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. Keywords: Emotional empathy; cognitive empathy; mirror neurons; inferior frontal gyrus; ventromedial prefrontal cortex Abbreviations: ANOVA = analysis of variance; BA = Brodmann area; EC = empathic concern scale; FS = fantasy scale; HC = healthy control; IFG = inferior frontal gyrus; IRI = Interpersonal Reactivity Index; MNS = mirror neuron system; PC = posterior lesion; PD = personal distress scale; PT = perspective-taking scale; ToM = Theory of Mind; VM = ventromedial prefrontal; WCST = Wisconsin Card Sorting Test

ARE EMOTIONAL DISPLAYS AN EVOLUTIONARY PRECURSOR TO COMPOSITIONALITY IN LANGUAGE?

Compositionality is a basic property of language, spoken and signed, according to which the meaning of a complex structure is determined by the meanings of its constituents and the way they combine (e.g., Jackendoff, 2011 for spoken language; Sandler 2012 for constituents conveyed by face and body signals in sign language; Kirby & Smith, 2012 for emergence of compositionality). Here we seek the foundations of this property in a more basic, and presumably prior, form of communication: the spontaneous expression of emotion. To this end, we ask whether features of facial expressions and body postures are combined and recombined to convey different complex meanings in extreme displays of emotions. There is evidence that facial expressions are processed in a compositional fashion (Chen & Chen, 2010). In addition, facial components such as nose wrinkles or eye opening elicit systematic confusion while decoding facial expressions of disgust and anger and fear and surprise, respectively (Jack et al., 2014), suggesting that other co-occurring signals contribute to their interpretation. In spontaneous emotional displays of athletes, the body – and not the face – better predicts participants’ correct assessments of victory and loss pictures, as conveying positive or negative emotions (Aviezer et al., 2012), suggesting at least that face and body make different contributions to interpretations of the displays. Taken together, such studies lead to the hypothesis that emotional displays are compositional - that each signal component, or possibly specific clusters of components (Du et al., 2014), may have their own interpretations, and make a contribution to the complex meaning of the whole. On the assumption that emotional displays are older than language in evolution, our research program aims to determine whether the crucial property of compositionality is indeed present in communicative displays of emotion

Compositionality in the language of emotion

Emotions are signaled by complex arrays of face and body actions. The main point of contention in contemporary treatments is whether these arrays are discrete, holistic constellations reflecting emotion categories, or whether they are compositional-comprised of smaller components, each of which contributes some aspect of emotion to the complex whole. We address this question by investigating spontaneous face and body displays of athletes and place it in the wider context of human communicative signals and, in particular, of language. A defining property of human language is compositionality-the ability to combine and recombine a relatively small number of elements to create a vast number of complex meaningful expressions, and to interpret them. We ask whether this property of language can be discerned in a more ancient communicative system: intense emotional displays. In an experiment, participants interpreted a range of emotions and their strengths in pictures of athletes who had just won or lost a competition. By matching participants' judgements with minutely coded features of face and body, we find evidence for compositionality. The distribution of participants' responses indicates that most of the athletes' face and body features contribute to displays of dominance or submission. More particular emotional components related, for example, to positive valence (e.g. happy) or goal obstruction (e.g. frustrated), were also found to significantly correlate with certain face and body features. We propose that the combination of features linked to broader components (i.e, dominant or submissive) and to more particular emotions (e.g, happy or frustrated) reflects more complex emotional states. In sum, we find that the corporeal expression of intense, unfiltered emotion has compositional properties, potentially providing an ancient scaffolding upon which, millions of years later, the abstract and constrained compositional system of human language could build

The neural networks underlying reappraisal of empathy for pain

Emotion regulation plays a central role in empathy. Only by successfully regulating our own emotions can we reliably use them in order to interpret the content and valence of others’ emotions correctly. In an functional magnetic resonance imaging (fMRI)-based experiment, we show that regulating one’s emotion via reappraisal modulated biased emotional intensity ratings following an empathy for pain manipulation. Task-based analysis revealed increased activity in the right inferior frontal gyrus (IFG) when painful emotions were regulated using reappraisal, whereas empathic feelings that were not regulated resulted in increased activity bilaterally in the precuneus, supramarginal gyrus and middle frontal gyrus (MFG), as well as the right parahippocampal gyrus. Functional connectivity analysis indicated that the right IFG plays a role in the regulation of empathy for pain, through its connections with regions in the empathy for pain network. Furthermore, these connections were further modulated as a function of the type of regulation used: in sum, our results suggest that accurate empathic judgment (i.e. empathy that is unbiased) relies on a complex interaction between neural regions involved in emotion regulation and regions associated with empathy for pain. Thus, demonstrating the importance of emotion regulation in the formulation of complex social systems and sheds light on the intricate network implicated in this complex process

Cognitive and affective components of Theory of Mind in preschoolers with oppositional defiance disorder : clinical evidence

