Prefrontal substrates of empathy: psychometric evidence in a community sample

Empathy is a vicarious experience of others’ emotions, and is crucial to many forms of adaptive social interaction. Clinical, experimental, and functional neuroimaging studies convergently suggest a role for prefrontal-limbic circuits in mediating empathy. This study examined the prefrontal basis of empathy in a community sample using self-report measures: the frontal systems behavior scale (FrSBe), Barratt impulsiveness scale (BIS), and the interpersonal reactivity index (IRI). Multiple correlations emerged supporting an inverse relationship between prefrontal system dysfunction and empathy, particularly emotional empathy and perspective taking. Many of these relationships persisted after controlling for age, sex, and education. However, FrSBe scales did not correlate with one's identification with fictional characters, and motor impulsivity correlated positively, presumably due to the different cognitive and emotional context (i.e. real versus fictional individuals). These studies parallel others using objective methodologies and suggest a graded relationship between prefrontal function and empathy and likely reflect normal variations in prefrontal-limbic function.     

The role of sleep in aesthetic perception and empathy: A mediation analysis

The ability to experience aesthetics plays a fundamental role in human social interactions, as well as the capacity to feel empathy. Some studies have shown that beauty perception shares part of the neural network underlying emotional and empathic abilities, which are also known to affect sleep quality and duration. In this study, we evaluated for the first time the effects of sleep on the relation between aesthetic perception and empathic abilities in healthy subjects using a mediation analysis approach. One‐hundred and twenty‐six subjects participated in this study. One‐hundred and one subjects slept at home (Sleep Group). The remaining 25 subjects were tested as controls after 1 night of sleep deprivation to assess the effects of lack of sleep on aesthetic perception and empathy (Sleep‐Deprived Group). All participants underwent one testing session in which they performed a battery of empathy tests and an aesthetic perception task (Golden Beauty). The results showed that sleep duration mediates the relationship between empathy and aesthetic perception in the sleep group. The mediation effect of sleep was more evident on the emotional empathy measures. Conversely, in the sleep deprivation group the lack of correlations among empathy, aesthetic perception and sleep variables did not allow to perform the mediation analysis. These results suggest that adequate sleep duration may play a significant role in improving cognitive and emotional empathic abilities as well as the capability to give accurate aesthetic judgements.     

Can self-pain sensitivity quantify empathy for others' pain?

Empathy is essential for the survival of social species. In many studies, especially those with animal models, empathy for pain was evaluated by the modulation of pain sensitivity. However, the relationship between pain sensitivity and empathy for pain is not well established. Here, by performing two experiments, we aimed to investigate their relationship at both behavioral and electrophysiological levels. In Experiment 1, we characterized individual pain sensitivity using pain threshold and tolerance in a cold pressor test, self-report empathy using Interpersonal Reactivity Index, and pain-related psychological factors, including pain-related anxiety, depression, pain catastrophizing, and pain-related fear, using well-validated questionnaires. We observed that pain sensitivity was positively correlated with emotional empathy, and their relationship was mediated by pain-related anxiety, pain catastrophizing, and pain-related fear. In Experiment 2, we quantified empathy for pain using pain intensity and unpleasantness as well as event-related potentials (ERPs) in an empathy for pain task. Positive correlations were observed between pain sensitivity and psychophysiological empathic responses (i.e., the P3 component and the late positive potential in ERPs), and their relationship was mediated by pain-related fear. These results suggested that being influenced by some pain-related psychological factors, individuals with higher pain sensitivity tended to have stronger empathy for pain, manifested as stronger emotional reactions to others' pain. Our results indicated that the conventional strategy of using pain sensitivity to quantify empathy should be treated with caution, as their relationship could be disturbed by experimental manipulations or pathological modulations that could influence individual emotional states or cognitive processes.     

