Cortical thickness of the dorsolateral prefrontal cortex predicts strategic choices in economic games

Human prosociality has been traditionally explained in the social sciences in terms of internalized social norms. Recent neuroscientific studies extended this traditional view of human prosociality by providing evidence that prosocial choices in economic games require cognitive control of the impulsive pursuit of self-interest. However, this view is challenged by an intuitive prosociality view emphasizing the spontaneous and heuristic basis of prosocial choices in economic games. We assessed the brain structure of 411 players of an ultimatum game (UG) and a dictator game (DG) and measured the strategic reasoning ability of 386. According to the reflective norm-enforcement view of prosociality, only those capable of strategically controlling their selfish impulses give a fair share in the UG, but cognitive control capability should not affect behavior in the DG. Conversely, we support the intuitive prosociality view by showing for the first time, to our knowledge, that strategic reasoning and cortical thickness of the dorsolateral prefrontal cortex were not related to giving in the UG but were negatively related to giving in the DG. This implies that the uncontrolled choice in the DG is prosocial rather than selfish, and those who have a thicker dorsolateral prefrontal cortex and are capable of strategic reasoning (goal-directed use of the theory of mind) control this intuitive drive for prosociality as a means to maximize reward when there are no future implications of choices.Humans are a cooperative species, and the question of why humans are so cooperative has been a subject of considerable interest in social and biological sciences (1–4). The traditional answer in the social sciences highlights critical roles of social norms and cultural values internalized as personal values and social preferences (5, 6). Recent neuroscientific studies of brain structure and activity extended this traditional view of human prosociality by showing that players of economic games act prosocially when they cognitively control selfish impulses (7–13). Experimental evidence shows that prosocial choices in economic games positively relate to local gray matter volume and thickness and the activation of brain areas that control selfish impulsive drives, such as the dorsolateral prefrontal cortex (DLPFC) and temporoparietal junction (TPJ) (7–9). Furthermore, impairment of cognitive control by disruption of DLPFC function prevents rejection of unfair offers in the ultimatum game (UG), which some authors considered prosocial and fairness-seeking behavior (10–13). Recently, this reflective view of human prosociality has been challenged by an alternative view emphasizing the intuitive nature of prosocial behavior, subsumed under intuitive prosociality (14) or heuristic cooperation (15–17). Support for the intuitive and automatic nature of prosocial behavior is provided by findings that prosocial choices are promoted under time pressure (15, 16, 18), under cognitive load (19–21), or after priming by successful experiences of intuitive decision making (15, 22). Also, participants who expressed more positive emotional words and less inhibitory words during and after an economic game cooperated more (23). Additionally, increased activity in the lateral prefrontal cortex was negatively related to fairness-seeking behavior in an economic game (24). According to the heuristic prosociality model (14–17), humans are predisposed to cooperate in social exchange situations. People fail to behave in a prosocial manner in social exchanges when this predisposition is overridden by strategic reasoning to secure their self-interest. By comparing participants’ behaviors in two economic games with brain structural differences and strategic reasoning abilities, we provide evidence that strategic reasoning controls, and thus reduces rather than promotes, game players’ prosocial behavior.The contrast between two simple, two-person economic games—namely, the dictator game (DG) and the UG—is often used to support the reflective prosocial model by demonstrating how strategic reasoning affects game players’ decisions. In both games, one player freely decides how much of a fixed reward to take and how much to leave for the other player. The difference between the two games is that the other player in the UG (termed “responder”) has the option to reject the decision made by the first player (termed “proposer”), causing both to earn nothing. This option is not provided to the second player in the DG, who plays the role of a “recipient”. The recipient simply receives whatever the first player (“dictator”) gives. The level of giving by the proposer in the UG is usually higher than that by the dictator in the DG (25). This is attributed to the proposer’s strategic reasoning, which requires inference of the recipient’s internal state and prediction of the resulting response (e.g., anger on the basis of unfair giving and subsequent rejection) (8, 9, 13). Given that neuroimaging and neuroendocrinological studies showed that negative emotions are associated with rejection of unfair offers (24, 26, 27), UG proposers may anticipate negative responses to unfair offers. UG proposers anticipate norm-enforcing responses (rejection of the offer) to norm-violating behavior (taking most of the reward) and strategically adjust giving behavior to secure acceptance by the responder. Thus, those capable of using strategic reasoning are expected to make fair offers in the UG compared with those who struggle to control their selfish drive for immediate reward.In contrast, in the DG, which