So why do human beings turn a perfectly good reward into a disappointment when others are getting more? One proposal is that the superficially “irrational” rejection of inferior shares is a costly but effective means of enforcing social norms (Boyd et al., 2003). Ultimately, the costs of giving up inferior shares are presumably outweighed by the long-term benefits of establishing a cooperative social environment (Fehr and Gachter, 2002; de Quervain et al., 2004). Although this may be so, the strategy of measuring one's own gains against others also has a downside. In wealthy societies, a comfortable income can become unsatisfactory if compared to an extravagant one: the millionaire envies the billionaire, and the billionaire envies still richer billionaires. This arms race of reward can in itself lead to inequity and social unrest, as in the rapid escalation of corporate executive compensation in recent years, which led to a backlash of widespread public indignation (Ariely, 2008).

The human tendency to see rewards in socially relative terms may therefore be a mixed blessing. If so, the question arises as to whether some people are capable of ignoring social considerations and assessing a reward based on its intrinsic qualities alone. The willingness to sacrifice money to punish an unfair proposer is associated with affective responses, as measured by skin conductance responses (van't Wout et al., 2006). These affective responses have specific neural correlates, identified in neuroimaging studies of social exchange. Unfair offers elicit greater activation in the anterior insula (Rilling et al., 2002; Sanfey et al., 2003; King-Casas et al., 2008), an area linked to interoceptive function (Craig, 2002, 2009; Critchley et al., 2004), and in particular to the emotion of disgust (Calder et al., 2001). Anterior insula activation scales inversely with offer size, and predict whether an unfair offer will be rejected (Sanfey et al., 2003). These results suggest that rejection of unfair offers in the Ultimatum Game is driven by negative emotional reactions.

If some individuals had expertise in uncoupling such emotional reactions from their actual behavior, they might be better equipped to assess a reward on its own merits. Such individuals could potentially be found among experienced practitioners of mindfulness meditation. Mindfulness meditation has its roots in a 2500-year-old Buddhist tradition, and has grown increasingly popular in Western societies over the last few decades. A central technique in mindfulness is to attend to the events in the present moment, on purpose, in a spirit of observation rather than judgment.

Meditation has been conceptualized as complex emotional regulatory training techniques developed for cultivation of well-being and emotional balance (Lutz et al., 2008a). Previous research on emotion regulation show that humans are able to exert a degree of control by reducing or enhancing emotional reactions elicited by various categories of stimuli and events in the world (Jackson et al., 2000; Ochsner et al., 2002; Ochsner and Gross, 2005; Eippert et al., 2007). Based on these previous studies we hypothesized that successful regulation of negative emotional reactions would lead to increased acceptance rates of unfair offers in the Ultimatum Game. In line with this hypothesis, we expected that meditators would exhibit greater acceptance rates for highly asymmetric offers.

Recent neuroimaging studies suggest some convergence between the neural correlates of social exchange and mindfulness meditation. Voxel-based morphometry studies demonstrate higher gray matter volumes in the anterior insula of meditators versus age-matched controls, suggesting long-term effects of meditation (Lazar et al., 2005; Holzel et al., 2008; Luders et al., 2009). The mid and posterior aspects of the insular cortex are activated during meditative states (Farb et al., 2007; Lutz et al., 2008b, 2009). In addition, even a short course of mindfulness training is effective in decoupling the activity of the insula from the activity of other regions involved in social decision-making, such as the medial prefrontal cortex (Farb et al., 2007; Tang et al., 2009). Taken together, these findings suggest that experienced mindfulness meditators could be capable of regulating emotional and social considerations in their evaluation of rewards in the Ultimatum Game.

Specifically, we hypothesized that the key anatomical locus for such regulation would be attenuation of the anterior insula responses toward unfair offers in meditators compared with controls. Furthermore, we expected that meditators would attend to internal bodily states in order to successfully regulate negative emotional reactions to unfair monetary offers. In accordance with previous studies we expected that elevated interoceptive awareness would involve brain regions such as the posterior parts of the insula and somatosensory cortices (Farb et al., 2007; Lutz et al., 2008b, 2009; Tang et al., 2009). Conversely, we expected that non-meditator controls might rely more on medial cortical areas linked to prospection and theory of mind, in line with previous studies (Rilling et al., 2002; Sanfey et al., 2003).

