The Green-eyed Monster and Malicious Joy: The Neuroanatomical Bases of Envy and Gloating (Schadenfreude)

Simone G. Shamay-Tsoory; Yasmin Tibi-Elhanany; Judith Aharon-Peretz

Disclosures

Brain. 2007;130(6):1663-1678. 

In This Article

Discussion

In the present study, we assessed basic ToM and emotion recognition capacities as well as the ability to understand 'fortune of others' emotions in patients with localized brain lesions. We speculated that the ability to understand particularly competitive emotions, such as gloating and envy, is related to a broader mentalizing and perspective taking capacities and that, therefore, lesions in the VM may impair the ability to understand these emotions. Our results support this hypothesis by showing selective impairment in recognizing gloating and envy but not identification in patients with VM damage. Contrary to our initial hypothesis, these patients did not show impaired performance on basic first order ToM tasks based on eye gaze. However, in accordance with our hypothesis, it was shown that VM patients did show impaired perspective taking abilities.

Furthermore, correlation analysis indicated that the perception of 'fortune of others' emotions was related not only to ToM but also to perspective-taking abilities. The ability to understand envy and gloating, but not identification, was particularly related to perspective taking scales.

These results are consistent with findings that children with autism reveal a less coherent understanding of jealousy (Bauminger, 2004), an emotion with characteristics similar to envy that may co-occur in equivalent situations (Parrot, 1991). Since ToM difficulties in autism are well established (Klin et al., 2003), it is likely that emotions such as envy and gloat which involve social comparisons will be perceived differently in these individuals.

Indeed, the involvement of the VM in 'fortune of others' emotion is consistent with its role in ToM. As already mentioned, previous neuroimaging studies (Baron-Cohen et al., 1994; Fletcher et al., 1995; Goel et al., 1995; Gallagher et al., 2000; Calarge et al., 2004; Grezes et al., 2004) and lesion studies (Stone et al., 1998; Stuss et al., 2000; Rowe et al., 2001) reported findings concerning the contribution of specific PFC regions to ToM abilities. In the present study, only patients with MIX (DLC and VM) damage showed impaired basic ToM abilities. The VM patients were not different from the HC in the basic ToM task although they had a poorer performance and they were impaired in the perspective taking task. The ToM task used in the present study represents a first order mentalizing inference. In accordance with these results, it has been shown that patients with damage that encompasses the VM do not usually show impaired first order ToM (Stone et al., 1998). It has been further suggested that the VM is involved in complex, more affective, mentalizing conditions rather than in basic ToM (Stone et al., 1998; Shamay-Tsoory et al., 2005). Furthermore, a report by Mitchell et al. (2005) demonstrates that the VM may guide the understanding of others' complex mental states through affective 'simulation' processing. Additional support for the role of the VM may be found in the intimate connections of the VMPFC with the anterior insula, temporal pole, inferior parietal region and amygdala, which place this region in a position to integrate limbic input with complex frontal information that can consequently be used to understand complicated social emotions.

While VM damage was associated with impaired recognition of both gloating and envy, recognition of gloating involved additionally lesions in the inferior parietal lobule. In line with this finding, recent experimental reports suggest that the temoporo-pariental junction and the superior temporal sulcus (STS) play a prominent role in attribution of beliefs (Apperly et al., 2004; Samson et al., 2004). The inferior parietal area was also found to be particularly important in tasks that involved emotional perceptual analysis (Herberlein et al., 2004). Moreover, Chaminade and Decety (2002) suggested that a neural network that involves the inferior parietal cortex and the prefrontal cortex plays a special role in the essential ability to distinguish the self from others, and in the way the self represents the other. In a later study, Ruby and Decety (2004) examined the difference between adopting first- and second-person perspective in response to situations involving social emotions. The authors reported an increase in the haemodynamic response in the medial PFC, the STS and the right inferior parietal lobe in third-person versus first-person perspectives.

Gloating (schadenfreude), similarly to envy, is a social comparative emotion that involves both the perception of another's negative emotion and, in consequence, one's own positive emotion. In the present study, understanding of gloating involved perspective taking abilities. Therefore, it is not surprising that lesions in the mentalizing network that include the VM and the inferior parietal lobe were associated with impaired identification of gloating. One may speculate whether gloating which appears to be less basic or automatic than envy may involve more prominent participation of structures from the mentalizing network.

