Prefrontal activation in suicide attempters during decision making with emotional feedback

AdriáN Alacreu-Crespo,Emmanuelle Le Bars,Jérémy Deverdun,Emilie Olié,Philippe Courtet,Fabienne Cyprien

doi:10.1038/s41398-020-00995-z

Abstract

Emotional feedback, such as faces showing emotions, can influence decision making. Decision making and emotional face processing, mainly mediated by the prefrontal and cingulate cortices, are impaired in suicide attempters. Here, we used functional MRI (fMRI) to study prefrontal activation in suicide attempters during a modified version of the Iowa Gambling Task (IGT) that included emotional face feedback. We randomly distributed the 116 euthymic women (n = 45 suicide attempters, n = 41 affective controls with history of depression without suicide attempt, and n = 30 healthy controls) included in the study in three emotional IGT groups: concordant (safe and risky choices followed by happy and angry faces, respectively), discordant (safe and risky choices followed by angry and happy faces, respectively), and neutral condition (safe and risky choices followed by neutral faces). Considering the two IGT phases (ambiguous and risky), we then analyzed five regions of interest during the risky vs. safe choices: orbitofrontal (OFC), anterior cingulate (ACC), ventrolateral (VLPFC), medial (MPFC) and dorsal prefrontal (DPFC) cortices. We found: (1) impaired decision making and increased DPFC and OFC activation in suicide attempters vs. controls in the discordant condition during the risky phase; (2) reduced VLPFC activation in suicide attempters in the concordant condition during the ambiguous phase; and (3) decreased OFC, ACC and DPFC activation in both control groups in the concordant condition during the ambiguous phase. Suicide attempters showed prefrontal alterations during reward-learning decision making with emotional feedback. Suicide attempters may guide their decisions to avoid social negative feedback despite the expected outcome.

Highlights

Suicidal acts may be viewed as the outcome of dysfunctional decision making
Several studies that used the Iowa Gambling Task (IGT)[2] found that decision making is impaired in subjects with history of suicidal acts, but not suicidal ideation[3,4,5,6,7,8,9,10]
In our modified version of the IGT, emotional feedback was added between the choice and the monetary feedback to create three different feedback conditions: concordant, discordant, and neutral condition independently of the monetary gains or losses

Summary

Introduction

Suicidal acts may be viewed as the outcome of dysfunctional decision making. In a phenomenological qualitative analysis that included eight suicide attempters, Bergman et al.[1] reported a precarious decision-making state about their own life and destiny. Several studies that used the Iowa Gambling Task (IGT)[2] found that decision making is impaired in subjects with history of suicidal acts, but not suicidal ideation[3,4,5,6,7,8,9,10]. IGT is a decision-making task that involves value-based learning and presents two degrees of uncertainty: an ambiguous phase when subjects cannot estimate the outcome (first 40 trials), and a risky phase when subjects can better estimate the possible outcome (last 60 trials)[12,13]. Compared with patients without history of suicide attempt, decision-making is impaired in the risky phase of the IGT in suicide attempters[4,7,8,9,10]

Methods

Results

Conclusion