Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Altered brain processing of decision-making in healthy first-degree biological relatives of suicide completers

Abstract

Suicidal behavior is heritable, with the transmission of risk being related to the transmission of vulnerability traits. Previous studies suggest that risky decision-making may be an endophenotype of suicide. Here, we aimed at investigating brain processing of decision-making in relatives of suicide completers in order to shed light on heritable mechanisms of suicidal vulnerability. Seventeen healthy first-degree biological relatives of suicide completers with no personal history of suicidal behavior, 16 relatives of depressed patients without any personal or family history of suicidal behavior, and 19 healthy controls were recruited. Functional 3 T magnetic resonance imaging scans were acquired while participants underwent the Iowa Gambling Task, an economic decision-making test. Whole-brain analyses contrasting activations during risky vs safe choices were conducted with AFNI and FSL. Individuals with a family history of suicide in comparison to control groups showed altered contrasts in left medial orbitofrontal cortex, and right dorsomedial prefrontal cortex. This pattern was different from the neural basis of familial depression. Moreover, controls in comparison to relatives showed increased contrast in several regions including the post-central gyrus, posterior cingulate and parietal cortices, and cerebellum (culmen) in familial suicide; and inferior parietal, temporal, occipital, anteromedial and dorsolateral prefrontal cortices, and cerebellum (vermis) in familial depression. These findings most likely represent a complex combination of vulnerability and protective mechanisms in relatives. They also support a significant role for deficient risk processing, and ventral and dorsal prefrontal cortex functioning in the suicidal diathesis.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1

Similar content being viewed by others

References

  1. Jollant F, Lawrence NL, Olie E, Guillaume S, Courtet P . The suicidal mind and brain: a review of neuropsychological and neuroimaging studies. World J Biol Psychiatry 2011; 12: 319–339.

    Article  PubMed  Google Scholar 

  2. Richard-Devantoy S, Berlim MT, Jollant F . A meta-analysis of neuropsychological markers of vulnerability to suicidal behavior in mood disorders. Psychol Med 2014; 44: 1663–1674.

    Article  CAS  PubMed  Google Scholar 

  3. Jollant F, Bellivier F, Leboyer M, Astruc B, Torres S, Verdier R et al. Impaired decision making in suicide attempters. Am J Psychiatry 2005; 162: 304–310.

    Article  PubMed  Google Scholar 

  4. Bergen H, Hawton K, Waters K, Ness J, Cooper J, Steeg S et al. How do methods of non-fatal self-harm relate to eventual suicide? J Affect Disord 2012; 136: 526–533.

    Article  PubMed  Google Scholar 

  5. Brent DA, Mann JJ . Family genetic studies, suicide, and suicidal behavior. Am J Med Genet C Semin Med Genet 2005; 133: 13–24.

    Article  Google Scholar 

  6. Turecki G, Brent DA . Suicide and suicidal behaviour. Lancet 2016; 387: 1227–1239.

    Article  PubMed  Google Scholar 

  7. McGirr A, Alda M, Seguin M, Cabot S, Lesage A, Turecki G . Familial aggregation of suicide explained by cluster B traits: a three-group family study of suicide controlling for major depressive disorder. Am J Psychiatry 2009; 166: 1124–1134.

    Article  PubMed  Google Scholar 

  8. Tuvblad C, Gao Y, Wang P, Raine A, Botwick T, Baker LA . The genetic and environmental etiology of decision-making: a longitudinal twin study. J Adolesc 2013; 36: 245–255.

    Article  PubMed  Google Scholar 

  9. Lovallo WR, Yechiam E, Sorocco KH, Vincent AS, Collins FL . Working memory and decision-making biases in young adults with a family history of alcoholism: studies from the Oklahoma family health patterns project. Alcohol Clin Exp Res 2006; 30: 763–773.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Cavedini P, Zorzi C, Piccinni M, Cavallini MC, Bellodi L . Executive dysfunctions in obsessive-compulsive patients and unaffected relatives: searching for a new intermediate phenotype. Biol Psychiatry 2010; 67: 1178–1184.

