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Indeed, without such control, the mere activation of the perception-action mechanism, including the associated autonomic and somatic responses, could lead to emotional contagion or emotional distress. Such regulation is also important in modulating one's own vicarious emotion so that it is not experienced as aversive. Previous research indicates that emotion regulation is positively related to feelings of concern for the other person [ 97 , 99 ].
In contrast, individuals who experience their emotions intensely, especially negative emotions, are prone to personal distress, i. Chronic incapacity to suppress negative emotion may be a key factor in anxiety, and aggressive and violent behavior [ ]. A circuit that includes several interconnected regions of the prefrontal cortex, the amygdala, hippocampus, ACC, insular cortex, and ventral striatum has been acknowledged to be implicated in various aspects of emotion regulation [ ].
In neurology, the term "self-regulatory disorder" has been coined for the syndrome exhibited by patients with ventromedial prefrontal cortex damage particularly on the right. This syndrome is defined as the inability to regulate behavior according to internal goals and constraints [ ]. It arises from the inability to hold a mental representation of the self on-line and to use this self-related information to inhibit inappropriate responses.
Interestingly, the orbitofrontal, ventromedial, and dorsolateral cortices have been reported in the neurological literature to be involved in empathy. Notably, damage to the orbitofrontal is associated with a wide range of social emotional deficits, including impaired social judgment and disinhibited behavior. For instance, Stone, Baron-Cohen and Knight [ ] found that patients with bilateral lesions of the orbitofrontal cortex are impaired in the "faux pas" task.
This task requires both an understanding of false or mistaken belief and an appreciation of the emotional impact of a statement on the listener. A study conducted by Stuss and colleagues [ 94 ] extended this finding by showing that only lesions in the right orbitofrontal produce such a deficit. In addition, a number of clinical studies reported a relationship between the deficit in empathy and poor performance of cognitive flexibility tasks among patients with lesions in the dorsolateral regions, whereas those with orbitofrontal cortex lesions were more impaired in empathy but not in cognitive flexibility [ , ].
The ventromedial prefrontal cortex with its reciprocal connections with brain regions involved in emotional processing amygdala , memory hippocampus , and executive functions dorsolateral prefrontal cortex plays also a major role in emotion regulation. Damasio's [ ] somatic markers hypothesis, which posits that memories of somatic states that are associated with particular experiences or outcomes are stored in the ventromedial prefrontal cortex, is directly relevant in the process of affective regulation.
Recent work by Shamay-Tsoory and colleagues [ ] supports this hypothesis. They tested patients with lesions of the ventromedial prefrontal cortex or dorsolateral prefrontal cortex with three theory-of-mind tasks second-order beliefs and faux pas that differed in the level of emotional processing involved. They found that patients with ventromedial lesions were most impaired in the faux pas task but presented normal performance in the second-order belief tasks. The authors further argued that in order to detect faux pas, one is required not only to understand the knowledge of the other but also to have empathic understanding of other's feelings.
Finally, the ACC is part of a circuit involved in a form of attention that serves to regulate both cognitive and emotional processing [ ]. Its lesion produces a host of symptoms, which include apathy, inattention, dysregulation of autonomic functions, and emotional instability. Neuroimaging research has recently begun to investigate neural mechanisms involved in affective reappraisal, a cognitive strategy used to regulate emotion.
For instance, an fMRI experiment on emotion reappraisal has detected co-activation of the lateral prefrontal and medial prefrontal cortices and decreased activity in the medial orbitofrontal cortex and the amygdala [ ]. Another study identified a circuit composed of the right orbitofrontal, right dorsolateral prefrontal cortex and anterior cingulate for voluntary suppression of sadness [ ].
One recent functional MRI study investigated whether observation of distress in others leads to empathic concern and altruistic motivation or to personal distress and egoistic motivation [ ]. In this experiment behavioral measures and event-related functional MRI were used to explore the effect of perspective taking and emotion regulation on empathy processing while participants watched video-clips of patients expressing pain resulting from medical treatment. Video-clips were presented either with the instruction to imagine the feelings of the patient "imagine other" or to imagine oneself to be in the patient's situation "imagine self".
Need for emotion regulation was manipulated by providing information that the medical treatment had or had not be successful.
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Behavioral measures clearly demonstrated that imagery and reappraisal instructions were effective. Neuroimaging data showed consistent activity in the insular cortex and anterior medial cingulate cortex aMCC. Graded responses related to the imagery instructions were observed in dorsal insula, aMCC, and left and right parietal cortex.
