Simone G. Shamay-Tsoory

Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions

Recent evidence suggests that there are two possible systems for empathy: a basic emotional contagion system and a more advanced cognitive perspective-taking system. However, it is not clear whether these two systems are part of a single interacting empathy system or whether they are independent. Additionally, the neuroanatomical bases of these systems are largely unknown. In this study, we tested the hypothesis that emotional empathic abilities (involving the mirror neuron system) are distinct from those related to cognitive empathy and that the two depend on separate anatomical substrates. Subjects with lesions in the ventromedial prefrontal (VM) or inferior frontal gyrus (IFG) cortices and two control groups were assessed with measures of empathy that incorporate both cognitive and affective dimensions. The findings reveal a remarkable behavioural and anatomic double dissociation between deficits in cognitive empathy (VM) and emotional empathy (IFG). Furthermore, precise anatomical mapping of lesions revealed Brodmann area 44 to be critical for emotional empathy while areas 11 and 10 were found necessary for cognitive empathy. These findings are consistent with these cortices being different in terms of synaptic hierarchy and phylogenetic age. The pattern of empathy deficits among patients with VM and IFG lesions represents a first direct evidence of a double dissociation between emotional and cognitive empathy using the lesion method.

Characterization of Empathy Deficits following Prefrontal Brain Damage: The Role of the Right Ventromedial Prefrontal Cortex

Impaired empathic response has been described in patients following brain injury, suggesting that empathy may be a fundamental aspect of the social behavior disturbed by brain damage. However, the neuroanatomical basis of impaired empathy has not been studied in detail. The empathic response of patients with localized lesions in the prefrontal cortex (n = 25) was compared to responses of patients with posterior (n = 17) and healthy control subjects (n = 19). To examine the cognitive processes that underlie the empathic ability, the relationships between empathy scores and the performance on tasks that assess processes of cognitive flexibility, affect recognition, and theory of mind (TOM) were also examined. Patients with prefrontal lesions, particularly when their damage included the ventromedial prefrontal cortex, were significantly impaired in empathy as compared to patients with posterior lesions and healthy controls. However, among patients with posterior lesions, those with damage to the right hemisphere were impaired, whereas those with left posterior lesions displayed empathy levels similar to healthy controls. Seven of nine patients with the most profound empathy deficit had a right ventromedial lesion. A differential pattern regarding the relationships between empathy and cognitive performance was also found: Whereas among patients with dorsolateral prefrontal damage empathy was related to cognitive flexibility but not to TOM and affect recognition, empathy scores in patients with ventromedial lesions were related to TOM but not to cognitive flexibility. Our findings suggest that prefrontal structures play an important part in a network mediating the empathic response and specifically that the right ventromedial cortex has a unique role in integrating cognition and affect to produce the empathic response.

Impaired affective theory of mind is associated with right ventromedial prefrontal damage

Objective:To examine the hypothesis that patients with ventromedial (VM) frontal lesions are impaired in the affective rather than cognitive facets of theory of mind (ToM). Background:Prefrontal brain damage may result in impaired social behavior, especially when the damage involves the orbitofrontal/VM prefrontal cortex (PFC). It has been previously suggested that deficits in ToM may account for such aberrant behavior. However, inconsistent results have been reported, and different regions within the frontal cortex have been associated with ToM impairment. Method:The performance of 26 patients with localized lesions in the PFC was compared with responses of 13 patients with posterior lesions and 13 normal control subjects. Three ToM tasks differing in the level of emotional processing involved were used: second-order false belief task, understanding ironic utterances, and identifying social faux pas. Results and Conclusions:The results indicated that patients with VM (but not dorsolateral) prefrontal lesions were significantly impaired in irony and faux pas but not in second-order false belief as compared with patients with posterior lesions and normal control subjects. Lesions in the right VM area were associated with the most severe ToM deficit. These results are discussed in terms of the cognitive and affective facets of “mind-reading” processes mediated by the VM cortex.

Intranasal Administration of Oxytocin Increases Envy and Schadenfreude (Gloating)

BACKGROUND Humans have a strong social tendency to compare themselves with others. We tend to feel envious when we receive less valuable rewards and may rejoice when our payoffs are more advantageous. Envy and schadenfreude (gloating over the others misfortune) are social emotions widely agreed to be a symptom of the human social tendency to compare ones payoffs with those of others. Given the important social components of envy and gloating, we speculated that oxytocin may have a modulating effect on the intensity of these emotions. METHODS Fifty-six participants participated in this double-blind, placebo-controlled, within-subject study. Following the administration of oxytocin or a placebo, participants played a game of chance with another (fake) participant who either won more money (envy manipulation), lost more money (schadenfreude manipulation), or won/lost equal amounts of money. RESULTS In comparison with the placebo, oxytocin increased the envy ratings during unequal monetary gain conditions involving relative loss (when the participant gained less money than another player). Oxytocin also increased the ratings of gloating during relative gain conditions (when the participant gained more money than the other player). By contrast, oxytocin had no effect on the emotional ratings following equal monetary gains nor did it affect general mood ratings. CONCLUSIONS These results suggest that the oxytocinergic system is involved in modulating envy and gloating. Thus, contrary to the prevailing belief that this system is involved solely in positive prosocial behaviors, it probably plays a key role in a wider range of social emotion-related behaviors.

