Hostname: page-component-745bb68f8f-s22k5 Total loading time: 0 Render date: 2025-01-14T05:53:53.648Z Has data issue: false hasContentIssue false
  • English
  • Français

The temptation of suicide: striatal gray matter, discounting of delayed rewards, and suicide attempts in late-life depression

Published online by Cambridge University Press:  17 October 2011

A. Y. Dombrovski ,
G. J. Siegle ,
K. Szanto ,
L. Clark ,
C. F. Reynolds 3rd  and
H. Aizenstein
A. Y. Dombrovski*
Affiliation:
Western Psychiatric Institute and Clinic, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
G. J. Siegle
Affiliation:
Western Psychiatric Institute and Clinic, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
K. Szanto
Affiliation:
Western Psychiatric Institute and Clinic, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
L. Clark
Affiliation:
Behavioural and Clinical Neuroscience Institute, Department of Experimental Psychology, University of Cambridge, UK
C. F. Reynolds 3rd
Affiliation:
Western Psychiatric Institute and Clinic, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
H. Aizenstein
Affiliation:
Western Psychiatric Institute and Clinic, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
*
*Address for correspondence: A. Y. Dombrovski, M. D., Western Psychiatric Institute and Clinic, 100 N Bellefield Ave, Pittsburgh, PA 15213, USA. (Email: dombrovskia@upmc.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Converging evidence implicates basal ganglia alterations in impulsivity and suicidal behavior. For example, D2/D3 agonists and subthalamic nucleus stimulation in Parkinson's disease (PD) trigger impulse control disorders and possibly suicidal behavior. Furthermore, suicidal behavior has been associated with structural basal ganglia abnormalities. Finally, low-lethality, unplanned suicide attempts are associated with increased discounting of delayed rewards, a behavior dependent upon the striatum. Thus, we tested whether, in late-life depression, changes in the basal ganglia were associated with suicide attempts and with increased delay discounting.

Method

Fifty-two persons aged ⩾60 years underwent extensive clinical and cognitive characterization: 33 with major depression [13 suicide attempters (SA), 20 non-suicidal depressed elderly] and 19 non-depressed controls. Participants had high-resolution T1-weighted magnetization prepared rapid acquisition gradient–echo (MPRAGE) magnetic resonance imaging (MRI) scans. Basal ganglia gray matter voxel counts were estimated using atlas-based segmentation, with a highly deformable automated algorithm. Discounting of delayed rewards was assessed using the Monetary Choice Questionnaire (MCQ) and delay aversion with the Cambridge Gamble Task (CGT).

Results

SA had lower putamen but not caudate or pallidum gray matter voxel counts, compared to the control groups. This difference persisted after accounting for substance use disorders and possible brain injury from suicide attempts. SA with lower putamen gray matter voxel counts displayed higher delay discounting but not delay aversion. Secondary analyses revealed that SA had lower voxel counts in associative and ventral but not sensorimotor striatum.

Conclusions

Our findings, although limited by small sample size and the case–control design, suggest that striatal lesions could contribute to suicidal behavior by increasing impulsivity.

Keywords

Basal gangliacorpus striatumdecision makingglobus pallidusputamenrewardsuicide
Type
Original Articles
Information
Psychological Medicine , Volume 42 , Issue 6 , June 2012 , pp. 1203 - 1215
Copyright
Copyright © Cambridge University Press 2011