Emotion regulation resulted in hemodynamic changes in anterior paracingulate cortex, subgenual ACC, orbitofrontal, and right temporal cortex. These findings support the view that the response to the pain of others can be modulated by cognitive and motivational processes. These processes influence whether observing a conspecific in need of help will result in empathic concern, an important prerequisite for helping behavior.
Overall, the capacity to regulate emotions is an important aspect of our ability to interact appropriately with other people. The prefrontal cortex is highly differentiated in terms of cell structures and patterns of interconnectivity with other cortical subsystems. In line with this fact, neuroimaging studies suggest that specific systems interact in generating emotion regulation.
Social neuroscience is beginning to shed light on the physiological and neural mechanisms subserving the various emotion regulation strategies that allow us to better understand our conspecifics. The way our nervous system is organized and tailored by evolution provides the basic biological mechanism for resonating with the behaviors of others. This mechanism driven by the common coding between perception and action provides the default mode to implicitly relate to others and may be responsible for the projective tendency to ascribe one's own characteristics and self-traits to others [ 38 , ].
However, this tendency needs to be regulated or calibrated for appropriate social interaction [ 17 ]. This requires additional computational mechanisms, including monitoring and manipulation of internal information generated by the activation of the shared representations between the self and the other. In addition, there are limits to the extent to which the experiences are isomorphic, as demonstrated by the non-overlapping neural areas. This idea is far from new e. For instance, Ax [ ] in had suggested that empathy might be thought of as an autonomic nervous system state, which tends to simulate that of another person.
This idea fits neatly with the notion of embodiment, which refers both to actual bodily states and to simulations of experience in the brain's modality-specific systems for perception, action, and the introspective systems that underlie conscious experiences of emotion, motivation and cognitive operations [ ]. However, this simulation is not exclusively under automatic management and, at least in humans, falls under conscious control.
This makes empathy, as described here, an intentional capacity. Without self-awareness and emotion regulation processing, there may be no true empathy. The automatic activation of shared representations would instead be associated with anxiety and discomfort and would lead to responses oriented to the self e. Such a formulation is also consistent with the observation that prosocial behaviors, which stem from empathy, emerge during child development in parallel with self-conscious emotions [ ].
These emotions require self-evaluation and comparison with others, as well as some form of emotion regulation. Forming an explicit representation of another person's feeling, as an intentional agent, thus necessitates additional computational mechanisms beyond the shared representation level. This requires that second-order representations of the other are available to consciousness a decoupling mechanism between first-person information and second-person information [ ].
Thus human empathy cannot be described only as a simple resonance of affect between the self and other. Indeed, empathy is both about sharing and understanding the emotional state of others in relation to oneself. The capacity for two people to resonate with each other emotionally, prior to any cognitive understanding, is the basis for developing shared emotional meanings, but is not sufficient for empathy.
Such an understanding goes beyond this reflex-like response. It involves an explicit representation of the subjectivity of the other and a minimal self-other distinction. Recent neuroimaging investigations of the perception of pain in others support such a view e. Indeed, all these studies have shown that part of the neural network including the anterior cingulate cortex and the anterior insula mediating self-experienced pain is shared when empathizing or observing the pain in others, and also that non-overlapping aspects within these regions are specifically activated for the self or the other.
This supports the idea that personal and vicarious experiences at some level differ physiologically [ ] and result in qualitatively distinct responses. Finally, empathy also necessitates emotion regulation in which the ventral prefrontal cortex, with its strong connections with the limbic system, dorsolateral, and medial prefrontal areas, plays an important role.
We believe that a greater understanding of the underlying computational processes and their neural underpinnings can contribute to a better characterization of empathy disorders in psychopathology. The empirical evidence reviewed here illuminates the neurobiological underpinnings of the different components of empathy and strongly suggests the view that lesion to different cortical and sub-cortical structures or circuits can lead to an alteration of empathy or even a lack of empathic ability.
However qualitative differences exist in the nature of underlying deficits, and this supports our assertion that empathy entails a number of distinct components mediated by isolable neural systems. It is possible that psychopathological disorders such as antisocial personality disorders, schizophrenia or autism, in which social breakdown are predominant for various reasons, will benefit from this integrative model.
The clinical imperative is to understand the factors that lead to these conditions, uncover what neural mechanisms may underlie these deficits, and hence treat them. Many psychiatric disorders are associated with deficits or even lack of empathy. Psychopathy is a disorder that encapsulates the essence of a lack of empathy. The classification of psychopathy, introduced by Hare [ ], involves both affective-interpersonal e.
Empathy deficit in antisocial personality disorder has been suggested to come from a reduced ability to feel other people's emotional state, and more so for sadness and fear [ ]. This deficit has been ascribed to a dysfunction in the amygdala of developmental origin. This view is compatible with the fact that individuals with this disorder have generally intact executive functions and can successfully complete Theory of Mind tasks [ ].
