Adult-like neuroelectrical response to inequity in children: Evidence from the ultimatum game

People react aversely when faced with unfair situations, a phenomenon that has been related to an electroencephalographic (EEG) potential known as medial frontal negativity (MFN). To our knowledge, the existence of the MFN in children has not yet been demonstrated. Here, we recorded EEG activity from 15 children playing the ultimatum game (UG) and who afterward performed a recognition task, in order to assess whether they could recognize the unfair and fair (familiar) proposers among unfamiliar faces. During the recognition task, we also acquired pupil dilation data to investigate subconscious recognition processes. A typical (adult-like) MFN component was detected in reaction to unfair proposals. We found a positive correlation between reaction time and empathy, as well as a negative correlation between reaction time and systematic reasoning scores. Finally, we detected a significant difference in pupil dilation in response to unfamiliar faces versus UG proposers. Our data provide the first evidence of MFN in children, which appears to index similar neurophysiological phenomena as in adults. Also, reaction time to fair proposals seems to be related to individual traits, as represented by empathy and systematizing. Our pupil dilation data provide evidence that automatic responses to faces did not index fairness, but familiarity. These findings have implications for our understanding of social development in typically developing children.     

A neural signature of the creation of social evaluation

Previous research has shown that receiving an unfair monetary offer in economic bargaining elicits also-called feedback negativity (FN). This scalp-recorded brain potential probably reflects a bad-vs-good evaluation in the medial frontal cortex and has been linked to fundamental processes of reinforcement learning. In the present study, we investigated whether the evaluative mechanism indexed by the FN is also involved in learning who is an unfair vs fair bargaining partner. An electroencephalogram was recorded while participants completed a computerized version of the Ultimatum Game, repeatedly receiving fair or unfair monetary offers from alleged other participants. Some of these proposers were either always fair or always unfair in their offers. In each trial, participants first saw a portrait picture of the respective proposer before the monetary offer was presented. Therefore, the faces could be used as predictive cues for the fairness of the pending offers. We found that not only unfair offers themselves induced a FN, but also (over the task) faces of unfair proposers. Thus, when interaction partners repeatedly behave in an unfair way, their faces acquire a negative valence, which manifests in a basal neural mechanism of bad-vs-good evaluation.     

Taking it easy when playing ultimatum game with a Down syndrome proposer: Effects on behavior and medial frontal negativity

The ultimatum game (UG) is an endowment sharing game in which a proposer suggests a division of an asset to a recipient, who must accept or reject it. Economic studies showed that despite recipients usually rejecting unfair offers, perception and reaction to unfairness are highly dependent on who is the proposer. Event-related potentials (ERPs) commonly detected in UG games are the medial frontal negativity (MFN), a component detected in recipients facing unfair offers, and the P300, a component related to attentional and memory processes. Given this, we aimed to investigate the behavioral and ERP responses of healthy people playing the UG game with Down syndrome (DS) and typical development (TD) proposers. Nineteen subjects participated in this study. The UG behavioral data were similar to previous studies. ERP analysis showed no MFN in participants facing unfair offers. A higher P300 amplitude was detected when participants faced fair offers from TD compared to DS fair offers. We also found a positive correlation between P300 amplitude for TD offers and self-esteem scale score. Together these findings indicate that insertion of an atypical player in the UG led to changes in participants’ perception and expectancy of the game.     

Responding to unfair offers made by a friend: neuroelectrical activity changes in the anterior medial prefrontal cortex

When receiving unfair monetary offers from another person, the most common response is punishment. Existing literature on the Ultimatum Game indicates that individuals frequently refuse unfair offers even when this results in a loss for themselves. Here, we present behavioral and neurophysiological evidence demonstrating that friendship substantially modifies this response. When the proposer was a friend rather than an unknown person, unfair offers were less frequently rejected and the medial frontal negativity (MFN) typically associated with unfair offers was reversed to positive polarity. The underlying generators were located in inferior-mesial and right inferior- and medial-lateral frontal regions (BA10 and BA11). These findings highlight the fundamental role of the anterior prefrontal cortex in interpersonal economic interaction and, particularly, present new evidence on the effects of social distance on the MFN.     

