly all participants (n = 34) met criteria for a drug use disorder. C29 loading weights were not significantly different between offenders with and without a drug use disorder (t(36) = 1.44, p = 0.16)
References
Aguilar, E. J., García-Martí, G., Martí-Bonmatí, L., Lull, J. J., Moratal, D., Escartí, M. J., et al. (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), 1673–1676.
Angst, J., Angst, F., Gerber-Werder, R., & Gamma, A. (2005). Suicide in 406 mood-disorder patients with and without long-term medication: A 40 to 44 years' follow-up. Archives of Suicide Research, 9(3), 279–300.
Arsenault-Lapierre, G., Kim, C., & Turecki, G. (2004). Psychiatric diagnoses in 3275 suicides: A meta-analysis. BMC Psychiatry, 4(1), 37.
Ashburner, J., & Friston, K. J. (2005). Unified segmentation. Neuroimage, 26(3), 839–851.
Benedetti, F., Radaelli, D., Poletti, S., Locatelli, C., Falini, A., Colombo, C., et al. (2011). Opposite effects of suicidality and lithium on gray matter volumes in bipolar depression. Journal of Affective Disorders, 135(1), 139–147.
Blaauw, E., Kerkhof, A. J. F. M., & Hayes, L. M. (2005). Demographic, criminal, and psychiatric factors related to inmate suicide. Suicide and Life-threatening Behavior, 35(1), 63–75.
Brådvik, L., Mattisson, C., Bogren, M., & Nettelbladt, P. (2008). Long-term suicide risk of depression in the Lundby cohort 1947–1997–severity and gender. Acta Psychiatrica Scandinavica, 117(3), 185–191.
Briere, J., & Elliott, D. M. (2003). Prevalence and psychological sequelae of self-reported childhood physical and sexual abuse in a general population sample of men and women. Child Abuse and Neglect, 27, 1205–1222.
Brown, G. K., Beck, A. T., Steer, R. A., & Grisham, J. R. (2000). Risk factors for suicide in psychiatric outpatients: A 20-year prospective study. Journal of Consulting and Clinical Psychology, 68(3), 371–377.
Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The brain's default network. Annals of the New York Academy of Sciences, 1124(1), 1–38.
Dahlgren, K. (1977). Attempted suicides—35 years afterward. Suicide and Life-threatening Behavior, 7(2), 75–79.
Ding, Y., Lawrence, N., Olie, E., Cyprien, F., Le Bars, E., Bonafe, A., Phillips, M. L., Courtet, P., & Jollant, F. (2015). Prefrontal cortex markers of suicidal vulnerability in mood disorders: A model-based structural neuroimaging study with a translational perspective. Translational Psychiatry, 5(2), e516.
Douglas, K. S., Lilienfeld, S. O., Skeem, J. L., Poythress, N. G., Edens, J. F., & Patrick, C. J. (2008). Relation of antisocial and psychopathic traits to suicide-related behavior among offenders. Law and Human Behavior, 32(6), 511–525.
Duarte, D. G., Maila de Castro, L. N., Albuquerque, M. R., Turecki, G., Ding, Y., de Souza-Duran, F. L., Busatto, G., & Correa, H. (2017). Structural brain abnormalities in patients with type I bipolar disorder and suicidal behavior. Psychiatry Research: Neuroimaging, 265, 9–17.
Dube, S. R., Anda, R. F., Felitti, V. J., Chapman, D. P., Williamson, D. F., & Giles, W. H. (2001). Childhood abuse, household dysfunction, and the risk of attempted suicide throughout the life span: Findings from the adverse childhood experiences study. JAMA, 286(24), 3089–3096.
First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (1997). Structured clinical interview for DSM-IV Axis I disorders – Clinical version (SCID-IV). Washington, D.C.: American Psychiatric Press.
Fruehwald, S., Matschnig, T., Koenig, F., Bauer, P., & Frottier, P. (2004). Suicide in custody: case–control study. The British Journal of Psychiatry, 185(6), 494–498.
Giakoumatos, C. I., Tandon, N., Shah, J., Mathew, I. T., Brady, R. O., Clementz, B. A., et al. (2013). Are structural brain abnormalities associated with suicidal behavior in patients with psychotic disorders? Journal of Psychiatric Research, 47(10), 1389–1395.