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

Ahearn, EP, Jamison, KR, Steffens, DC, Cassidy, F, Provenzale, JM, Lehman, A, Weisler, RH, Carroll, BJ, Krishnan, KR (2001). MRI correlates of suicide attempt history in unipolar depression. Biological Psychiatry 50, 266–270.CrossRefGoogle ScholarPubMed
Arango, V, Underwood, MD, Mann, JJ (1997). Postmortem findings in suicide victims. Implications for in vivo imaging studies. Annals of the New York Academy of Sciences 836, 269–287.CrossRefGoogle ScholarPubMed
Beautrais, AL (2002). A case control study of suicide and attempted suicide in older adults. Suicide and Life-Threatening Behavior 32, 1–9.CrossRefGoogle ScholarPubMed
Beck, AT, Beck, R, Kovacs, M (1975). Classification of suicidal behaviors: I. Quantifying intent and medical lethality. American Jounal of Psychiatry 132, 285–287.Google ScholarPubMed
Beck, AT, Kovacs, M, Weissman, A (1979). Assessment of suicidal intention: the Scale for Suicide Ideation. Journal of Consulting and Clinical Psychology 47, 343–352.CrossRefGoogle ScholarPubMed
Beck, AT, Shuyler, D, Herman, I (1974). Development of suicidal intent scales. In The Prediction of Suicide (ed. Beck, A. T., Resnik, H. L. P. and Lettieri, D. J.), pp. 45–56. Charles Press: Bowie, MD.Google Scholar
Cardinal, RN, Pennicott, DR, Sugathapala, CL, Robbins, TW, Everitt, BJ (2001). Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science 292, 2499–2501.CrossRefGoogle ScholarPubMed
Chen, M, Kanade, T, Pomerleau, D, Schneider, J (1999). 3-D deformable registration of medical images using a statistical atlas. In Medical Image Computing and Computer-Assisted Intervention – MICCAI'99 (ed. Taylor, C. and Colchester, A.), pp. 621–630. Springer: Berlin.Google Scholar
Clark, L, Dombrovski, AY, Siegle, GJ, Butters, MA, Shollenberger, CL, Sahakian, BJ, Szanto, K (2011). Impairment in risk-sensitive decision-making in older suicide attempters with depression. Psychology and Aging 26, 321–330.CrossRefGoogle ScholarPubMed
Cohen, J, Cohen, P (1983). Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences. Erlbaum: Hillsdale, NJ.Google Scholar
Conwell, Y, Lyness, JM, Duberstein, P, Cox, C, Seidlitz, L, DiGiorgio, A, Caine, ED (2000). Completed suicide among older patients in primary care practices: a controlled study. Journal of the American Geriatrics Society 48, 23–29.CrossRefGoogle ScholarPubMed
Davatzikos, C, Resnick, SM (2002). Degenerative age changes in white matter connectivity visualized in vivo using magnetic resonance imaging. Cerebral Cortex 12, 767–771.CrossRefGoogle ScholarPubMed
Deakin, J, Aitken, M, Robbins, T, Sahakian, BJ (2004). Risk taking during decision-making in normal volunteers changes with age. Journal of the International Neuropsychological Society 10, 590–598.CrossRefGoogle ScholarPubMed
Di Maio, L, Squitieri, F, Napolitano, G, Campanella, G, Trofatter, JA, Conneally, PM (1993). Suicide risk in Huntington's disease. Journal of Medical Genetics 30, 293–295.CrossRefGoogle ScholarPubMed
Dombrovski, AY, Clark, L, Siegle, GJ, Butters, MA, Ichikawa, N, Sahakian, BJ, Szanto, K (2010). Reward/punishment reversal learning in older suicide attempters. American Journal of Psychiatry 167, 699–707.CrossRefGoogle ScholarPubMed
Dombrovski, AY, Szanto, K, Siegle, GJ, Wallace, ML, Forman, SD, Sahakian, B, Reynolds, CF 3rd, Clark, L (2011). Lethal forethought: delayed reward discounting differentiates high- and low-lethality suicide attempts in old age. Biological Psychiatry 70, 138–144.CrossRefGoogle ScholarPubMed
Epstein, LH, Richards, JB, Saad, FG, Paluch, RA, Roemmich, JN, Lerman, C (2003). Comparison between two measures of delay discounting in smokers. Experimental and Clinical Psychopharmacology 11, 131–138.CrossRefGoogle ScholarPubMed
Ernst, C, Mechawar, N, Turecki, G (2009). Suicide neurobiology. Progress in Neurobiology 89, 315–333.CrossRefGoogle ScholarPubMed