    Article  PubMed  Google Scholar 

  11. Hoehne A, Richard-Devantoy S, Ding Y, Turecki G, Jollant F . First-degree relatives of suicide completers may have impaired decision-making but functional cognitive control. J Psychiatr Res 2015; 68: 192–197.

    Article  CAS  PubMed  Google Scholar 

  12. Lawrence NS, Jollant F, O’Daly O, Zelaya F, Phillips ML . Distinct roles of prefrontal cortical subregions in the Iowa Gambling Task. Cereb Cortex 2009; 19: 1134–1143.

    Article  PubMed  Google Scholar 

  13. Jollant F, Lawrence NS, Olie E, O’Daly O, Malafosse A, Courtet P et al. Decreased activation of lateral orbitofrontal cortex during risky choices under uncertainty is associated with disadvantageous decision-making and suicidal behavior. Neuroimage 2010; 51: 1275–1281.

    Article  PubMed  Google Scholar 

  14. Olié E, Ding Y, Le Bars E, de Champfleur NM, Mura T, Bonafé A et al. Processing of decision-making and social threat in patients with history of suicidal attempt: A neuroimaging replication study. Psychiatry Res 2015; 234: 369–377.

    Article  PubMed  Google Scholar 

  15. Dombrovski AY, Szanto K, Clark L, Reynolds CF, Siegle GJ . Reward Signals, Attempted Suicide, and Impulsivity in Late-Life Depression. JAMA Psychiatry 2013; 70: 1.

    Article  PubMed  Google Scholar 

  16. Jollant F, Lawrence NS, Giampietro V, Brammer MJ, Fullana MA, Drapier D et al. Orbitofrontal cortex response to angry faces in men with histories of suicide attempts. Am J Psychiatry 2008; 165: 740–748.

    Article  PubMed  Google Scholar 

  17. First MB, Spitzer RL, Gibbon M, Williams JBW . Structured Clinical Interview for DSM-IV Axis I Disorders, Clinician Version (SCID-CV). American Psychiatric Press, Inc: Washington, DC, 1996.

  18. Hamilton M . A rating scale for depression. J Neurol Neurosurg Psychiatry 1960; 23: 56–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Oldfield RC . The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971; 9: 97–113.

    Article  CAS  PubMed  Google Scholar 

  20. First MB, Gibbon M, Spitzer RL, Williams JBW, Benjamin LS . Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II). Biometrics Research Department, New York State Psychiatric Institute: New York, USA, 1997.

    Google Scholar 

  21. Beck AT, Ward CH, Mendelson M . An inventory for measuring depression. Arch Gen Psychiatry 4: 561–571 1961.

    Article  CAS  PubMed  Google Scholar 

  22. Spielberger CD . Manual for the State-Trait Anxiety Inventory (Form Y). Consulting Psychologists Press: Palo Alto, CA, USA, 1983.

    Google Scholar 

  23. Buss AH, Durkee A . An inventory for assessing different kinds of hostility. J Consult Psychol 1957; 21: 343–349.

    Article  CAS  PubMed  Google Scholar 

  24. Brown GL, Ebert MH, Goyer PF, Jimerson DC, Klein WJ, Bunney WE et al. Aggression, suicide, and serotonin: relationships to CSF amine metabolites. Am J Psychiatry 1982; 139: 741–746.

    Article  CAS  PubMed  Google Scholar 

  25. Patton JH, Stanford MS, Barratt ES . Factor structure of the Barratt impulsiveness scale. J Clin Psychol 1995; 51: 768–774.

    Article  CAS  PubMed  Google Scholar 

  26. Mackinnon A, Ritchie K, Mulligan R . The measurement properties of a French language adaptation of the National Adult Reading Test. Int J Methods Psychiatr Res 1999; 8: 27–38.