To test these hypotheses, we recruited a group of experienced mindfulness meditators and a control group of non-meditators. We enrolled subjects in the study to play the role of responders in an anonymous version of the Ultimatum Game (Figure ​(Figure1),1), while undergoing fMRI. We report both the behavioral and the neuroimaging findings resulting from the experiment.

In dual-process accounts of human decision-making, separate “rational,” and “emotional” systems compete to control the outcome of human decisions (Tversky and Kahneman, 1981; St. Evans, 2008). Neuroimaging studies have suggested that these two systems may have distinct neural correlates. For example, intuitive or emotion-driven decisions tend to be associated with greater activity in medial prefrontal and medial orbitofrontal cortical areas and their striatal counterparts, while more rational or deliberative decisions tend to be associated with a shift in activity toward more lateral prefrontal and parietal areas and their striatal counterparts (Goel and Dolan, 2003; Greene et al., 2004; McClure et al., 2004). Hence, when comparing meditators to control subjects, we might have expected to see a shift in activity from medial to lateral prefrontal cortical areas in meditators playing the Ultimatum Game. In reality, the neuroimaging results showed quite a different pattern. During decision-making, control subjects activated a network of areas including medial prefrontal cortex, anterior cingulate cortex, and superior temporal sulcus (Figure ​(Figure2A;2A; Table ​Table3).3). This network was largely consistent with that seen in previous neuroimaging studies of the Ultimatum Game, and other tasks involving social cognition and theory of mind (Sanfey et al., 2003; Amodio and Frith, 2006; Adolphs, 2009). In sharp contrast, meditators showed activity in an entirely separate network, which comprised primarily the mid- and posterior insula and ventral posterior thalamus (Figure ​(Figure2B;2B; Table ​Table2).2). Rather than social cognition and theory of mind, these areas are more typically associated with interoception: the representation of the body's internal state (Craig, 2002, 2009). Specifically, a representation of the body's internal state is mapped by afferents through the ventromedial thalamic nucleus to the sensorimotor cortex and the mid/posterior insula (Craig, 2002).

Strikingly, there was very little overlap in activity between meditators and controls. The left ACC (BA 24/32) was the only region activated in a conjunction analysis between controls and meditators. So, when playing the Ultimatum Game, meditators were distinct from controls not only in their decision-making behavior, but also in its underlying neural correlates. However, although the meditators played the game more like the rational homo economicus, they did not draw upon the network of lateral prefrontal and parietal regions typically seen for mathematical and logical reasoning (Duncan et al., 2000; Goel and Dolan, 2003; Lee et al., 2006). Instead, they drew upon the posterior insula and thalamus: areas usually linked to visceral, emotional rather than rational, deliberative functions.

The behavioral difference between meditators and controls was significant for the most asymmetric offers (Figure ​(Figure1C).1C). Focusing on unfair trials, a direct contrast of activation between the two groups showed illuminating differences in neural activity (Figures ​(Figures2C,D).2C,D). Controls responded to asymmetric offers by engaging the precuneus and a dorsal region of the caudate nucleus. This specific region of the precuneus figures prominently in studies of episodic memory and prospection (the construction of imaginary or future personal scenarios; Buckner and Carroll, 2007; Addis et al., 2009; Spreng et al., 2009). The dorsal caudate region also appears as a specific neural correlate of “fictive error,” or the difference between actual and optimal reward, during financial decision-making (Lohrenz et al., 2007). Hence, control subjects may be assessing asymmetric offers in terms of past or hypothetical future scenarios and fictive losses. Furthermore, the dorsal striatum is elevated during altruistic punishment of defectors in an economic exchange (de Quervain et al., 2004), presumably reflecting signals to punish norm violators, which in the current study may explain controls’ increasing rejection rates to the most asymmetric offers, compared with meditators. In contrast, meditators showed greater activity in the insula and PPC: areas more closely linked to interoception and attending to the present moment (Critchley et al., 2004; Farb et al., 2007). There exist physiological evidence from previous meditation studies that the left insula is predominantly responsible for parasympathetic control (Lutz et al., 2009; Tang et al., 2009), whereas the right insula, which we observed in the interaction between group (meditator versus control) and offer type (unfair versus fair; Figure ​Figure3),3), has in several studies been proposed to play a role in attending to internal bodily states (Craig, 2003). Previous meditation studies have found right insula involvement in focused attention to internal experiences (Holzel et al., 2008), and momentary self-reference (Farb et al., 2007). Based on these findings it is likely that meditators particularly during unfair offers were better able than controls to maintain interoceptive awareness, e.g., attending to internal bodily states. This interpretation is further supported by the finding that posterior insula is significantly correlated with behavioral measures of mindfulness trait levels in meditators in the direction of being more engaged in those meditators with higher mindfulness scores as measured by the MAAS and KIMS.