There is also evidence to suggest that psychopathic patients do well on the 'Reading the Mind in the Eyes' task by simply asking them to focus on the eyes of other target people [ ]. Therefore, their lack of empathy could be related to disrupted affective processing rather than an inability, for instance, to adopt the perspective of others. In fact, people with antisocial personality disorders are probably good at perceiving others' intentions, while disregarding the emotional content, however, and thus may take advantage of it.
This is precisely what the research of Mealey [ ] suggests. The psychopath cannot simulate emotions he cannot experience, and must rely exclusively on cognitive inputs to his theory of mind mechanism. An interesting single case of acquired sociopathy has been reported by Blair and Cipolotti [ ]. The authors investigated an individual, J. While J. Notably, he was both impaired in the recognition of emotional expressions happiness, anger, disgust and sadness and in the attribution of emotional states to others fear, anger and embarrassment.
His ability to attribute mental states to others was preserved. His SRC responses to negative emotional expressions were reduced. Blair and Cipolotti argued that the distinctive features of the acquired sociopathy of J. Antisocial personalities are often reported to perform poorly on neuropsychological tests of executive functioning e. Executive functions are considered necessary for socially appropriate conduct, and in our framework, they contribute to empathy through self-regulation. In line with this view, a meta-analysis of thirty-nine studies yielding a total of participants helped to clarify the relation between antisocial behavior and executive functions [ ].
The results of this meta-analysis indicate that there is a robust and statistically significant relation between executive functions and antisocial behavior. The authors were unable to subdivide executive function measure in terms of their associations with different brain regions e. Interestingly, Blair [ ] proposed that people with antisocial personalities have a disruption of a violence inhibition mechanism that is normally triggered by distress cues of others, and this aspect belongs to executive functioning. Clinical and forensic research usually distinguish "affective" or "reactive" aggression, which is a response to physical or verbal aggression initiated by others with violence that is relatively uncontrolled and emotionally charged, from a "predatory" or "instrumental" cold-blooded aggression, which is a controlled, purposeful aggression lacking in emotion that is used to achieve a desired goal [ ].
Our model of empathy predicts that the former type of personality would lack executive control particularly self-control and emotion regulation, whereas the latter personality would have some dysfunctions in sharing feelings with others. Interestingly, measurements of glucose metabolism in two groups of affective and predatory murderers have shown that the first group has lower prefrontal activity, and the second group has similar prefrontal activity as compared to controls, but lower activity at the subcortical level including the amygdala [ ]. Borderline personality disorder BPD is characterized by emotional dysregulation, "splitting" or black and white thinking, and fluctuating and chaotic interpersonal relationships, including pervasive instability in mood, interpersonal relationships, identity, and behavior, as well as a disturbance in the individual's sense of self.
They often have severe deficiencies in impulse control, which results in self-destructive behaviors, burst aggression to others. In accord with this notion, patients with BPD showed enhanced amygdala activation in response to standardized emotionally aversive pictures [ ]. Donegan et al [ ] reported that BPD patients showed significantly greater left amygdala activation to the facial expressions of emotion compared with healthy subjects, and in post-scan debriefing some patients had difficulty disambiguating neutral faces or found them threatening.
A FDG-PET study demonstrated a tight coupling of glucose metabolic activity in resting condition between right OFC and ventral amygdala in healthy subjects with dorso-ventral differences in amygdala circuitry, but not present in BPD group, without any significant differences in amygdala volumes or metabolism between BPD patients and controls.
All these studies described above suggest that BPD includes 'hyper-sensitivity' in the limbic system primarily including the amygdala and a hypofunction of the prefrontal cortices. In the context of empathy, both emotional and cognitive function and interaction between two components may be altered in patients with BPD. These notions are in line with their self-oriented immature level of empathy e. People with narcissistic personality disorder NPD also have difficulty recognizing the needs and feelings of others, and are dismissive, contemptuous and impatient when others share or discuss their concerns or problems.
They are also oblivious to the hurtfulness of their behavior or remarks, show an emotional coldness and a lack of reciprocal interest, exhibit envy especially when others are accorded recognition , have an arrogant, disdainful and patronizing attitude, and are quick to blame and criticize others when their needs and expectations are not met.
Although there is scarcely neuroscientific evidence in NPD c. It was shown that abusive parents are more likely to lack parental warmth, compassion and concern and experience difficulty in perspective taking, and at the same time, have less self-confidence, a greater lack of impulse control and are more narcissistic [ ]. It is assumed that patients with NPD might have reduced affective neural component of empathy. Further evidences are needed to validate this hypothesis. Autistic spectrum disorders ASD is a severe developmental disorder where there is marked neuro-cognitive impairment.