    Article  Google Scholar 

  27. Bechara A, Damasio H, Damasio AR, Lee GP . Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 1999; 19: 5473–5481.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Iglesias JE, Liu CY, Thompson PM, TUZ . Robust brain extraction across datasets and comparison with publicly avalable methods. IEEE Trans Med Imaging 2011; 30: 1617–1634.

    Article  PubMed  Google Scholar 

  29. Pereira FR, Alessio A, Sercheli MS, Pedro T, Bilevicius E, Rondina JM et al. Asymetricla hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI. BMC Neurosci 2010; 11: 66.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Cox RW . AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 1996; 29: 162–173.

    Article  CAS  PubMed  Google Scholar 

  31. Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM . FSL. Neuroimage 2012; 62: 782–790.

    Article  PubMed  Google Scholar 

  32. Richard-Devantoy S, Ding Y, Lepage M, Turecki G, Jollant F . Cognitive inhibition in depression and suicidal behavior: a neuroimaging study. Psychol Med 2016; 46: 933–944.

    Article  CAS  PubMed  Google Scholar 

  33. Ward BD . Simultaneous inference for fMRI data. Medical College of Wisconsin: Milwaukee, Wissconsin, 2000.

    Google Scholar 

  34. Mackey S, Petrides M . Architecture and morphology of the human ventromedial prefrontal cortex. Eur J Neurosci 2014; 40: 2777–2796.

    Article  PubMed  Google Scholar 

  35. Wallis JD . Orbitofrontal cortex and its contribution to decision-making. Annu Rev Neurosci 2007; 30: 31–56.

    Article  CAS  PubMed  Google Scholar 

  36. Grabenhorst F, Rolls ET . Value, pleasure and choice in the ventral prefrontal cortex. Trends Cogn Sci 2011; 15: 56–67.

    Article  PubMed  Google Scholar 

  37. Mar AC, Walker AL, Theobald DE, Eagle DM, Robbins TW . Dissociable effects of lesions to orbitofrontal cortex subregions on impulsive choice in the rat. J Neurosci 2011; 31: 6398–6404.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Carmichael ST, Price JL . Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 1994; 346: 366–402.

    Article  CAS  PubMed  Google Scholar 

  39. O’Doherty J, Kringelbach ML, Rolls ET, Hornak J, Andrews C . Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 2001; 4: 95–102.

    Article  PubMed  Google Scholar 

  40. McClure SM, Laibson DI, Loewenstein G, Cohen JD . Separate neural systems value immediate and delayed monetary rewards. Science 2004; 306: 503–507.

    Article  CAS  PubMed  Google Scholar 

  41. Kouneiher F, Charron S, Koechlin E . Motivation and cognitive control in the human prefrontal cortex. Nat Neurosci 2009; 12: 939–945.

    Article  CAS  PubMed  Google Scholar 

  42. Dixon ML, Christoff K . The lateral prefrontal cortex and complex value-based learning and decision making. Neurosci Biobehav Rev 2014; 45C: 9–18.

    Article  Google Scholar 

Download references

Acknowledgements

This study was funded thanks to a grant from the American Foundation for Suicide Prevention to Dr F. Jollant. M. Y. Ding held a Fond de Recherche du Québec—Santé (FRQS) Ph.D. Grant # 24117 and Dr. F Jollant a FRQS 'chercheur-boursier clinicien' salary grant during this study. The sponsors had no role in the design, data analyses or manuscript writing. We thank Mrs Annukka Jäkälä for data collection. Preliminary results from this study have been presented at the Society of Biological Psychiatry’s 69th Annual Meeting in New York on 9 May 2014.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F Jollant.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Additional information

Supplementary Information accompanies the paper on the Molecular Psychiatry website

Supplementary information

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ding, Y., Pereira, F., Hoehne, A. et al. Altered brain processing of decision-making in healthy first-degree biological relatives of suicide completers. Mol Psychiatry 22, 1149–1154 (2017). https://doi.org/10.1038/mp.2016.221

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/mp.2016.221

This article is cited by

Search

Quick links