Deliberate or unintended: Intentions modulate empathic responses to others’ economic payoffs in social interactions

Previous studies examining empathy have revealed the neural substrates of how the physical pain of others is represented in the human brain. However, little is known about the empathic modulation of behavioral and neural responses to others’ economic payoffs, especially in the social context. In the present study, we engaged participants in a revised Dictator Game as observers who observe the powerless players receiving varied offers proposed by the dominant players, establishing the link between empathy and fairness perception. Results showed that unfair division schemes elicited a more pronounced FRN than fair ones only if a human agent proposed the initial offer. In addition, observers sacrificed their own payments to adjust unfair proposals, especially when a human agent proposed the offer. Thus, results of the current study demonstrated that perceived intention modulates behavioral and neural responses to others’ economic payoffs in social interactions.     

The time course of neural responses to social versus non-social unfairness in the ultimatum game

The unfairness effects are always the hotspot within social psychology and cognitive neuroscience. However, people’s neural responses to social versus non-social unfairness remain under-researched, especially about temporal features. We engaged participants in the Ultimatum Game to respond to human and computer proposers (representing social and non-social contexts respectively) and recorded their event-related potentials. The interactions elicited three components of interest: medial frontal negativity (MFN), late positive potential (LPP) and response related negativity (RRN). First, unfair human offers elicited larger MFN than unfair computer offers did, suggesting a greater perception of unfairness in the social context. Second, rejected unfair human offers elicited smaller LPP than rejected unfair computer offers did. This finding implies that the rejection to social unfairness could down-regulate the unfairness-aversive emotions. These two mechanisms explained the stronger resistance to social unfairness in behavioural results. Last, the RRN for unfairness rejections were larger than for fairness acceptances, but showed no variance to the two types of proposers, signifying a similar degree of response conflict behind rejections to social and non-social unfairness. These results of our exploratory study will be helpful in revealing the sociality effect on the perceptual, emotional and reappraisal processing during the unfairness response.     

Whose loss is it? Human electrophysiological correlates of non-self reward processing

Abstract

To recognize whether another person's action results in a good or bad outcome is imperative for social learning, as well as for understanding the behavior of others in a broad context. Recent studies have reported that a scalp-surface event-related potential (ERP) called medial-frontal negativity (MFN), considered to be an index of negative reward processing, is generated when perceiving not only one's own losses, but also those of others. This suggests that the same neural mechanisms operate in monitoring one's own actions and in perceiving the consequences of the actions of others. To further elucidate the properties of this “observational” MFN, this study examined whether its amplitude differs with different observational targets. In a gambling task, participants observed the performances of non-self agents: a human friend and PC programs. The outcomes of the decisions of these agents were not associated with the participants’ own benefits. ERP results showed that the MFN-like pattern was significantly elicited only when observing the outcomes of decisions made by human agents. Furthermore, self-reported measures of empathy were positively associated with the magnitude of the observational MFN. These findings suggest that the neural activity in non-self reward processing reflects a socioemotional state generated by the target of observation, as well as an empathetic trait of the individual.     

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.     

Mentalizing in economic decision-making

In the Ultimatum Game, participants typically reject monetary offers they consider unfair even if the alternative is to gain no money at all. In the present study, ERPs were recorded while subjects processed different offers of a proposer. In addition to clearly fair and unfair offers, mid-value offers which cannot be easily classified as fair or unfair and therefore involve more elaborate decision making were analyzed. A fast initial distinction between fair and other kinds of offers was reflected by amplitude of the feedback related negativity (FRN). Mid-value offers were associated with longer RTs, and a larger N350 amplitude. In addition, source analyses revealed a specific involvement of the superior temporal gyrus and the inferior parietal lobule during processing of mid-value offers compared to offers categorized clearly as fair or unfair, suggesting a contribution of mentalizing about the intention of the proposer to the decision making process. Taken together, the present findings support the idea that economic decisions are significantly affected by non-rational factors, trying to narrow the gap between formal theory and the real decisional behaviour.     

Retaliation or selfishness? An rTMS investigation of the role of the dorsolateral prefrontal cortex in prosocial motives

Equity, fairness and cooperative behavior are crucial for everyday social interactions. Recent neuroimaging studies suggest that the dorsolateral prefrontal cortex (DLPFC) is involved in the evaluation of violations of fairness rules, though difficulties remain to determine its role in implementing retaliating or forgiving responses to unfairness. Accordingly, we applied repetitive transcranial magnetic stimulation (rTMS) to the left and right DLPFC and investigated the impact of the DLPFC on retaliation and selfishness using a sequential neuroeconomic task establishing a role reversal. That is, participants first played an Ultimatum Game (in the role of a recipient) against fair or unfair proposers, followed by a Dictator Game in the role of a proposer. Following inhibition of the right DLPFC, subjects showed an increased punishment rate regarding previously unfair opponents. Surprisingly, previously fair opponents were also treated less fairly after rTMS to the right DLPFC, but not after left or sham rTMS. Previous work suggests that the right DLPFC provides “top-down” cognitive control over prepotent emotional responses to unfairness. Our results indicate, however, that the right DLPFC may be involved in controlling selfish behavior and that its suppression leads to maximization of one’s own benefit, regardless of another’s fairness or unfairness in previous encounters.     