The inferior parietal lobe including the STS has been also associated with determination of the direction of the other person's gaze (Wicker et al., 1998; Hoffman and Haxby, 2000). Additionally, Calder et al. (2002) have suggested that the medial PFC regions are also involved in gaze direction. Furthermore, the authors demonstrated a considerable degree of overlap between the medial frontal areas involved in eye gaze processing and theory of mind tasks (Calder et al., 2002). The task used in the present study involved recognition of envy and gloating based on different cues, including eye gaze direction. Given the role of the medial PFC and the STS in detection of eye gaze, it would be expected that the VM and the INF groups will not show advantage in the gaze versus no-gaze conditions. However, our results indicated that the pattern of accuracy in gaze and in straight ahead conditions did not differ between groups. Overall, all participants performed better in the gaze direction conditions and even patients with inferior parietal damage and patients with medial prefrontal damage where doing better when the eyes were directed towards the protagonist. We believe that the directed eye-gaze conditions were easier to interpret since the stimuli included an additional cue that was not included in the straight ahead conditions (the eye-gaze clue). Since the difference between these two conditions does not interact with the group variable, it may support our assumption that the significant differences observed above are not due to the difference between the two conditions.

Another difference between gloating and envy was manifested in the asymmetry of lesions associated with impaired recognition of these emotions. While left-sided lesions were associated with impaired understanding of gloating, right sided lesions were more related to recognition of envy. Several attempts have been made to explain the contribution of hemispheric lateralization for emotional processing. While traditional views have hypothesized that the right hemisphere has a central role in modulating all forms emotional processing (Mandal et al., 1996), the 'valence hypothesis' suggested dissociable roles for the right and left hemispheres in modulating emotions. According to this formulation, the left hemisphere is dominant for positive emotions (such as happiness) and the right hemisphere is dominant for negative emotions (such as sadness) (Davidson 1992).

While envy is usually a very unpleasant emotion (Parrot, 1991), a misfortune befalling an envied other can be even pleasing as it eliminates the basis of envy (inferiority) (van Dijk et al., 2006). Gloating involves a conflict between our pleasure or positive evaluation of the situation and the other's misfortune or negative evaluation of the other person, raising the competitive aspect of this emotion (Ben-Zeev, 2000). The favourable comparison that evokes this pleasure therefore points to both the mentalizing processing that underlies this emotion and the positive aspects of experiencing it. On the other hand, it has been suggested that the experience of envy is complex and engages particularly negative primary emotions, such as anger, as well as other emotions, such as sadness and fear (Parrott, 1991). In the present study, lesions particularly in the right VM were associated with impaired understanding of envy. In line with this, a recent case study suggests that pathological jealousy (Othello syndrome) may be related to right orbitofrontal damage (Numero et al., 2006). Blair and Cipolotti (2000) have also emphasized the role played by the right VM in responding to negative emotions, such as anger. The authors reported a single case study of a patient suffering from PFC damage including the VM who specifically showed impairment in the recognition of, and autonomic responding to, angry and disgusted expressions. The authors concluded that this impairment was due to a reduced ability to generate expectations of others' negative emotional reactions, anger in particular, and proposed that the right VM may be implicated specifically either in the generation of these expectations or the use of these expectations to suppress inappropriate behaviour. According to this hypothesis, impaired recognition of envy is based on these patients' deficits in anticipating the emotional reactions of other people, particularly negative reactions.

Taken together, Davidsons' 'valence' theory appears to be compatible with our results regarding asymmetry of lesions, as patients with left-sided lesions were doing poorly in the gloating conditions (positive emotion) and patients with right-sided lesions were doing worse in the envy conditions (negative emotion). Nevertheless, the results of the present study regarding lesion asymmetry should be treated with caution since the standard deviations of groups were very high and since the INF group included only patients with left lesions. Additionally, it would be expected that patients with bilateral damage should behave similarly to patients with unilateral damage. As may be seen in Fig. 5, in the gloating condition, indeed the bilateral patients were as impaired as the left-lesioned patients. However, in the envy condition the bilateral group was even better than the patients with right hemisphere lesion. These inconsistencies which may reflect the high standard deviations, somewhat undermines the conclusions regarding lesion asymmetry.

The ventromedial prefrontal cortex is thought to be important in various complex behaviours. Indeed, neurological research has demonstrated that patients with VM lesions exhibit several impairments such as in inhibition (Rolls et al., 1994), in decision-making (Bechara et al., 1998; Fellows et al., 2007), in empathic processing (Shamay-Tsoory et al., 2003) and in the experience of regret (Camille et al., 2004). One may wonder what are the common characteristics between these behavioural deficits and the impairments in understanding gloating and envy that were observed in the present study.

A common denominator that these emotions and behaviours have is that all are complex, and involve integration and comparisons between several perspectives. While empathy involves decoupling of observers' and targets' perspectives, 'fortune of others' emotions also involve comparison between observers' and targets' emotion or mental state. The experience of regret, on the other hand, requires comparison between the observers' current outcome and a different potential outcome (Camille et al., 2004). Comparisons between options are also necessary when making decisions (Bechara et al., 1998). It might, therefore, be assumed that the VM is engaged in situations where two or more possibilities must be processed simultaneously, such as one's own, as well as the other's, emotional mental state. Moreover, perhaps, it is the lack of inhibition of their own perspective that interferes with these patients' ability to process simultaneously their own and the other perspectives.