Gunnell, D., & Lewis, G. (2005). Studying suicide from the life course perspective: Implications for prevention. The British Journal of Psychiatry, 187(3), 206–208.
Hare, R. D. (2003). The hare psychopathy checklist-revised. Toronto: Multi-Health Systems.
Harrison, B. J., Pujol, J., López-Solà, M., Hernández-Ribas, R., Deus, J., Ortiz, H., et al. (2008). Consistency and functional specialization in the default mode brain network. Proceedings of the National Academy of Sciences, 105(28), 9781–9786.
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.
Jenkins, R., Bhugra, D., Meltzer, H., Singleton, N., Bebbington, P., Brugha, T., et al. (2005). Psychiatric and social aspects of suicidal behaviour in prisons. Psychological Medicine, 35(2), 257–269.
Johnston, J. A., Wang, F., Liu, J., Blond, B. N., Wallace, A., Liu, J., Spencer, L., Cox Lippard, E. T., Purves, K. L., Landeros-Weisenberger, A., & Hermes, E. (2017). Multimodal neuroimaging of frontolimbic structure and function associated with suicide attempts in adolescents and young adults with bipolar disorder. American Journal of Psychiatry, 174(7), 667–675.
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. American Journal of Psychiatry, 165, 740–748.
Kašpárek, T., Mareček, R., Schwarz, D., Přikryl, R., Vaníček, J., Mikl, M., et al. (2010). Source-based morphometry of gray matter volume in men with first-episode schizophrenia. Human Brain Mapping, 31(2), 300–310.
Li, Y. O., Adalı, T., & Calhoun, V. D. (2007). Estimating the number of independent components for functional magnetic resonance imaging data. Human Brain Mapping, 28(11), 1251–1266.
London, E. D., Ernst, M., Grant, S., Bonson, K., & Weinstein, A. (2000). Orbitofrontal cortex and human drug abuse: Functional imaging. Cerebral Cortex, 10(3), 334–342.
Minzenberg, M. J., Lesh, T. A., Niendam, T. A., Yoon, J. H., Cheng, Y., Rhoades, R. N., et al. (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.
Monkul, E., Hatch, J. P., Nicoletti, M. A., Spence, S., Brambilla, P., Lacerda, A. L. T. d., et al. (2007). Fronto-limbic brain structures in suicidal and non-suicidal female patients with major depressive disorder. Molecular Psychiatry, 12(4), 360–366.
Nock, M. K., & Kessler, R. C. (2006). Prevalence of and risk factors for suicide attempts versus suicide gestures: Analysis of the National Comorbidity Survey. Journal of Abnormal Psychology, 115(3), 616–623.
Ochsner, K. N., Silvers, J. A., & Buhle, J. T. (2012). Functional imaging studies of emotion regulation: A synthetic review and evolving model of the cognitive control of emotion. Annals of the New York Academy of Sciences, 1251(1), E1–E24.
Pan, L., Hassel, S., Segreti, A., Nau, S., Brent, D., & Phillips, M. (2013). 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.
Patton, J. H., Stanford, M. S., & Barratt, E. S. (1995). Factor structure of the barratt impulsiveness scale. Journal of Clinical Psychology, 51(6), 768–774.
Phillips, M. L., Ladouceur, C. D., & Drevets, W. C. (2008). A neural model of voluntary and automatic emotion regulation: Implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry, 13(9), 833–857.
Posner, K., Brown, G. K., Stanley, B., Brent, D. A., Yershova, K. V., Oquendo, M. A., et al. (2011). The Columbia–suicide severity rating scale: Initial validity and internal consistency findings from three multisite studies with adolescents and adults. American Journal of Psychiatry., 168, 1266–1277.
Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences, 98(2), 676–682.
Reisch, T., Seifritz, E., Esposito, F., Wiest, R., Valach, L., & Michel, K. (2010). An fMRI study on mental pain and suicidal behavior. Journal of Affective Disorders, 126(1–2), 321–325.
Rentería, M. E., Schmaal, L., Hibar, D. P., Couvy-Duchesne, B., Strike, L. T., Mills, N. T., de Zubicaray, G. I., McMahon, K. L., Medland, S. E., Gillespie, N. A., & Hatton, S. N. (2017). Subcortical brain structure and suicidal behaviour in major depressive disorder: A meta-analysis from the ENIGMA-MDD working group. Translational Psychiatry, 7(5), e1116.