Do different fairness contexts and facial emotions motivate ‘irrational’ social decision-making in major depression? An exploratory patient study

Although ‘irrational’ decision-making has been linked to depression, the contribution of biases in information processing to these findings remains unknown. To investigate the impact of cognitive biases and aberrant processing of facial emotions on social decision-making, we manipulated both context-related and emotion-related information in a modified Ultimatum Game. Unfair offers were (1) paired with different unselected alternatives, establishing the context in which an offer was made, and (2) accompanied by emotional facial expressions of proposers. Responder behavior was assessed in patients with major depressive disorder and healthy controls. In both groups alike, rejection rates were highest following unambiguous signals of unfairness, i.e. an angry proposer face or when an unfair distribution had deliberately been chosen over an equal split. However, depressed patients showed overall higher rejection rates than healthy volunteers, without exhibiting differential processing biases. This suggests that depressed patients were, as healthy individuals, basing their decisions on informative, salient features and differentiating between (i) fair and unfair offers, (ii) alternatives to unfair offers and (iii) proposers' facial emotions. Although more fundamental processes, e.g. reduced reward sensitivity, might underlie increased rejection in depression, the current study provides insight into mechanisms that shape fairness considerations in both depressed and healthy individuals.     

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.     

Do Children with Autism Spectrum Disorder Share Fairly and Reciprocally?

This study investigated whether children with autism spectrum disorder (ASD) and typically developing children matched on receptive language share resources fairly and reciprocally. Children completed age-appropriate versions of the Ultimatum and Dictator Games with real stickers and an interactive partner. Both groups offered similar numbers of stickers (preferring equality over self-interest), offered more stickers in the Ultimatum Game, and verbally referenced ‘fairness’ at similar rates. However, children with ASD were significantly more likely to accept unfair offers and were significantly less likely to reciprocate the puppet’s offers. Failure to reciprocate fair sharing may significantly impact on social cohesion and children’s ability to build relationships. These important differences may be linked to broader deficits in social-cognitive development and potentially self-other understanding.     

The Ultimatum Game and the brain: A meta-analysis of neuroimaging studies

Social decision-making tasks involve psychological processes key to effective functioning in a complex, social world. The Ultimatum Game (UG) is a widely studied social decision-making task, which models responses to fairness. A number of neuroimaging studies have investigated the UG to identify neural correlates of unfairness and decisions to reject versus accept an offer. We present the first quantitative summary of neuroimaging studies in social decision-making with a meta-analysis of 11 fMRI studies of the UG, including data from 282 participants. Effect-Size Signed Differential Mapping was used to estimate effect sizes from statistical parametric maps and reported peak information before meta-analysing them. Consistent activations were seen in the anterior insula, anterior cingulate cortex (ACC), supplementary motor area (SMA) and cerebellum in response to unfair offers. Robust activations in the ACC, SMA and putamen were seen when deciding to reject rather than accept UG offers. These are consistent with models of motivational conflict during the UG decision-making process, a response to norm violations, with a possible role for the reward system.     

Superior 'theory of mind' in borderline personality disorder: an analysis of interaction behavior in a virtual trust game

To gain further insight into interpersonal dysfunction in Borderline Personality Disorder (BPD) we investigated the effects of emotional cues and the fairness of a social partner on the ability to infer other peoples' intentions in a virtual social exchange. 30 BPD patients and 30 nonpatients were asked to play a multiround trust game with four virtual trustees. The trustees varied in regard to fairness and presence of emotional facial cues which were both linked to repayment ratio. BPD patients adjusted their investment to the fairness of their partner. In contrast, nonpatients disregarded the trustees' fairness in the presence of emotional facial expressions. Both groups performed equally in an emotion recognition task and assessed the trustees' fairness comparably. When the unfair trustee provided emotional cues, BPD patients assessed their own behavior as more fair, while the lack of cues led patients to assess their own behavior as unfair. BPD patients are superior in the attribution of mental states to interaction partners when emotional cues are present. While the emotional expressions of a partner dominated the exchange behavior in nonpatients, BPD patients used the objective fairness of their social counterparts to guide their own behavior despite the existence of emotional cues.     