Folstein, MF, Folstein, SE, McHugh, PR (1975). ‘Mini-mental state’. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 12, 189–198.CrossRefGoogle Scholar
Foncke, EM, Schuurman, PR, Speelman, JD (2006). Suicide after deep brain stimulation of the internal globus pallidus for dystonia. Neurology 66, 142–143.CrossRefGoogle ScholarPubMed
Frank, MJ, Samanta, J, Moustafa, AA, Sherman, SJ (2007 a). Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science 318, 1309–1312.CrossRefGoogle ScholarPubMed
Frank, MJ, Scheres, A, Sherman, SJ (2007 b). Understanding decision-making deficits in neurological conditions: insights from models of natural action selection. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 362, 1641–1654.CrossRefGoogle ScholarPubMed
Green, L, Myerson, J, Ostaszewski, P (1999). Discounting of delayed rewards across the life span: age differences in individual discounting functions. Behavioural Processes 46, 89–96.CrossRefGoogle ScholarPubMed
Haber, SN, Kim, KS, Mailly, P, Calzavara, R (2006). Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. Journal of Neuroscience 26, 8368–8376.CrossRefGoogle ScholarPubMed
Haber, SN, Knutson, B (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26.CrossRefGoogle ScholarPubMed
Haber, SN, Kunishio, K, Mizobuchi, M, Lyndbalta, E (1995). The orbital and medial prefrontal circuit through the primate basal ganglia. Journal of Neuroscience 15, 4851–4867.CrossRefGoogle ScholarPubMed
Halbig, TD, Tse, W, Frisina, PG, Baker, BR, Hollander, E, Shapiro, H, Tagliati, M, Koller, WC, Olanow, CW (2009). Subthalamic deep brain stimulation and impulse control in Parkinson's disease. European Journal of Neurology 16, 493–497.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Hariri, AR, Brown, SM, Williamson, DE, Flory, JD, de Wit, H, Manuck, SB (2006). Preference for immediate over delayed rewards is associated with magnitude of ventral striatal activity. Journal of Neuroscience 26, 13213–13217.CrossRefGoogle ScholarPubMed
Housden, CR, O'Sullivan, SS, Joyce, EM, Lees, AJ, Roiser, JP (2010). Intact reward learning but elevated delay discounting in Parkinson's disease patients with impulsive-compulsive spectrum behaviors. Neuropsychopharmacology 35, 2155–2164.CrossRefGoogle ScholarPubMed
Jollant, F, Bellivier, F, Leboyer, M, Astruc, B, Torres, S, Verdier, R, Castelnau, D, Malafosse, A, Courtet, P (2005). Impaired decision making in suicide attempters. American Journal of Psychiatry 162, 304–310.CrossRefGoogle ScholarPubMed
Jollant, F, Lawrence, NS, Giampietro, V, Brammer, MJ, Fullana, MA, Drapier, D, Courtet, P, Phillips, ML (2008). Orbitofrontal cortex response to angry faces in men with histories of suicide attempts. American Journal of Psychiatry 165, 740–748.CrossRefGoogle ScholarPubMed
Jollant, F, Lawrence, NS, Olie, E, O'Daly, O, Malafosse, A, Courtet, P, Phillips, ML (2010). Decreased activation of lateral orbitofrontal cortex during risky choices under uncertainty is associated with disadvantageous decision-making and suicidal behavior. NeuroImage 51, 1275–1281.CrossRefGoogle ScholarPubMed
Kable, JW, Glimcher, PW (2007). The neural correlates of subjective value during intertemporal choice. Nature Neuroscience 10, 1625–1633.CrossRefGoogle ScholarPubMed
Kirby, KN, Petry, NM, Bickel, WK (1999). Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. Journal of Experimental Psychology: General 128, 78–87.CrossRefGoogle ScholarPubMed
Luo, S, Ainslie, G, Giragosian, L, Monterosso, JR (2009). Behavioral and neural evidence of incentive bias for immediate rewards relative to preference-matched delayed rewards. Journal of Neuroscience 29, 14820–14827.CrossRefGoogle ScholarPubMed
Mai, JK, Assheuer, J, Paxinos, P (1997). Atlas of the Human Brain. Academic Press: San Diego, CA.Google Scholar