In the subset of participants who tended to accept the most unfair offers we found increased activity in bilateral DLPFC for controls, presumably reflecting the higher cognitive demands in order to overcome the emotional tendency to reject an unfair offer (Figure ​(Figure5).5). The involvement of the DLPFC in playing the Ultimatum Game like homo economicus is well known (Sanfey et al., 2003; Knoch et al., 2006). This result is also consistent with recent studies associating the DLPFC with self-control (Hare et al., 2009) which provide an anatomical base for successful self-regulation in rational controls. Yet the subset of rational meditators displayed activity in a different set of regions suggesting that they were not motivated by economic self-interest. This group recruited the somatosensory cortex, pSTC, and the parahippocampal gyrus. The somatosensory cortex is reported in studies requiring mapping of subjective feeling states arising from bodily responses (Critchley et al., 2004; Lutz et al., 2008b, 2009). Whereas the pSTC is involved in shifting attention to focus on another's perspective (Behrens et al., 2008; Hampton et al., 2008) as well as related to altruistic behavior (Harbaugh et al., 2007; Tankersley et al., 2007).

Meditators and controls also showed a marked difference in the activity of the anterior insula during the Ultimatum Game. The anterior insula has previously been linked to the emotion of disgust (Calder et al., 2001), and plays a key role in social norm violations, rejection, betrayal, and mistrust (Rilling et al., 2002; Spitzer et al., 2004; King-Casas et al., 2005; Montague and Lohrenz, 2007). In previous studies of the Ultimatum Game, anterior insula activity was higher for unfair offers, and the strength of its activity predicted the likelihood of an offer being rejected (Sanfey et al., 2003). In the present study, this was true for controls, but not for meditators. In control subjects, the anterior insula became active in response to unfair offers, and individuals with higher anterior insula activity tended to reject more of such offers (Figures ​(Figures4B,D).4B,D). However, in meditators, the anterior insula showed no significant activation for either fair or unfair offers, and there was no significant relationship between anterior insula activity and offer rejection (Figures ​(Figures4C,E).4C,E). Hence, meditators were able to uncouple the negative emotional response to an unfair offer, presumably by attending to internal bodily states reflected by activity in the posterior insula. This relationship was not apparent in control subjects. Meditators may not experience unfair offers as social norm violations, as suggested by their higher acceptance rates for asymmetric offers.

One limitation of the present study is that it employed a cross-sectional rather than longitudinal design. Hence, it was not possible to compare the behavior of the subjects before and after they started practicing meditation. Without this information, we cannot yet determine whether the meditators actually acquired a different behavioral profile through meditation experience, or whether the meditation group is simply a highly selected subset of a rare behavioral phenotype within the general population. Future work may help to determine whether a structured program of meditative training can produce the observed changes in social cognition and decision-making.

To summarize, we have identified a population of human beings with an unusual tendency to behave more like rational economic agents in the Ultimatum Game. Specifically, these experienced meditators are roughly twice as likely as controls to say yes to a free dollar over no money at all, rather than reject the reward due to its unfavorable social context. Proximately, meditators seem to avoid generating aversive responses in the anterior insula during unfair offers. In controls, such responses are powerful predictors of rejecting offers during social interaction, but in meditators, these responses are largely absent during the Ultimatum Game. Future studies should assess whether blunting of the high-level emotional representation of the anterior insula is an automatic interoceptive response based on acquired mindfulness skills. Our results suggest that the lower-level interoceptive representation of the posterior insula is recruited based on individual trait levels in mindfulness. When assessing unfair offers, meditators seem to activate an almost entirely different network of brain areas than do normal controls. Controls draw upon areas involved in theory of mind, prospection, episodic memory, and fictive error. In contrast, meditators instead draw upon areas involved in interoception and attention to the present moment.