Reward and social valuation deficits following ventromedial prefrontal damage

Lesion and imaging studies have implicated the ventromedial prefrontal cortex (vmPFC) in economic decisions and social interactions, yet its exact functions remain unclear. Here, we investigated the hypothesis that the vmPFC represents the subjective value or desirability of future outcomes during social decision-making. Both vmPFC-damaged patients and control participants acted as the responder in a single-round ultimatum game. To test outcome valuation, we contrasted concrete, immediately available gains with abstract, future ones. To test social valuation, we contrasted interactions with a human partner and those involving a computer. We found that, compared to controls, vmPFC patients substantially reduced their acceptance rate of unfair offers from a human partner, but only when financial gains were presented as abstract amounts to be received later. When the gains were visible and readily available, the vmPFC patients' acceptance of unfair offers was normal. Furthermore, unlike controls, vmPFC patients did not distinguish between unfair offers from a human agent and those from a computerized opponent. We conclude that the vmPFC encodes the expected value of abstract, future goals in a common neural currency that takes into account both reward and social signals in order to optimize economic decision-making.     

Neural correlates of fair behavior in interpersonal bargaining

Research findings show that proposers make surprisingly fair offers in the ultimatum and dictator games, an observation that contradicts predictions of classical game theory. The present functional magnetic resonance imaging (fMRI) study examines brain activities of proposers that contribute to fair and unfair behaviors. We hypothesized that egoistic and altruistic motives of proposers affect fairness differentially in the two games. fMRI analysis revealed that the 28% of fair offers in the present ultimatum game were related to enhanced activity in prefrontal areas, in particular, in regions involved in reward and theory of mind. This corroborates the idea that egoistic motives are primarily responsible for fair offers in this game, which we denote as strategic fairness. Fair offers in the dictator game, however, were related to increased activity in the dorsal anterior cingulate cortex and the posterior cingulate cortex. This supports the idea that altruistic motives primarily drive fair offers in the dictator game, denoted here as altruistic fairness.     

Neural correlates of fair behavior in interpersonal bargaining

Research findings show that proposers make surprisingly fair offers in the ultimatum and dictator games, an observation that contradicts predictions of classical game theory. The present functional magnetic resonance imaging (fMRI) study examines brain activities of proposers that contribute to fair and unfair behaviors. We hypothesized that egoistic and altruistic motives of proposers affect fairness differentially in the two games. fMRI analysis revealed that the 28% of fair offers in the present ultimatum game were related to enhanced activity in prefrontal areas, in particular, in regions involved in reward and theory of mind. This corroborates the idea that egoistic motives are primarily responsible for fair offers in this game, which we denote as strategic fairness. Fair offers in the dictator game, however, were related to increased activity in the dorsal anterior cingulate cortex and the posterior cingulate cortex. This supports the idea that altruistic motives primarily drive fair offers in the dictator game, denoted here as altruistic fairness.     

Neural mechanism of proposer's decision-making in the ultimatum and dictator games

Previous studies have demonstrated that reactions to unfair offers in the ultimatum game are correlated with negative emotion. However, little is known about the difference in neural activity between a proposer''s decision-making in the ultimatum game compared with the dictator game. The present functional magnetic resonance imaging study revealed that proposing fair offers in the dictator game elicited greater activation in the right supramarginal gyrus, right medial frontal gyrus and left anterior cingulate cortex compared with proposing fair offers in the ultimatum game in 23 Chinese undergraduate and graduate students from Beijing Normal University in China. However, greater activation was found in the right superior temporal gyrus and left cingulate gyrus for the reverse contrast. The results indicate that proposing fair offers in the dictator game is more strongly associated with cognitive control and conflicting information processing compared with proposing fair offers in the ultimatum game.     