Neuroanatomical and neurochemical bases of theory of mind

This paper presents a novel neurobiological model of theory of mind (ToM) that incorporates both neuroanatomical and neurochemical levels of specificity. Within this model, cortical and subcortical regions are functionally organized into networks that subserve the ability to represent cognitive and affective mental states to both self and other. The model maintains that (1) cognitive and affective aspects of ToM are subserved by dissociable, yet interacting, prefrontal networks. The cognitive ToM network primarily engages the dorsomedial prefrontal cortex, the dorsal anterior cingulate cortex and the dorsal striatum; and the affective ToM network primarily engages the ventromedial and orbitofrontal cortices, the ventral anterior cingulate cortex, the amygdala and the ventral striatum; (2) self and other mental-state representation is processed by distinct brain regions within the mentalizing network, and that the ability to distinguish between self and other mental states is modulated by a functionally interactive dorsal and ventral attention/selection systems at the temporoparietal junction and the anterior cingulate cortex; and (3) ToM functioning is dependent on the integrity of the dopaminergic and serotonergic systems which are primarily engaged in the maintenance and application processes of represented mental states. In addition to discussing the mechanisms involved in mentalizing in terms of its component processes, we discuss the models implications to pathologies that variably impact ones ability to represent, attribute and apply mental states.

Impairment in Cognitive and Affective Empathy in Patients with Brain Lesions: Anatomical and Cognitive Correlates

ABSTRACT The present study was designed to examine the degree of impairment in cognitive and affective empathy among patients with focal brain lesions, and the contribution of specific cognitive abilities (such as cognitive flexibility and processing of emotional information), to empathy. The cognitive and affective empathic response of patients with localized prefrontal lesions (n=36) was compared to responses of patients with parietal lesions (n=15) and healthy control subjects (n=19). Results indicate that patients with prefrontal lesions (especially those with lesions involving the orbitoprefrontal and medial regions) were significantly impaired in both cognitive and affective empathy as compared to parietal patients and healthy controls. When the damage was restricted to the prefrontal cortex, either left- or right-hemisphere lesions resulted in impaired empathy. However, when the lesion involved the right hemisphere, patients with parietal lesions were also impaired. The pattern of relationships between cognitive performance and empathy suggested dissociation between the cognitive correlates of affective and cognitive empathy.

The Neuroanatomical Basis of Understanding Sarcasm and Its Relationship to Social Cognition

The authors explored the neurobiology of sarcasm and the cognitive processes underlying it by examining the performance of participants with focal lesions on tasks that required understanding of sarcasm and social cognition. Participants with prefrontal damage (n=25) showed impaired performance on the sarcasm task, whereas participants with posterior damage (n=16) and healthy controls (n=17) performed the same task without difficulty. Within the prefrontal group, right ventromedial lesions were associated with the most profound deficit in comprehending sarcasm. In addition, although the prefrontal damage was associated with deficits in theory of mind and right hemisphere damage was associated with deficits in identifying emotions, these 2 abilities were related to the ability to understand sarcasm. This suggests that the right frontal lobe mediates understanding of sarcasm by integrating affective processing with perspective taking.

The Social Salience Hypothesis of Oxytocin

Oxytocin is a nonapeptide that also serves as a neuromodulator in the human central nervous system. Over the last decade, a sizeable body of literature has examined its effects on social behavior in humans. These studies show that oxytocin modulates various aspects of social behaviors such as empathy, trust, in-group preference, and memory of socially relevant cues. Several theoretical formulations have attempted to explain the effects of oxytocin. The prosocial account argues that oxytocin mainly enhances affiliative prosocial behaviors; the fear/stress theory suggests that oxytocin affects social performance by attenuating stress; and the in-/out-group approach proposes that oxytocin regulates cooperation and conflict among humans in the context of intergroup relations. Nonetheless, accumulating evidence reveals that the effects of oxytocin are dependent on a variety of contextual aspects and the individuals characteristics and can induce antisocial effects including aggression and envy. In an attempt to reconcile these accounts, we suggest a theoretical framework that focuses on the overarching role of oxytocin in regulating the salience of social cues through its interaction with the dopaminergic system. Crucially, the salience effect modulates attention orienting responses to external contextual social cues (e.g., competitive vs. cooperative environment) but is dependent on baseline individual differences such as gender, personality traits, and degree of psychopathology. This view could have important implications for the therapeutic applications of oxytocin in conditions characterized with aberrant social behavior.

Double dissociation between cognitive and affective empathy in borderline personality disorder

We sought to characterize the cognitive and affective empathic abilities of patients with borderline personality disorder (BPD). While controls showed higher cognitive as compared with affective empathy scores, the BPD group demonstrated the opposite pattern. These results suggest that a dysfunctional pattern of empathic capacity may account for behavioral difficulties in BPD.

The ventromedial prefrontal cortex is involved in understanding affective but not cognitive theory of mind stories

Abstract Lesion and neuroimaging studies have implicated the medial frontal lobes as playing an important role in our ability to predict other peoples behavior by attributing to them mental states, such as beliefs, intention and emotion (termed “Theory of Mind”; ToM). However, recent studies have challenged these findings by highlighting the role of the temporal–parietal junction (TPJ) in ToM. In the present study, we tested the hypothesis that the ventromedial (VM) prefrontal cortex plays a unique role in affective ToM reasoning rather than a general role in ToM. We compared the performance of patients with lesions localized either in the VM, dorsolateral, TPJ, or superior parietal to healthy controls, with a battery of naturalistic affective and cognitive ToM stories (about false beliefs, false attribution, irony and lies). Patients with VM damage were impaired at providing appropriate mental state explanations for the affective ToM stories, compared to healthy controls and patients with posterior damage. In the VM group, performance in the affective ToM was significantly impaired as compared to cognitive ToM stories. Furthermore, in the VM group, ratings of levels of emotionality of each story suggested that levels of affective load correlated with number of errors in the stories, indicating that the more the emotional load involved in the story the greater the difficulty posed for the subjects in this group.