requires no strategic reasoning to earn as much as possible, strategic control over selfish impulses is expected not to influence the player’s choices. Spitzer et al. (9) confirmed this by showing a positive correlation between the difference in giving in the UG and the DG (i.e., a measure of strategic reasoning) and activity of the right DLPFC and the lateral orbitofrontal cortex. Given earlier findings implicating the DLPFC in cognitive control of impulsive behavior (28–33), this is taken to support the reflective model of prosociality, in which prosocial behavior requires cognitive control of the impulsive drive toward selfish behavior. Steinbeis et al. (8) provided further support via a comparison of young children’s choices in the two economic games. Children took a large share in the DG while providing fairer amounts to responders in the UG. The children’s more generous giving in the UG may be based upon strategic reasoning regarding the possible consequences of not giving enough in the UG—that is, receiving no reward due to rejection by the other child—which plays no role in the DG. Thus, the difference in giving between the UG and the DG is considered to reflect the use of strategic reasoning in the UG. The strategic choices of more giving in the UG than in the DG is related to children’s age, cortical thickness, and activity of their left DLPFC. As children age and their DLPFC develops further, they become able to control their selfish drive and adjust their behavior to the anticipated negative consequences.This interpretation of UG–DG difference in prosocial giving as a reflection of strategic reasoning (8, 9) assumes that the default choice in the DG is impulsive and selfish. Younger children and those with a thinner DLPFC are presumably less capable of strategically adjusting their decisions to deal with anticipated responses and would impulsively pursue their own benefits in both the UG and the DG. In contrast, older children and those with a thicker DLPFC are more likely to have enhanced cognitive control, which can be used to strategically adjust their choices, especially in the UG but not in the DG. Therefore, a UG–DG positive reward transfer difference is produced by strategists’ control over the selfish impulses in the UG, whereas those who fail to control such impulses in the UG claim a considerable share in both games (Fig. 1A). In contrast, the alternative, intuitive prosociality model assumes that the uncontrolled choice is prosocial in both the UG and the DG, rather than selfish. Strategists control this impulse toward prosociality in the DG where immediate pursuit of self-interest causes no strategic problem (Fig. 1B). Nonstrategists do not control this impulse and provide a fair share in both games. Thus, a difference due to strategic reasoning is predicted to exist in the DG but not in the UG. The reflective and intuitive prosociality models thus make distinct predictions regarding the relationship between DLPFC thickness and behavior in the UG and DG. The reflective model predicts a positive relationship between DLPFC thickness and giving in the UG, whereas the intuitive model predicts a negative relationship between DLPFC thickness and giving in the DG.Open in a separate windowFig. 1.Schematic representations of how strategic considerations generate the difference between strategists (ST) and nonstrategists (Non-ST) in the UG and DG. A shows the prediction that strategic considerations should improve fair behavior in the UG. B shows the prediction that strategic considerations should depress fair behavior in the DG.These two alternative accounts of differences in giving in the UG and DG (8, 9) provide a way to test the intuitive selfishness assumption against the intuitive prosociality assumption. We first successfully replicated earlier findings that strategic behavior is more pronounced among those who had a thicker DLPFC than those who had a thinner DLPFC (8) in a study of 411 adult, nonstudent participants who played both the UG and DG and from whom brain structural images were obtained. Then, we found for the first time, to our knowledge, that local gray matter thickness of the DLPFC negatively correlated with giving in the DG but was not correlated with giving in the UG (Fig. 2 C and D). We further measured the strategic reasoning of 386 of these participants using a newly developed test of strategic reasoning, measured 411 participants’ Machiavellianism (34, 35) score, and found that those exhibiting better strategic reasoning behaved more selfishly in the DG than those with poor strategic reasoning, but no relationship was found between task performance and fairness in the UG. These striking findings provide strong evidence supporting the intuitive prosociality prediction depicted in Fig. 1B but not the reflective prosociality prediction shown in Fig. 1A.Open in a separate windowFig. 2.Brain areas in the Destrieu Atlas (A), the relationship of cortical thickness of the DLPFC (middle frontal gyrus) and strategic choice (UG–DG) (B), the relationship of its right cortical thickness and giving in the UG and DG (C), and the relationship of its left cortical thickness and giving in the UG and DG (D). The horizontal axis represents the residual cortical thickness adjusted for participants’ age, sex, and ICV. The vertical axis represents the mean strategic choice of the players, giving in the UG or the DG within 0.1-mm intervals of residual cortical thickness. Each interval spans 0.1 mm on the horizontal axis segment. The size of each circle shows the number of players who fell within the interval. Error bars are SEs. n = 411. Correlations are after adjusting for age, sex, and ICV.