Brain responses to social norms: Meta‐analyses of fMRI studies

Social norms have a critical role in everyday decision‐making, as frequent interaction with others regulates our behavior. Neuroimaging studies show that social‐based and fairness‐related decision‐making activates an inconsistent set of areas, which sometimes includes the anterior insula, anterior cingulate cortex, and others lateral prefrontal cortices. Social‐based decision‐making is complex and variability in findings may be driven by socio‐cognitive activities related to social norms. To distinguish among social‐cognitive activities related to social norms, we identified 36 eligible articles in the functional magnetic resonance imaging (fMRI) literature, which we separate into two categories (a) social norm representation and (b) norm violations. The majority of original articles (>60%) used tasks associated with fairness norms and decision‐making, such as ultimatum game, dictator game, or prisoner's dilemma; the rest used tasks associated to violation of moral norms, such as scenarios and sentences of moral depravity ratings. Using quantitative meta‐analyses, we report common and distinct brain areas that show concordance as a function of category. Specifically, concordance in ventromedial prefrontal regions is distinct to social norm representation processing, whereas concordance in right insula, dorsolateral prefrontal, and dorsal cingulate cortices is distinct to norm violation processing. We propose a neurocognitive model of social norms for healthy adults, which could help guide future research in social norm compliance and mechanisms of its enforcement.     

The role of prefrontal cortex in psychopathy

Psychopathy is a personality disorder characterized by remorseless and impulsive antisocial behavior. Given the significant societal costs of the recidivistic criminal acti\xadvity associated with the disorder, there is a pressing need for more effective treatment strategies and, hence, a better understanding of the psychobiological mechanisms underlying the disorder. The prefrontal cortex (PFC) is likely to play an important role in psychopathy. In particular, the ventromedial and anterior cingulate sectors of PFC are theorized to mediate a number of social and affective decision-making functions that appear to be disrupted in psychopathy. This article provides a critical summary of human neuroimaging data implicating prefrontal dysfunction in psychopathy. A growing body of evidence associates psychopathy with structural and functional abnormalities in ventromedial PFC and anterior cingulate cortex. Although this burgeoning field still faces a number of methodological challenges and outstanding questions that will need to be resolved by future studies, the research to date has established a link between psychopathy and PFC.     

Effects of transcranial direct current stimulation over the right dorsolateral prefrontal cortex on fairness-related decision-making

Neuroimaging studies suggest that the right dorsolateral prefrontal cortex (rDLPFC) is an important brain area involved in fairness-related decision-making. In the present study, we used transcranial direct current stimulation (tDCS) over the rDLPFC to investigate the effects of changed cortical excitability on fairness norm enforcement in social decision-making. Participants received anodal, cathodal or sham stimulation before performing a modified ultimatum game task, in which participants were asked to accept or reject the proposer’s offer and self-rate the intensity of their anger at offers on a 7-point scale. The results showed that the rejection rate of unfair offers and anger level were higher in the anodal compared to the sham and cathodal groups and that the level of anger at unfair offers can predict the rejection rate. Furthermore, the fairness effect of RTs was more prominent in the anodal group than in the sham and cathodal groups. Our findings validate the causal role of the rDLPFC in fairness-related decision-making through tDCS, suggesting that strengthening the rDLPFC increases individuals’ reciprocal fairness in social decision-making, both in subjective rating and behaviors.     

Neural basis of increased costly norm enforcement under adversity

Humans are willing to punish norm violations even at a substantial personal cost. Using fMRI and a variant of the ultimatum game and functional magnetic resonance imaging, we investigated how the brain differentially responds to fairness in loss and gain domains. Participants (responders) received offers from anonymous partners indicating a division of an amount of monetary gain or loss. If they accept, both get their shares according to the division; if they reject, both get nothing or lose the entire stake. We used a computational model to derive perceived fairness of offers and participant-specific inequity aversion. Behaviorally, participants were more likely to reject unfair offers in the loss (vs gain) domain. Neurally, the positive correlation between fairness and activation in ventral striatum was reduced, whereas the negative correlations between fairness and activations in dorsolateral prefrontal cortex were enhanced in the loss domain. Moreover, rejection-related dorsal striatum activation was higher in the loss domain. Furthermore, the gain–loss domain modulates costly punishment only when unfair behavior was directed toward the participants and not when it was directed toward others. These findings provide neural and computational accounts of increased costly norm enforcement under adversity and advanced our understanding of the context-dependent nature of fairness preference.     