The goal of the study was to examine the affective-cognitive components of Theory of Mind (ToM), in a community sample of 538 preschoolers, and more specifically in a subsample of 40 children diagnosed with ODD. The relationship between affective and cognitive ToM and some ODD clinical characteristics was examined. Children were assessed with structured diagnostic interviews and dimensional measures of psychopathology, impairment and unemotional traits. A measure based on eye-gaze was used to assess ToM. Mixed analysis of variance compared the mean cognitive versus affective scale scores and the between-subjects factor ODD. The association between ToM-scores and clinical measures was assessed through correlation models. Execution and reaction time to emotional and cognitive components of ToM tasks are different at age 5 in normally developing children. Oppositional Defiant children had slower response time when performing the affective mentalizing condition than children without the disorder. The correlation matrix between ToM-scores and clinical measures showed specific associations depending on the impaired ToM aspect and the psychological domain. Results may have clinical implications for the prevention and management of OD

The role of oxytocin in empathy to the pain of conflictual out-group members among patients with schizophrenia

Background.Oxytocin (OT) is associated with our ability to empathize and has been shown to play a major role in mediating social behaviors within the context of intergroup dynamics. Schizophrenia is associated with impaired empathy, and with a dysfunctional oxytocinergic system. The effect of OT on the empathic responses of patients with schizophrenia within the context of intergroup relationships has not been studied. The present study examined the effect of OT on the patients' empathic responses to pain experienced by in-group, conflictual out-group and neutral out-group members.Method.In a double-blind, placebo-controlled, within-subject cross-over design, the responses on the Pain Evaluation Task of 28 male patients with schizophrenia were compared to 27 healthy male controls. All participants received a single intranasal dose of 24 IU OT or placebo, 1 week apart.Results.OT induced an empathy bias in the healthy controls towards the conflictual out-group members. Although this effect was absent in the patient group, OT seems to heighten an empathic bias in the patient group towards the in-group members when rating non-painful stimuli.Conclusions.The study demonstrates that the administration of OT can result in empathic bias towards adversary out-group members in healthy controls but not in patients with schizophrenia. However, the OT-induced bias in both the patients (in the no-pain condition towards the in-group members) and the healthy controls (in the no-pain and pain conditions towards the adversary out-group) suggests that OT enhances the distinction between conflictual in-group and out-group members.</jats:sec

Mindblind eyes: an absence of spontaneous theory of mind in Asperger syndrome

Adults with Asperger syndrome can understand mental states such as desires and beliefs (mentalizing) when explicitly prompted to do so, despite having impairments in social communication. We directly tested the hypothesis that such individuals nevertheless fail to mentalize spontaneously. To this end, we used an eye-tracking task that has revealed the spontaneous ability to mentalize in typically developing infants. We showed that, like infants, neurotypical adults’ (n = 17 participants) eye movements anticipated an actor’s behavior on the basis of her false belief. This was not the case for individuals with Asperger syndrome (n = 19). Thus, these individuals do not attribute mental states spontaneously, but they may be able to do so in explicit tasks through compensatory learning

The role of simulation in intertemporal choices

One route to understanding the thoughts and feelings of others is by mentally putting one's self in their shoes and seeing the world from their perspective, i.e., by simulation. Simulation is potentially used not only for inferring how others feel, but also for predicting how we ourselves will feel in the future. For instance, one might judge the worth of a future reward by simulating how much it will eventually be enjoyed. In intertemporal choices between smaller immediate and larger delayed rewards, it is observed that as the length of delay increases, delayed rewards lose subjective value; a phenomenon known as temporal discounting. In this article, we develop a theoretical framework for the proposition that simulation mechanisms involved in empathizing with others also underlie intertemporal choices. This framework yields a testable psychological account of temporal discounting based on simulation. Such an account, if experimentally validated, could have important implications for how simulation mechanisms are investigated, and makes predictions about special populations characterized by putative deficits in simulating others

Theory of mind in utterance interpretation: the case from clinical pragmatics

The cognitive basis of utterance interpretation is an area that continues to provoke intense theoretical debate among pragmatists. That utterance interpretation involves some type of mind-reading or theory of mind (ToM) is indisputable. However, theorists are divided on the exact nature of this ToM-based mechanism. In this paper, it is argued that the only type of ToM-based mechanism that can adequately represent the cognitive basis of utterance interpretation is one which reflects the rational, intentional, holistic character of interpretation. Such a ToM-based mechanism is supported on conceptual and empirical grounds. Empirical support for this view derives from the study of children and adults with pragmatic disorders. Specifically, three types of clinical case are considered. In the first case, evidence is advanced which indicates that individuals with pragmatic disorders exhibit deficits in reasoning and the use of inferences. These deficits compromise the ability of children and adults with pragmatic disorders to comply with the rational dimension of utterance interpretation