Ryan, J. J., Lopez, S. J., & Werth, T. R. (1999). Development and preliminary validation of a Satz-Mogel short form of the Wais-III in a sample of persons with substance abuse disorders. International Journal of Neuroscience, 98, 131–140.
Scheuerecker, J., Meisenzahl, E. M., Koutsouleris, N., Linn, J., Wiesmann, M., Brückmann, H., et al. (2010). Orbitofrontal volume reductions during emotion recognition in patients with major depression. Journal of psychiatry & neuroscience: JPN, 35(5), 311–320.
Schoenbaum, G., Roesch, M. R., & Stalnaker, T. A. (2006). Orbitofrontal cortex, decision-making and drug addiction. Trends in Neurosciences, 29(2), 116–124.
Silvers, J. A., Hubbard, A. D., Chaudhury, S., Biggs, E., Shu, J., Grunebaum, M. F., et al. (2016). Suicide attempters with borderline personality disorder show differential orbitofrontal and parietal recruitment when reflecting on aversive memories. Journal of Psychiatric Research, 81, 71–78.
Suominen, K., Isometsä, E., Suokas, J., Haukka, J., Achte, K., & Lönnqvist, J. (2004). Completed suicide after a suicide attempt: A 37-year follow-up study. American Journal of Psychiatry, 161(3), 562–563.
Swann, A. C., Dougherty, D. M., Pazzaglia, P. J., Pham, M., Steinberg, J. L., & Moeller, F. G. (2005). Increased impulsivity associated with severity of suicide attempt history in patients with bipolar disorder. American Journal of Psychiatry, 162(9), 1680–1687.
Swanson, J. W., Swartz, M. S., Van Dorn, R. A., Elbogen, E. B., Wagner, H. R., Rosenheck, R. A., et al. (2006). A national study of violent behavior in persons with schizophrenia. Archives of General Psychiatry, 63(5), 490–499.
Swogger, M. T., You, S., Cashman-Brown, S., & Conner, K. R. (2011). Childhood physical abuse, aggression, and suicide attempts among criminal offenders. Psychiatry Research, 185(3), 363–367.
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.
Volkow, N. D., & Fowler, J. S. (2000). Addiction, a disease of compulsion and drive: Involvement of the orbitofrontal cortex. Cerebral Cortex, 10(3), 318–325.
Wager, T. D., Davidson, M. L., Hughes, B. L., Lindquist, M. A., & Ochsner, K. N. (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron, 59(6), 1037–1050.
Wagner, G., Koch, K., Schachtzabel, C., Peikert, G., Sauer, H., & Schlösser, R. (2008). Enhanced rostral anterior cingulate cortex activation during cognitive control is related to orbitofrontal volume reduction in unipolar depression. Journal of Affective Disorders, 107, S76–S77.
Wagner, G., Koch, K., Schachtzabel, C., Schultz, C. C., Sauer, H., & Schlösser, R. G. (2011). Structural brain alterations in patients with major depressive disorder and high risk for suicide: Evidence for a distinct neurobiological entity? Neuroimage, 54(2), 1607–1614.
Wechsler, D. (1997). Wechsler Adult Intelligence Scale. New York: Psychological Corporation.
Wolf, R. C., Huber, M., Lepping, P., Sambataro, F., Depping, M. S., Karner, M., et al. (2014). Source-based morphometry reveals distinct patterns of aberrant brain volume in delusional infestation. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 48, 112–116.
Xu, L., Groth, K. M., Pearlson, G., Schretlen, D. J., & Calhoun, V. D. (2009). Source-based morphometry: The use of independent component analysis to identify gray matter differences with application to schizophrenia. Human Brain Mapping, 30(3), 711–724.
Zalsman, G., Hawton, K., Wasserman, D., van Heeringen, K., Arensman, E., Sarchiapone, M., et al. (2016). Suicide prevention strategies revisited: 10-year systematic review. Lancet Psychiatry, 3, 646–659.
Funding
This work was supported by grants from the National Institutes of Health (P20GM103472; R01DA026505; R01MH070539).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
About this article
Cite this article
Harenski, C.L., Harenski, K.A., Calhoun, V.D. et al. Source-based morphometry reveals gray matter differences related to suicidal behavior in criminal offenders. Brain Imaging and Behavior 14, 1–9 (2020). https://doi.org/10.1007/s11682-018-9957-2
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-018-9957-2