Neural correlates of social cooperation and non-cooperation as a function of psychopathy.

BACKGROUND: Psychopathy is a disorder involving a failure to experience many emotions that are necessary for appropriate social behavior. In this study, we probed the behavioral, emotional, and neural correlates of psychopathic traits within the context of a dyadic social interaction. METHODS: Thirty subjects were imaged with functional magnetic resonance imaging while playing an iterated Prisoner's Dilemma game with human confederates who were outside the scanner. Subjects also completed two self-report psychopathy questionnaires. RESULTS: Subjects scoring higher on psychopathy, particularly males, defected more often and were less likely to continue cooperating after establishing mutual cooperation with a partner. Further, they experienced more outcomes in which their cooperation was not reciprocated (cooperate-defect outcome). After such outcomes, subjects scoring high in psychopathy showed less amygdala activation, suggesting weaker aversive conditioning to those outcomes. Compared with low-psychopathy subjects, subjects higher in psychopathy also showed weaker activation within orbitofrontal cortex when choosing to cooperate and showed weaker activation within dorsolateral prefrontal and rostral anterior cingulate cortex when choosing to defect. CONCLUSIONS: These findings suggest that whereas subjects scoring low on psychopathy have emotional biases toward cooperation that can only be overcome with effortful cognitive control, subjects scoring high on psychopathy have an opposing bias toward defection that likewise can only be overcome with cognitive effort.     

Someone has to give in: theta oscillations correlate with adaptive behavior in social bargaining

During social bargain, one has to both figure out the others’ intentions and behave strategically in such a way that the others’ behaviors will be consistent with one’s expectations. To understand the neurobiological mechanisms underlying these behaviors, we used electroencephalography while subjects played as proposers in a repeated ultimatum game. We found that subjects adapted their offers to obtain more acceptances in the last round and that this adaptation correlated negatively with prefrontal theta oscillations. People with higher prefrontal theta activity related to a rejection did not adapt their offers along the game to maximize their earning. Moreover, between-subject variation in posterior theta oscillations correlated positively with how individual theta activity influenced the change of offer after a rejection, reflecting a process of behavioral adaptation to the others’ demands. Interestingly, people adapted better their offers when they knew that they where playing against a computer, although the behavioral adaptation did not correlate with prefrontal theta oscillation. Behavioral changes between human and computer games correlated with prefrontal theta activity, suggesting that low adaptation in human games could be a strategy. Taken together, these results provide evidence for specific roles of prefrontal and posterior theta oscillations in social bargaining.     

Economic decision-making in psychopathy: A comparison with ventromedial prefrontal lesion patients

Psychopathy, which is characterized by a constellation of antisocial behavioral traits, may be subdivided on the basis of etiology: “primary” (low-anxious) psychopathy is viewed as a direct consequence of some core intrinsic deficit, whereas “secondary” (high-anxious) psychopathy is viewed as an indirect consequence of environmental factors or other psychopathology. Theories on the neurobiology of psychopathy have targeted dysfunction within ventromedial prefrontal cortex (vmPFC) as a putative mechanism, yet the relationship between vmPFC function and psychopathy subtype has not been fully explored. In this study, we administered two laboratory decision-making tasks (the Ultimatum Game and the Dictator Game) to a group of prisoners (n = 47) to determine whether the different subtypes of psychopathy (primary vs. secondary) are associated with characteristic patterns of economic decision-making, and furthermore, whether either subtype exhibits similar performance to patients with vmPFC lesions. Comparing primary psychopaths (n = 6) to secondary psychopaths (n = 6) and non-psychopaths (n = 22), we found that primary psychopathy was associated with significantly lower acceptance rates of unfair Ultimatum offers and lower offer amounts in the Dictator Game. Moreover, primary psychopaths were quantitatively similar to vmPFC lesion patients in their response patterns. These results support the purported connection between psychopathy and vmPFC dysfunction, bolster the distinction between primary and secondary psychopathy, and demonstrate the utility of laboratory economic decision-making tests in differentiating clinical subgroups.     