Distinct neural activation patterns underlie economic decisions in high and low psychopathy scorers

Psychopathic traits affect social functioning and the ability to make adaptive decisions in social interactions. This study investigated how psychopathy affects the neural mechanisms that are recruited to make decisions in the ultimatum game. Thirty-five adult participants recruited from the community underwent functional magnetic resonance imaging scanning while they performed the ultimatum game under high and low cognitive load. Across load conditions, high psychopathy scorers rejected unfair offers in the same proportion as low scorers, but perceived them as less unfair. Among low scorers, the perceived fairness of offers predicted acceptance rates, whereas in high scorers no association was found. Imaging results revealed that responses in each group were associated with distinct patterns of brain activation, indicating divergent decision mechanisms. Acceptance of unfair offers was associated with dorsolateral prefrontal cortex activity in low scorers and ventromedial prefrontal cortex activity in high scorers. Overall, our findings point to distinct motivations for rejecting unfair offers in individuals who vary in psychopathic traits, with rejections in high psychopathy scorers being probably induced by frustration. Implications of these results for models of ventromedial prefrontal cortex dysfunction in psychopathy are discussed.     

Social status modulates the neural response to unfairness

In human society, which is organized by social hierarchies, resources are usually allocated unequally and based on social status. In this study, we analyze how being endowed with different social statuses in a math competition affects the perception of fairness during asset allocation in a subsequent Ultimatum Game (UG). Behavioral data showed that when participants were in high status, they were more likely to reject unfair UG offers than in low status. This effect of social status correlated with activity in the right anterior insula (rAI) and with the functional connectivity between the rAI and a region in the anterior middle cingulate cortex, indicating that these two brain regions are crucial for integrating contextual factors and social norms during fairness perception. Additionally, there was an interaction between social status and UG offer fairness in the amygdala and thalamus, implicating the role of these regions in the modulation of social status on fairness perception. These results demonstrate the effect of social status on fairness perception and the potential neural underpinnings for this effect.     

The anterior cingulate cortex: monitoring the outcomes of others' decisions

The ability to attribute mental states to others and understand the basis of their decisions is essential for human social interaction. A controversial theory states that this is achieved by simulating another's information processing in one's own neural circuits. The anterior cingulate cortex (ACC) is known to play an important role in the registration of discrepancies between the predicted and actual outcomes of decisions (prediction errors).When positive and negative feedback fails altogether, the failure may also signal errors in the prediction that the outcome of that decision would be informative and guide future decisions. Does the ACC signal that an outcome is unexpectedly uninformative? When an outcome directed to others is uninformative, do we understand their mental states by simulating them in the circuits of the ACC in our own brain? The aim of our study was to test for these two possibilities in the human brain with event-related fMRI. We tested whether the ACC processes errors in the prediction of informative feedback and whether the ACC is also activated when scanned subjects process the same outcomes of another's decisions. We show that each is processed by a separate subregion of the ACC.     

Social economic decision-making across the lifespan: An fMRI investigation

Recent research in neuroeconomics suggests that social economic decision-making may be best understood as a dual-systems process, integrating the influence of deliberative and affective subsystems. However, most of this research has focused on young adults and it remains unclear whether our current models extend to healthy aging. To address this question, we investigated the behavioral and neural basis of simple economic decisions in 18 young and 20 older healthy adults. Participants made decisions which involved accepting or rejecting monetary offers from human and non-human (computer) partners in an Ultimatum Game, while undergoing functional magnetic resonance imaging (fMRI). The partners' proposals involved splitting an amount of money between the two players, and ranged from $1 to $5 (from a $10 pot). Relative to young adults, older participants expected more equitable offers and rejected moderately unfair offers ($3) to a larger extent. Imaging results revealed that, relative to young participants, older adults had higher activations in the left dorsolateral prefrontal cortex (DLPFC) when receiving unfair offers ($1-$3). Age group moderated the relationship between left DLPFC activation and acceptance rates of unfair offers. In contrast, older adults showed lower activation of bilateral anterior insula in response to unfair offers. No age group difference was observed when participants received fair ($5) offers. These findings suggest that healthy aging may be associated with a stronger reliance on computational areas subserving goal maintenance and rule shifting (DLPFC) during interactive economic decision-making. Consistent with a well-documented "positivity effect", older age may also decrease recruitment of areas involved in emotion processing and integration (anterior insula) in the face of social norm violation.