Indeed, the 'inhibition hypothesis', proposed by Sahakian and colleagues (Plaisted and Sahakian, 1997; Rahman et al., 1999) suggests that damage to the prefrontal cortex results in loss of inhibitory control over inappropriate responses to any current situation. Rahman et al. (1999) examined patients with frontal variant of frontotemporal dementia, and found that these patients' aberrant social behaviour was related to the inability of their ventromedial inhibitory mechanisms to suppress inappropriate behaviours elicited by the immediate environment. The authors suggest that these patients' behaviour is predominantly controlled by immediate emotional evaluation of the stimuli, and therefore, such disinhibition disrupts the selection of alternative and more appropriate action plans which are dictated by long-term goals.

This view may regard the deficit in recognizing 'fortune of others' emotion observed in patients with VM damage as stemming from a difficulty in inhibiting their own perspective and comparing alternative perspectives of others. Envy and gloating are complex emotions that involve social comparison. While envy is related to comparison between the observers' negative situation and the protagonists' positive situation, gloating is related to comparison between observers' positive situation and the protagonists' negative situation.

Additionally, it appears that both gloating and envy are more related to social comparisons than identification, since they are evoked particularly in competitive situations. Similarly to envy and gloating, identification encompasses a comparison process between the other and self, but to a lesser extent. As such, it requires less mentalization efforts. Recognition of identification might be easier as it involves spotting visual similarities (information processing reason) and since it requires less mentalization efforts. It may be argued that while gloating and envy involve understanding of rivals in competitive situations, understanding of identification may involve understanding of a collaborative protagonist.

Indeed, in an fMRI study, Decety et al. (2004) scanned individuals playing a computer game, according to a set of predefined rules, either in cooperation with or in competition against another person. The authors reported that the fronto-parietal network was involved in both cooperation and competition conditions. Yet, in competition, compared to the collaboration condition, activations were observed particularly in the inferior parietal and medial prefrontal cortices. These cortices have been shown to be consistently involved in mentalizing. Therefore, the authors argued that competitive situations recruit the mentalizing network more prominently to evaluate the rival response. The results of Decety and his colleagues are in accordance with the present study and further highlight the involvement of the VM and the inferior parietal lobule in competitive emotions.

While substantive treatment of this issue is well beyond the scope of the current study, it may be interesting to speculate whether competitive emotions encourage emotional mentalizing processing, and thereby engage more ventral PFC cortices. Indeed, the intimate connections of the VMPFC with limbic structures place it in a position to evaluate and regulate incoming limbic information which can consequently be used to perceive social emotions. In agreement with this assumption, two studies have highlighted the role of fronto-limbic circuits in understanding social emotions. While Adolphs et al. (2002) report that patients with unilateral or bilateral amygdala damage were impaired when recognizing social emotions, Shaw et al. (2005) recently reported that damage to either the left or the right amygdala was associated with impairment in recognition of both social and cognitive expressions. Lesions to the entire right prefrontal cortex led to a specific deficit in recognizing complex social expressions with a negative valence.

There are several limitations that need to be acknowledged and addressed regarding the present study. The first limitation concerns patients' variability in lesions aetiologies. Although most of our sample included patients with traumatic injury, the proportion of these patients is higher in the VM and MIX groups (but not in the INF group). Although patients with MRI evidence of diffuse axonal injury were excluded from the study, one cannot be completely certain that none had diffuse damage that was not observed in MRI. MRI identifies the injury using signs of oedema, which may not be present in all cases of diffuse damage. Patients with MIX damage showed deficits in several cognitive functions as well as in recognizing 'fortune of others' emotions. Additionally, their reaction time in all conditions was slower than the other groups even in the physical conditions. Although their lesion sizes did not differ significantly from the rest of the groups, it appears that they had slightly larger lesions that, perhaps, involved diffuse damage.

Finally, one may argue that the observed impairments in perception of envy and gloat in comparison to identification or basic ToM may simply represent the relatively greater complexity of these conditions. To rule out this possibility, we assessed whether perception of 'fortune of others' emotions related to IQ, years of education or impaired executive functions. It is important to note that the task, relying on visual presentation, involved minimal memory of executive load. In addition, patient difficulties in the 'fortune of others' emotions did not correlate with any measurement of executive function nor with intellectual functioning, suggesting that identifying these emotions was independent of other cognitive functions. Indeed, many authors from a variety of theoretical perspectives have argued that mentalizing involves a domain-specific cognitive module (e.g. Sperber, 2000). The lack of correlation between these emotions and cognitive functioning is consistent with this hypothesis, but any such conclusion must be regarded with caution. Nonetheless, it may be interesting to speculate whether the ability to understand 'fortune of others' emotion may simply represent a higher order affective ToM. Indeed, in the 'fortune of others' conditions in our study, participants had to make second-order affective inferences: how a character feels in regard to a protagonist's emotional state. This suggestion, however, may be refuted by the lack of effect in the identification condition. Future studies may help elucidate this point using tasks designed to assess the experience rather than recognition of these emotions.

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