Why we stay with our social partners: Neural mechanisms of stay/leave decision-making

How do we decide to keep interacting (e.g., stay) with a social partner or to switch (e.g., leave) to another? This paper investigated the neural mechanisms of stay/leave decision-making. We hypothesized that these decisions fit within a framework of value-based decision-making, and explored four potential mechanisms underlying a hypothesized bias to stay. Twenty-six participants underwent functional Magnetic Resonance Imaging (fMRI) while completing social and nonsocial versions of a stay/leave decision-making task. On each trial, participants chose between four alternative options, after which they received a monetary reward. Crucially, in the social condition, reward magnitude was ostensibly determined by the generosity of social partners, whereas in the nonsocial condition, reward amounts were ostensibly determined in a pre-programmed manner. Results demonstrated that participants were more likely to stay with options of relatively high expected value, with these values updated through Reinforcement Learning mechanisms and represented neurally within ventromedial prefrontal cortex. Moreover, we demonstrated that greater brain activity in ventromedial prefrontal cortex, caudate nucleus, and septo-hypothalamic regions for social versus nonsocial decisions to stay may underlie a bias towards staying with social partners in particular. These findings complement existing social psychological theories by investigating the neural mechanisms of actual stay/leave decisions.     

Fairness concerns predict medial frontal negativity amplitude in ultimatum bargaining

Abstract

Despite evidence that anterior cingulate cortex (ACC) activity is related to social exclusion, rejection and unfairness, evidence that medial frontal negativity (MFN), which has its source in the ACC, reflects these constructs remains unforthcoming. In the present study, subjects participated as recipients in an ultimatum game, while we recorded their electro-encephalogram (EEG). Participants responded to fair and unfair offers from different human proposers. In addition, participants rated themselves on a measure evaluating their concern for fairness. Results showed that MFN amplitude was more pronounced for unfair offers compared to fair offers. Moreover, this effect was shown to be most pronounced for subjects with high concerns for fairness. Our findings suggest that the MFN not only reflects whether outcomes match expectations, but also reflects whether the process by which these outcomes came about matches a social or even a moral norm. In addition, the present results suggest that people in bargaining situations are not only concerned with their own outcomes, but are also concerned with the fairness of the process that resulted in these outcomes.     

Neural responses to unfairness and fairness depend on self-contribution to the income

Self-contribution to the income (individual achievement) was an important factor which needs to be taken into individual’s fairness considerations. This study aimed at elucidating the modulation of self-contribution to the income, on recipient’s responses to unfairness in the Ultimatum Game. Eighteen participants were scanned while they were playing an adapted version of the Ultimatum Game as responders. Before splitting money, the proposer and the participant (responder) played the ball-guessing game. The responder’s contribution to the income was manipulated by both the participant’s and the proposer’s accuracy in the ball-guessing game. It turned out that the participants more often rejected unfair offers and gave lower fairness ratings when they played a more important part in the earnings. At the neural level, anterior insula, anterior cingulate cortex, dorsolateral prefrontal cortex and temporoparietal junction showed greater activities to unfairness when self-contribution increased, whereas ventral striatum and medial orbitofrontal gyrus showed higher activations to fair (vs unfair) offers in the other-contributed condition relative to the other two. Besides, the activations of right dorsolateral prefrontal cortex during unfair offers showed positive correlation with rejection rates in the self-contributed condition. These findings shed light on the significance of self-contribution in fairness-related social decision-making processes.     

