FundingThe work was funded by the Swedish Research Council, the Barbro and Bernard Osher Foundation, the Swedish Agency for Innovation Systems (VINNOVA), the Swedish Foundation for Strategic Research, the Jan Wallander and Tom Hedelius Foundation, the Swedish Council for Working Life and Social Research and the Knut and Alice Wallenberg Foundation and the Karolinska Institutet.

CitationLimbic Justice — Amygdala Involvement in Immediate Rejection in the Ultimate Game. Katarina Gospic, Erik Mohlin, Peter Fransson, Predrag Petrovic, Magnus Johannesson, Martin Ingvar. PLoS Biology 9(5): e1001054. doi:10.1371/journal.pbio.1001054
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Abstract

Imaging studies have revealed a putative neural account of emotional bias in decision making. However, it has been difficult in previous studies to identify the causal role of the different sub-regions involved in decision making. The Ultimatum Game (UG) is a game to study the punishment of norm-violating behavior. In a previous influential paper on UG it was suggested that frontal insular cortex has a pivotal role in the rejection response. This view has not been reconciled with a vast literature that attributes a crucial role in emotional decision making to a subcortical structure (i.e., amygdala). In this study we propose an anatomy-informed model that may join these views. We also present a design that detects the functional anatomical response to unfair proposals in a subcortical network that mediates rapid reactive responses. We used a functional MRI paradigm to study the early components of decision making and challenged our paradigm with the introduction of a pharmacological intervention to perturb the elicited behavioral and neural response. Benzodiazepine treatment decreased the rejection rate (from 37.6% to 19.0%) concomitantly with a diminished amygdala response to unfair proposals, and this in spite of an unchanged feeling of unfairness and unchanged insular response. In the control group, rejection was directly linked to an increase in amygdala activity. These results allow a functional anatomical detection of the early neural components of rejection associated with the initial reactive emotional response. Thus, the act of immediate rejection seems to be mediated by the limbic system and is not solely driven by cortical processes, as previously suggested. Our results also prompt an ethical discussion as we demonstrated that a commonly used drug influences core functions in the human brain that underlie individual autonomy and economic decision making.

Author Summary

It is well-established that emotions influence decision making. One way of studying this relationship is the Ultimatum Game, which has revealed that subjects punish unfair behavior in others in spite of receiving a concomitant economic loss. Previous brain imaging studies have suggested that this decision to punish involves complex cortical processing. However, punishment also involves an instant aggressive emotional response, a behavior often linked to subcortical structures such as the amygdala. In this study, we present a model that joins these views. We designed a paradigm that allows us to measure the activity of subcortical brain regions during decision making in the Ultimatum Game, while at the same time using a pharmacological approach that can suppress emotional responses and amygdala activity. The pharmacological treatment made subjects punish unfair behavior less, and decreased brain activity in the amygdala in response to unfair proposals, without changing the subjects' feeling of unfairness. In the control group, punishment was directly linked to an increase in amygdala activity. Thus, immediate punishment of unfair behavior involves the amygdala and is not solely driven by cortical processes, as previously suggested. Our results show that a commonly used drug influences autonomy and decision making, which may have ethical implications for its use.

Abbreviations: ACC, anterior cingulate cortex; dlPFC, dorsolateral prefrontal cortex; fMRI, functional MRI; mPFC, medial prefrontal cortex; RL, reinforcement learning; SEK, Swedish crowns; UG, Ultimatum Game.