Paralimbic and lateral prefrontal encoding of reward value during intertemporal choice in attempted suicide

Abstract

Background: Alongside impulsive suicide attempts, clinicians encounter highly premeditated suicidal acts, particularly in older adults. We have previously found that in contrast to the more impulsive suicide attempters' inability to delay gratification, serious and highly planned suicide attempts were associated with greater willingness to wait for larger rewards. This study examined neural underpinnings of intertemporal preference in suicide attempters. We expected that impulsivity and suicide attempts, particularly poorly planned ones, would predict altered paralimbic subjective value representations. We also examined lateral prefrontal and paralimbic correlates of premeditation in suicidal behavior.

Method: A total of 48 participants aged 46-90 years underwent extensive clinical and cognitive characterization and completed the delay discounting task in the scanner: 26 individuals with major depression (13 with and 13 without history of suicide attempts) and 22 healthy controls.

Results: More impulsive individuals displayed greater activation in the precuneus/posterior cingulate cortex (PCC) to value difference favoring the delayed option. Suicide attempts, particularly better-planned ones, were associated with deactivation of the lateral prefrontal cortex (lPFC) in response to value difference favoring the immediate option. Findings were robust to medication exposure, depression severity and possible brain damage from suicide attempts, among other confounders. Finally, in suicide attempters longer reward delays were associated with diminished parahippocampal responses.

Conclusions: Impulsivity was associated with an altered paralimbic (precuneus/PCC) encoding of value difference during intertemporal choice. By contrast, better-planned suicidal acts were associated with altered lPFC representations of value difference. The study provides preliminary evidence of impaired decision processes in both impulsive and premeditated suicidal behavior.

Keywords: Aging; discounting; impulsivity; neuroimaging; suicide.

Figure 1

Illustration of the incremental narrowing of the interval for SIR choice as a function of participant’s choices.

Figure 2

Panel A shows the BOLD response in the whole sample to value difference in the precuneus (BA7)/posterior cingulate cortex (PCC [BA30–31]) at p_voxelwise < .001, p_corr < .05 (MNI coordinates: −1, −61, 30; cluster volume = 28764 mm³; peak t[47] = −6.66). Panel B shows that the history of suicide attempts predicted a diminished response of the left dorsolateral prefrontal cortex (BA 9) to the increasing value difference favoring smaller immediate reward. (MNI coordinates: −48, 10, 35; cluster volume = 1107 mm³; peak t[44] = −4.60). These findings held when the data were analyzed using an alternate model of value difference (see Supplemental results for more details).

Figure 2

Panel A shows the BOLD response in the whole sample to value difference in the precuneus (BA7)/posterior cingulate cortex (PCC [BA30–31]) at p_voxelwise < .001, p_corr < .05 (MNI coordinates: −1, −61, 30; cluster volume = 28764 mm³; peak t[47] = −6.66). Panel B shows that the history of suicide attempts predicted a diminished response of the left dorsolateral prefrontal cortex (BA 9) to the increasing value difference favoring smaller immediate reward. (MNI coordinates: −48, 10, 35; cluster volume = 1107 mm³; peak t[44] = −4.60). These findings held when the data were analyzed using an alternate model of value difference (see Supplemental results for more details).

Figure 3

Panel A illustrates the correlation between SIS-planning and activity in the left dorsolateral prefrontal cortex (BA 9) derived from the value difference map. Panel B illustrates the correlation between Impulsive/careless subscale scores on Social Problem Solving scale and activity in the precuneus derived from the value difference map.

Figure 3

Panel A illustrates the correlation between SIS-planning and activity in the left dorsolateral prefrontal cortex (BA 9) derived from the value difference map. Panel B illustrates the correlation between Impulsive/careless subscale scores on Social Problem Solving scale and activity in the precuneus derived from the value difference map.