Psychopathic Traits and Social Cooperation in the Context of Emotional Feedback

Much is known about the affective deficits that characterise psychopathic traits. However, relatively little research has investigated psychopathy using paradigms that model social dynamics in interpersonal contexts. This study examined the association between psychopathic traits and social cooperation in an iterated prisoner's dilemma (IPD) paradigm, and tested the impact of affective cues from a co-player on participant cooperation. A sample of male university students participated in a block of standard IPD trials (game 1) followed by a block comprising a novel condition in which participants were provided with feedback on the emotional state of a bogus co-player throughout game-play (game 2). Whereas participants with low levels of psychopathic traits exhibited increased social cooperation in the context of affective feedback, poor cooperation was uniquely predicted by high levels of psychopathic traits. Findings are discussed in relation to recent accounts of psychopathy that emphasise attention-based mechanisms and empathic dysfunction.     

Differential neural circuitry and self-interest in real vs hypothetical moral decisions

Classic social psychology studies demonstrate that people can behave in ways that contradict their intentions—especially within the moral domain. We measured brain activity while subjects decided between financial self-benefit (earning money) and preventing physical harm (applying an electric shock) to a confederate under both real and hypothetical conditions. We found a shared neural network associated with empathic concern for both types of decisions. However, hypothetical and real moral decisions also recruited distinct neural circuitry: hypothetical moral decisions mapped closely onto the imagination network, while real moral decisions elicited activity in the bilateral amygdala and anterior cingulate—areas essential for social and affective processes. Moreover, during real moral decision-making, distinct regions of the prefrontal cortex (PFC) determined whether subjects make selfish or pro-social moral choices. Together, these results reveal not only differential neural mechanisms for real and hypothetical moral decisions but also that the nature of real moral decisions can be predicted by dissociable networks within the PFC.     

Emotions and cooperation in economic games

In this paper, we examine decisions to cooperate in economic games. We investigate which payoffs give players the greatest pleasure and whether the pleasure they feel about payoffs predicts their decisions to cooperate. To do this, we modify the ultimatum and dictator games by asking players to consider a fixed set of offers and report their preferences over all offers. Players also report the pleasure they imagine feeling from each possible payoff. Results show that players differ in the extent to which they derive pleasure from fairness or greediness. They also differ in the extent to which their choices depend on what we call "strategic" and "non-strategic" pleasure. Strategic pleasure is the expected pleasure of offers, whereas non-strategic pleasure is the pleasure of accepted payoffs. Players whose pleasure primarily depends on larger payoffs tend to make fair offers in the ultimatum game and selfish offers in the dictator game. They maximize strategic pleasure in the ultimatum game and non-strategic pleasure in the dictator game. Players who derive greater pleasure from fairness tend to act fairly in both games. These players maximize non-strategic pleasure. Brain imaging studies should address the question of whether the observed differences in pleasure and preference are systematically linked to differences in neurological activation.     

Mental attributes and temporal brain dynamics during bargaining: EEG source localization and neuroinformatic mapping

It was previously shown by fMRI studies that unfair offers during an ultimatum bargaining game activate regions in the brain associated with emotions and conflict, leading to decisions inconsistent with standard economic theory. The temporal dynamics of emotional processing and mental attributes were not clear due to the coarse temporal resolution in those studies (～2 s). Here, the ultimatum game was studied by EEG recorded from the responders in 19 channels. EEG time series were first in-put to independent component analysis. An equivalent current dipole model was used to localize the sources of the independent components in EEGLAB. The Talairach coordinates of the dipoles were matched with references in the Brede neuroinformatics database. Dipole magnitudes, anatomical regions, and mental attributes were used to explain the rejection of the offers by applying multiple regression as a function of time in epochs with a median resolution of 250 ms. The results are consistent with previous studies regarding responder behavior and activated regions (e.g., anterior cingulate cortex, frontal gyrus, insular cortex). There are three main findings observed with the higher temporal resolution: (1) regression results from fine-scale temporal data showed activations not captured when the analysis was done by using time-averaged data; (2) temporal analysis detected the individual significant epochs and fluctuations (positive and negative correlations) in regions and for the associated mental attributes (e.g., reward/harm perception, anger, unfairness); (3) there was a sequential activation of anterior cingulate cortex and insular cortex, respectively, leading to the rejection response. Overall, regression models could explain a large percentage (～80%) of out-of-sample behavioral responses. The results are promising for the prospect of using EEG and source localization techniques in neuroeconomics to study finer temporal dynamics of neural activation.     