Martinez, D, Slifstein, M, Broft, A, Mawlawi, O, Hwang, DR, Huang, Y, Cooper, T, Kegeles, L, Zarahn, E, Abi-Dargham, A, Haber, SN, Laruelle, M (2003). Imaging human mesolimbic dopamine transmission with positron emission tomography. Part II: Amphetamine-induced dopamine release in the functional subdivisions of the striatum. Journal of Cerebral Blood Flow and Metabolism 23, 285–300.CrossRefGoogle ScholarPubMed
Mattis, S (1988). Dementia Rating Scale (DRS): Professional Manual. Psychological Assessment Resources: Odessa, FL.Google Scholar
McClure, SM, Laibson, DI, Loewenstein, G, Cohen, JD (2004). Separate neural systems value immediate and delayed monetary rewards. Science 306, 503–507.CrossRefGoogle ScholarPubMed
McGirr, A, Alda, M, Seguin, M, Cabot, S, Lesage, A, Turecki, G (2009). Familial aggregation of suicide explained by cluster B traits: a three-group family study of suicide controlling for major depressive disorder. American Journal of Psychiatry 166, 1124–1134.CrossRefGoogle ScholarPubMed
Middleton, FA, Strick, PL (2000). Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies. Brain and Cognition 42, 183–200.CrossRefGoogle ScholarPubMed
Miller, MD, Paradis, CF, Houck, PR, Mazumdar, S, Stack, JA, Rifai, AH, Mulsant, B, Reynolds, CF 3rd (1992). Rating chronic medical illness burden in geropsychiatric practice and research: application of the Cumulative Illness Rating Scale. Psychiatry Research 41, 237–248.CrossRefGoogle ScholarPubMed
Monkul, ES, Hatch, JP, Nicoletti, MA, Spence, S, Brambilla, P, Lacerda, AL, Sassi, RB, Mallinger, AG, Keshavan, MS, Soares, JC (2007). Fronto-limbic brain structures in suicidal and non-suicidal female patients with major depressive disorder. Molecular Psychiatry 12, 360–366.CrossRefGoogle ScholarPubMed
Muranishi, M, Inokawa, H, Yamada, H, Ueda, Y, Matsumoto, N, Nakagawa, M, Kimura, M (2011). Inactivation of the putamen selectively impairs reward history-based action selection. Experimental Brain Research 209, 235–246.CrossRefGoogle ScholarPubMed
O'Carroll, PW, Berman, AL, Maris, RW, Moscicki, EK, Tanney, BL, Silverman, MM (1996). Beyond the Tower of Babel: a nomenclature for suicidology. Suicide and Life-Threatening Behavior 26, 237–252.CrossRefGoogle Scholar
Owen, AM, Roberts, AC, Hodges, JR, Summers, BA, Polkey, CE, Robbins, TW (1993). Contrasting mechanisms of impaired attentional set-shifting in patients with frontal lobe damage or Parkinson's disease. Brain 116, 1159–1175.CrossRefGoogle ScholarPubMed
Rangel, A, Camerer, C, Montague, PR (2008). A framework for studying the neurobiology of value-based decision making. Nature Reviews Neuroscience 9, 545–556.CrossRefGoogle ScholarPubMed
Raz, N, Lindenberger, U, Rodrigue, KM, Kennedy, KM, Head, D, Williamson, A, Dahle, C, Gerstorf, D, Acker, JD (2005). Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cerebral Cortex 15, 1676–1689.CrossRefGoogle ScholarPubMed
Raz, N, Rodrigue, KM (2006). Differential aging of the brain: patterns, cognitive correlates and modifiers. Neuroscience and Biobehavioral Reviews 30, 730–748.CrossRefGoogle ScholarPubMed
Rosano, C, Aizenstein, HJ, Studenski, S, Newman, AB (2007). A regions-of-interest volumetric analysis of mobility limitations in community-dwelling older adults. Journals of Geronology Series A: Biological Sciences and Medical Sciences 62, 1048–1055.CrossRefGoogle ScholarPubMed
Russchen, FT, Bakst, I, Amaral, DG, Price, JL (1985). The amygdalostriatal projections in the monkey. An anterograde tracing study. Brain Research 329, 241–257.CrossRefGoogle ScholarPubMed
Sackeim, HA (2001). The definition and meaning of treatment-resistant depression. Journal of Clinical Psychiatry 62 (Suppl. 16), 10–17.Google ScholarPubMed
Smith, SM (2002). Fast robust automated brain extraction. Human Brain Mapping 17, 143–155.CrossRefGoogle ScholarPubMed
Stenager, EN, Wermuth, L, Stenager, E, Boldsen, J (1994). Suicide in patients with Parkinson's disease. An epidemiological study. Acta Psychiatrica Scandinavica 90, 70–72.CrossRefGoogle ScholarPubMed