Children with ASD display a broad range of social communication deficits, and most scholars agree that a lack of empathy taken in a very broad sense prominently figures amongst them. The underlying cause of the empathy deficit is, however, more controversial. For instance, Baron-Cohen and colleagues [ ] put forward the hypothesis that the social impairment in autism arises from a failure of a mentalizing mechanism a theory-of-mind module.
Other authors believe that children with autism have a hard time feeling and expressing emotion, and that this basic deficit prevents them from engaging in social interactions [ ]. Rogers and Pennington [ ] suggested a cascade model of autism in which the lack of certain aspects of interpersonal development at every previous stage disrupts certain developments in the following stage. These authors view early imitation skills, emotion sharing, and theory of mind as increasingly complex expressions of the ability to form and coordinate certain representations of self and other.
These representations are then used to guide the planning and execution of one's own behavior. Finally, Dawson [ ] proposed that autism involves impairment in attentional functioning for social stimuli e. She hypothesized that, because social stimuli are complex, variable, and unpredictable, children with autism have difficulty processing and representing them and, therefore, their attention is not naturally drawn to such stimuli [ ]. Several studies have examined behavioral and autonomic responses of children with autism who look at adults depicting facial emotional expressions see [ ] for a critical review.
While most studies report that children with autism look less frequently at the adult faces than control subjects in empathy-eliciting situations, the remaining findings are equivocal. For instance, one study did not find any change of heartbeat rate during the observation of someone in distress [ ]. Another study has shown that the autonomic responses of these children change according to the distress of the target, if the emotions displayed are not ambiguous and if they are presented under conditions with reduced distraction [ ].
It is likely that these children present a difficulty in taking the perspective of others, which requires executive resources, but they seem to have the physiological substrate to display affective sharing abilities. Altogether, both impairment in executive functions and emotion sharing may account for the empathy deficit in autism. There is also evidence of deficits in the perception-action coupling, corresponding to basic level of empathy, like mimicry. One study has shown that when compared with developmentally delayed children, month-old infants with autism were found to be specifically impaired on empathy task, joint attention and imitation [ ].
Imitation deficits have been proposed to explain the difficultly of autistic children in establishing social relationships and identifying with others [ ]. This suggests that these children cannot readily identify with the experimenter's perspective entirely. It has also been demonstrated that long before children with autism show theory of mind deficits, they exhibit deficits in joint attention and attention monitoring [ ].
A study examined 30 to 70 month-old autistic and healthy children's social behavior, affect, and use of gaze during naturalistic interactions with their mothers [ ]. Both autistic and typically developing children responded with smiles more frequently to social events than to nonsocial events. However, when autistic children's responses to the mother's smiles were examined, the authors found that they never smiled in response to the mother's smile. In other words, they do not exhibit the biologically based ability to automatically resonate with others which consists of very basic level of empathy, indicating their perception-action coupling deficits in a behavior that is considered as a manifestation of emotion contagion, like facial mimicry.
Another recent study found that individuals with autism do not show spontaneous mimicry, but they perform voluntary mimicry well [ 35 ]. Burgeoning research efforts suggest that a deficient mirror neuron system may contribute to motor and social problems experienced in individuals with ASD. Indeed, brain areas associated with the mirror-neuron system and imitation have all been observed as aberrant in terms of structure and function in individuals with ASD. Indeed, recent research with humans using transcranial magnetic stimulation TMS demonstrates changes in the amplitude of the motor-evoked potentials during action observation, a clear demonstration of the motor resonance mechanism e.
Compared to the controls, adults with ASD showed significantly less M1 activation during the observation of transitive, meaningless finger movements [ ]. In contrast, observation of the finger movements in control subjects yielded enhanced M1 activity in areas delivering signals to the muscles concerned with the observed action.
The weaker M1 modulation in individuals with ASD suggests that the less mirror neuron activation in the motor cortex may be partly responsible for the deficits in social cognition, specifically abnormal self-other representations, diminished reciprocal social capacities, and hindered development of empathy. In attempt to examine a potential link between mirror neuron dysfunction and developmental delay of social cognitive skills, one fMRI study found a lack of activation in the inferior frontal gyrus a key mirror neuron area in children with ASD as compared to controls during the observation and imitation of basic facial emotion expression [ ].