Mental attributes and temporal brain dynamics during bargaining: EEG source localization and neuroinformatic mapping

It was previously shown by fMRI studies that unfair offers during an ultimatum bargaining game activate regions in the brain associated with emotions and conflict, leading to decisions inconsistent with standard economic theory. The temporal dynamics of emotional processing and mental attributes were not clear due to the coarse temporal resolution in those studies (～2 s). Here, the ultimatum game was studied by EEG recorded from the responders in 19 channels. EEG time series were first in-put to independent component analysis. An equivalent current dipole model was used to localize the sources of the independent components in EEGLAB. The Talairach coordinates of the dipoles were matched with references in the Brede neuroinformatics database. Dipole magnitudes, anatomical regions, and mental attributes were used to explain the rejection of the offers by applying multiple regression as a function of time in epochs with a median resolution of 250 ms. The results are consistent with previous studies regarding responder behavior and activated regions (e.g., anterior cingulate cortex, frontal gyrus, insular cortex). There are three main findings observed with the higher temporal resolution: (1) regression results from fine-scale temporal data showed activations not captured when the analysis was done by using time-averaged data; (2) temporal analysis detected the individual significant epochs and fluctuations (positive and negative correlations) in regions and for the associated mental attributes (e.g., reward/harm perception, anger, unfairness); (3) there was a sequential activation of anterior cingulate cortex and insular cortex, respectively, leading to the rejection response. Overall, regression models could explain a large percentage (～80%) of out-of-sample behavioral responses. The results are promising for the prospect of using EEG and source localization techniques in neuroeconomics to study finer temporal dynamics of neural activation.     

Dysfunctional involvement of emotion and reward brain regions on social decision making in excess weight adolescents

Obese adolescents suffer negative social experiences, but no studies have examined whether obesity is associated with dysfunction of the social brain or whether social brain abnormalities relate to disadvantageous traits and social decisions. We aimed at mapping functional activation differences in the brain circuitry of social decision making in adolescents with excess versus normal weight, and at examining whether these separate patterns correlate with reward/punishment sensitivity, disordered eating features, and behavioral decisions. In this fMRI study, 80 adolescents aged 12 to 18 years old were classified in two groups based on age adjusted body mass index (BMI) percentiles: normal weight (n = 44, BMI percentiles 5th–84th) and excess weight (n = 36, BMI percentile ≥ 85th). Participants were scanned while performing a social decision‐making task (ultimatum game) in which they chose to “accept” or “reject” offers to split monetary stakes made by another peer. Offers varied in fairness (Fair vs. Unfair) but in all cases “accepting” meant both players win the money, whereas “rejecting” meant both lose it. We showed that adolescents with excess weight compared to controls display significantly decreased activation of anterior insula, anterior cingulate, and midbrain during decisions about Unfair versus Fair offers. Moreover, excess weight subjects show lower sensitivity to reward and more maturity fears, which correlate with insula activation. Indeed, blunted insula activation accounted for the relationship between maturity fears and acceptance of unfair offers. Excess weight adolescents have diminished activation of brain regions essential for affective tracking of social decision making, which accounts for the association between maturity fears and social decisions. Hum Brain Mapp, 36:–237, 2015. © 2014 Wiley Periodicals, Inc .