Todes, CJ, Lees, AJ (1985). The pre-morbid personality of patients with Parkinson's disease. Journal of Neurology, Neurosurgery, and Psychiatry 48, 97–100.CrossRefGoogle ScholarPubMed
Trautner, RJ, Cummings, JL, Read, SL, Benson, DF (1988). Idiopathic basal ganglia calcification and organic mood disorder. American Journal of Psychiatry 145, 350–353.Google ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273–289.CrossRefGoogle ScholarPubMed
van Heeringen, C, Bijttebier, S, Godfrin, K (2011). Suicidal brains: a review of functional and structural brain studies in association with suicidal behaviour. Neuroscience and Biobehavioral Reviews 35, 688–698.CrossRefGoogle ScholarPubMed
Vang, FJ, Ryding, E, Träskman-Bendz, L, van Westen, D, Lindström, MB (2010). Size of basal ganglia in suicide attempters, and its association with temperament and serotonin transporter density. Psychiatry Research: Neuroimaging 183, 177–179.CrossRefGoogle ScholarPubMed
Voon, V, Krack, P, Lang, AE, Lozano, AM, Dujardin, K, Schupbach, M, D'Ambrosia, J, Thobois, S, Tamma, F, Herzog, J, Speelman, JD, Samanta, J, Kubu, C, Rossignol, H, Poon, YY, Saint-Cyr, JA, Ardouin, C, Moro, E (2008). A multicentre study on suicide outcomes following subthalamic stimulation for Parkinson's disease. Brain 131, 2720–2728.CrossRefGoogle ScholarPubMed
Voon, V, Reynolds, B, Brezing, C, Gallea, C, Skaljic, M, Ekanayake, V, Fernandez, H, Potenza, MN, Dolan, RJ, Hallett, M (2010). Impulsive choice and response in dopamine agonist-related impulse control behaviors. Psychopharmacology (Berlin) 207, 645–659.CrossRefGoogle ScholarPubMed
Voon, V, Thomsen, T, Miyasaki, JM, de Souza, M, Shafro, A, Fox, SH, Duff-Canning, S, Lang, AE, Zurowski, M (2007). Factors associated with dopaminergic drug-related pathological gambling in Parkinson disease. Archives of Neurology 64, 212–216.CrossRefGoogle ScholarPubMed
Waern, M, Runeson, BS, Allebeck, P, Beskow, J, Rubenowitz, E, Skoog, I, Wilhelmsson, K (2002). Mental disorder in elderly suicides: a case-control study. American Journal of Psychiatry 159, 450–455.CrossRefGoogle ScholarPubMed
Wagner, G, Koch, K, Schachtzabel, C, Schultz, CC, Sauer, H, Schlösser, RG (2011). Structural brain alterations in patients with major depressive disorder and high risk for suicide: evidence for a distinct neurobiological entity? NeuroImage 54, 1607–1614.CrossRefGoogle ScholarPubMed
Weintraub, D, Koester, J, Potenza, MN, Siderowf, AD, Stacy, M, Voon, V, Whetteckey, J, Wunderlich, GR, Lang, AE (2010). Impulse control disorders in Parkinson disease: a cross-sectional study of 3090 patients. Archives of Neurology 67, 589–595.CrossRefGoogle ScholarPubMed
Weintraub, D, Siderowf, AD, Potenza, MN, Goveas, J, Morales, KH, Duda, JE, Moberg, PJ, Stern, MB (2006). Association of dopamine agonist use with impulse control disorders in Parkinson disease. Archives of Neurology 63, 969–973.CrossRefGoogle ScholarPubMed
Woods, RP, Grafton, ST, Watson, JD, Sicotte, NL, Mazziotta, JC (1998). Automated image registration: II. Intersubject validation of linear and nonlinear models. Journal of Computer Assisted Tomography 22, 153–165.CrossRefGoogle ScholarPubMed
Wu, M, Carmichael, O, Lopez-Garcia, P, Carter, CS, Aizenstein, HJ (2006). Quantitative comparison of AIR, SPM, and the fully deformable model for atlas-based segmentation of functional and structural MR images. Human Brain Mapping 27, 747–754.CrossRefGoogle ScholarPubMed
Wu, M, Rosano, C, Aizenstein, HJ (2005). A morphological method to improve skull stripping of MR brain images. Paper presented at the Human Brain Mapping Conference, Toronto, Canada, 2005.Google Scholar
Yoo, TS (ed.) (2004). Insight into Images: Principles and Practice for Segmentation, Registration, and Image Analysis. AK Peters Ltd: Wellesey, MA.Google Scholar