These recent findings, which need to be replicated, seem to suggest that dysfunction in the mirror neuron system may hamper the normal development of self-other connectedness, creating a cascade of deficient processes that lead to social deficits, including some aspects of empathy. It should be noted that, to date, it is not clear what aspect of empathy is dysfunctional in ASD, and there is not enough empirical research that has addressed this question. Individuals with autism appear to have deficiencies over broader aspects of empathy, although this notion needs to be clarified in the future.
Alexithymia refers to deficiencies in understanding, processing, or describing emotions in the self [ ]. Since awareness of emotional states in the self is a prerequisite to recognizing such states in others, alexithymia should involve impairment in empathy. Although alexithymia is not a diagnostic disorder, it is a personal trait that is prevalent in broad psychiatric and psychosomatic spectrums, which are characterized by deficits in empathy, such as autistic spectrum disorder [ — ], schizophrenia [ — ], borderline [ ], narcissistic [ ] and psychopathic personality disorders [ ].
Guttman et al. Moriguchi and colleagues [ ] showed that alexithymic people showed low theory of mind ability when they mentalize the moving triangle animation and, using fMRI, low neural activity in medial prefrontal cortex, which is mostly associated with perspective taking scale. Moriguchi and colleagues [ 63 ] further used fMRI to compare neural response in a group of people with alexithymia with a group of healthy controls to the visual perception of pictures depicting human hands and feet in painful situations.
The alexithymia group showed less cerebral activation in the left dorsolateral prefrontal cortex, the dorsal pons, the cerebellum, and the left caudal anterior cingulate cortex within the pain matrix. The alexithymia group showed rather greater activation in the areas related to affective processing such as the right anterior and posterior insula and inferior frontal gyrus.
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Furthermore, alexithymic participants scored lower on the pain ratings and on the scores related to cognitive mature empathy. Another fMRI study [ ] also showed that a population with alexithymia had lower neural activity in medial prefrontal cortex in response to affective pictures, but there is no difference of activation in the brain areas associated with bottom up information processing such as limbic structures i. In sum, alexithymia has certain deficits in empathy, particularly in the aspects of mental flexibility to adopt the subjective perspective of the other and executive and regulatory processes that modulate the subjective feelings associated with emotion.
These facts also support the importance of self-awareness in empathy, and these cognitive impairments underlie and constitute core psychopathology related to the social and interpersonal difficulties in various psychiatric disorders listed above. Taken together, the available empirical evidence from the various forms of empathy disorders in psychiatry population fits neatly with a multiple-component model.
It further reveals that there are important differences in the cognitive and neural systems involved in the cognitive and affective architecture of empathy and its social behavioral outcomes. Empathy is a fundamental ability for social interaction and moral reasoning. It refers to an emotional response that is produced by the emotional state of another individual without losing sight of whose feelings belong to whom.
This response is contingent on cognitive, as well as emotional, factors and involves parallel and distributed processing in a number of dissociable computational mechanisms. Like many complex experiences, empathy emerges from the flow and integration of information between specific brain circuits.
Current trends in empathy theory suggest that it involves partly dissociable components, including shared neural affective representations, self-awareness, mental flexibility, and emotion regulation. These basic macro-components of empathy are mediated by specific and interacting neural systems. These macro-components may comprise more elementary components that future social neuroscience studies in combination with clinical research will elucidate. Moreover, because this model assumes that empathy relies on dissociable information processing components, it predicts a variety of structural or functional dysfunctions depending on which aspect is disrupted.
Indeed, there are various forms of empathy dysfunctions in psychopathology such as antisocial personality disorders, psychopathy, narcissistic personality disorders and autism, which seem to reflect selective impairment of one or several components of the neurocognitive architecture of empathy. The lack of empathy leads to profound disturbance and dysfunction in social interaction, and hence is important to study in the domain of psychopathology. Future clinical investigations of empathy disorders can only be informative if behavioral, dispositional and biological factors are combined. Multiple levels of analysis are fundamental when addressing such a complex aspect of psychology.
Too often, the assessment of empathy in both healthy and psychiatric populations relies on self-report measures that alone are not valid. Further, empathy may be a prerequisite for altruism, but the relation between empathy and prosocial motivation is far from being simple and direct. Both biology and experience contribute to empathy and sympathy in complex interactive, bidirectional ways. Finally, one of the challenges for a social neuroscience approach to empathy and its disorders is the difficulty of taking into account situational variables. To provide interpretable data, neuroscience experiments require intra-individual comparisons and repeated-measures designs.
To be financially feasible, they require small samples. These conditions limit opportunities to study the effects of potentially important situational variables. This is but one example of the perennial challenge objective science faces in the attempt to understand human subjectivity in all its richness and complexity [ ].
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