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

Western Psychiatric Institute and Clinic, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA PA 15213, USA.
Psychological Medicine (Impact Factor: 5.94). 10/2011; 42(6):1203-15. DOI: 10.1017/S0033291711002133
Source: PubMed


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.
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).
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.
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.

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Available from: Alexandre Y Dombrovski
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    • "Similarly , suicidality of patients with major depressive disorder was negatively related to gray matter volumes in the putamen , but positively to impulsivity assessed with a DD task ( Dombrovski et al . , 2012 ) . Also , in substance abuse disorders , both decreased as well as increased gray matter volumes of the striatum have been reported ( e . g . , Potvin et al . , 2007 ; Barrós - Loscertales et al . , 2011 ) . Consequently , a recent meta - analysis concludes that the most robust findings in substance abuse concern frontal areas with no "
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    ABSTRACT: Time-stable personality traits, such as impulsivity and its relationship with functional and structural brain alterations, have gained much attention in the recent literature. Evidence from functional neuroimaging data implies an association between impulsivity and cortical as well as subcortical areas of the reward system. Discounting future rewards during impulsive decisions can be related to activation in the orbitofrontal cortex and striatum. Cortical structural changes in prefrontal regions have been found for introspective impulsivity measures. The present study focuses on brain regions associated with delay discounting to investigate structural manifestations of trait impulsivity. To test this, seventy subjects underwent structural magnetic resonance imaging (MRI) followed by a behavioral delay discounting task outside of the scanner to measure impulsivity with questions like: "Would you like to have 3€ immediately or 10€ in 5 days?". The amount of smaller-but-sooner decisions was calculated and used as a measure of behavioral impulsivity. Furthermore, we estimated subject's individual delay discounting parameter K reflecting the tendency to discount future rewards. Behaviorally, we found strong evidence in favor of a discounting utility model compared to a standard hyperbolic model of choice valuation. Neuronally, we focused on cortical and subcortical brain structure and investigated the association of behavioral impulsivity with delay discounting tendencies and gray matter volume. Voxel-based morphometric analyses showed positive correlations between delay discounting and gray matter volume in the striatum. Additional analyses using Freesurfer provided evidence for a positive correlation between delay discounting and gray matter volume of the caudate. Taken together, our study provides strong evidence for a structural manifestation of time-stable trait impulsivity in the human brain.
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    • "Volumes in the right caudate were also found to be reduced when the experimental sample aggregated patients with a familial history of a suicidal gesture with patients with a history of a suicide attempt in a single group considered to be at a high risk of suicide (Wagner et al. 2011). Elderly suicide attempters showed reduced voxel counts in the putamen (Dombrovski et al. 2012). Moreover, the thalamus has similarly been implicated in a neuroimaging study (Benedetti et al. 2011) and in a volumetric post-mortem study (Young et al. 2008). "
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    ABSTRACT: Previously, studies have demonstrated cortical impairments in those who complete or attempt suicide. Subcortical nuclei have less often been implicated in the suicidal vulnerability. In the present study, we investigated, with a specific design in a large population, variations in the volume of subcortical structures in patients with mood disorders who have attempted suicide. We recruited 253 participants: 73 suicide attempters with a past history of both mood disorders and suicidal act, 89 patient controls with a past history of mood disorders but no history of suicidal act, and 91 healthy controls. We collected 1.5 T magnetic resonance imaging data from the caudate, pallidum, putamen, nucleus accumbens, hippocampus, amygdala, ventral diencephalon, and thalamus. Surface-based morphometry (Freesurfer) analysis was used to comprehensively evaluate gray matter volumes. In comparison to controls, suicide attempters showed no difference in subcortical volumes when controlled for intracranial volume. However, within attempters negative correlations between the left (r = -0.35, p = 0.002), and right (r = -0.41, p < 0.0005) nucleus accumbens volumes and the lethality of the last suicidal act were found. Our study found no differences in the volume of eight subcortical nuclei between suicide attempters and controls, suggesting a lack of association between these regions and suicidal behavior in general. However, individual variations in nucleus accumbens structure and functioning may modulate the lethality of suicidal acts during a suicidal crisis. The known role of nucleus accumbens in action selection toward goals determined by the prefrontal cortex, decision-making or mental pain processing are hypothesized to be potential explanations.
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    • "Seven structural imaging studies were excluded because Talairach or MNI coordinates of identified anatomical structures were not reported (Monkul et al., 2007; Matsuo et al., 2010; Vang et al., 2010; Cyprien et al., 2011; Spoletini et al., 2011; Nery- Fernandes et al., 2012; Giakoumatos et al., 2013). Two studies were excluded because the study population consisted of elderly (Hwang et al., 2010; Dombrovski et al., 2012). Two additional studies were excluded because results for suicide attempters were not reported separately as attempters were regarded as part of a larger group of individuals considered at increased risk of suicide (Wagner et al., 2011, 2012). "
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