Functional modularity of the medial prefrontal cortex: involvement in human empathy

To investigate medial frontal lobe mediation of human empathy, the authors analyzed the activation areas in statistical parametric maps of 80 studies reporting neural correlates of empathic processing. The meta-analysis revealed 6 spatially distinct activation clusters in the medial part of the frontal lobe dorsal to the intercommissural plane. The most dorsal cluster coincided with the left supplementary motor area (SMA). Rostrally adjacent was a cluster that overlapped with the right pre-SMA. In addition, there were 3 left-hemispheric and 1 right-hemispheric clusters located at the border between the superior frontal and anterior cingulate gyrus. A broad spectrum of cognitive functions were associated with these clusters, including attention to one's own action, which was related to activations in the SMA, and valuation of other people's behavior and ethical categories, which was related to activations in the most rostroventral cluster. These data complement the consistent observation that lesions of the medial prefrontal cortex interfere with a patient's perception of own bodily state, emotional judgments, and spontaneous behavior. The results of the current meta-analysis suggest the medial prefrontal cortex mediates human empathy by virtue of a number of distinctive processing nodes. In this way, the authors' findings suggest differentiated aspects of self-control of behavior.     

Early glycinergic axon contact with the Mauthner neuron during zebrafish development

One important aspect of empathy is a “resonance mechanism”, which includes emotional cue detection, facial mimicry (measured by electromyography, EMG) and a specific cortical response. This study explored the convergence of these three measures of affective empathy. The twenty students who took part in the study were required to empathise with the situation by entering into the other person's situation. The four emotions portrayed were anger, fear, happiness, and neutral, and the subjects were instructed to make a two-alternative response (emotion or no emotion) to each emotion. A repeated transcranial magnetic stimulation was used to produce a temporary inhibition of the medial prefrontal cortex (MPFC). The results support the hypothesis that there is a direct relationship between emotional cue recognition, EMG-measured facial response and prefrontal activity. First, both facial expression detection and autonomic mimicry in reaction to emotional faces were systematically modulated in response to inhibition of the MPFC. Second, the MPFC was implicated in facial cue detection and the subsequent autonomic response because an impaired performance on both measures was observed when this brain area was inhibited. Third, this effect increased when negative-valenced stimuli (angry and fearful faces) were presented to the subjects. These results revealed a significant effect of the MPFC on both cue detection and facial mimicry that was distinctly related to different types of emotions.     

The differences in neural network activity between methamphetamine abusers and healthy subjects performing an emotion-matching task: functional MRI study

Methamphetamine (MA) abusers commonly exhibit socially problematic behaviors, such as diminished empathy, decreased emotional regulation and interpersonal violence, which may be attributable to alterations in emotional experience. However, few studies have used functional MRI to examine directly the emotional experience of threatening or fearful non-face images in MA abusers. In this study, we investigated possible differences in neural correlates of negative emotional experiences between abstinent MA abusers and healthy subjects using complex visual scenes depicting fear or threat derived from the International Affective Picture System. In within-group analyses, healthy subjects and MA abusers activated a similarly distributed cortical network, prominently including the amygdala, fusiform gyrus, parahippocampal gyrus, ventrolateral prefrontal cortex and inferior frontal cortex. In between-group analyses, however, MA abusers showed a reduced activation in the bilateral dorsolateral prefrontal cortex and insula, and increased activation in the fusiform gyrus, hippocampus, parahippocampal gyrus and posterior cingulate cortex, relative to healthy subjects. Hypoactivation of the insula in MA abusers relative to healthy subjects suggests that the ability to have an emotional response to threatening scenes and empathy for another's pain could be compromised in MA abusers. Hyperactivity in the fusiform gyrus, parahippocampal gyrus and posterior cingulate cortex in MA abusers relative to healthy subjects indicates that threatening and fearful images from the International Affective Picture System may remind MA abusers of episodic memory related to similar experiences. Therefore, functional impairment of these neural networks in MA abusers may contribute to altered emotional experience in social interactions, which could lead to increased negative mood and stress in interpersonal communication.     

Fear-related activity in the prefrontal cortex increases with age during adolescence: a preliminary fMRI study

An emerging theory of adolescent development suggests that brain maturation involves a progressive "frontalization" of function whereby the prefrontal cortex gradually assumes primary responsibility for many of the cognitive processes initially performed by more primitive subcortical and limbic structures. To test the hypothesis of developmental frontalization in emotional processing, we analyzed the correlation between age and prefrontal cortex activity in a sample of 16 healthy adolescents (nine boys; seven girls), ranging in age from 8 to 15 years, as they viewed images of fearful and happy faces while undergoing functional magnetic resonance imaging (fMRI). During fear perception, age was significantly positively correlated with greater functional activity within the prefrontal cortex, whereas no significant relationship was evident between age and activity in the amygdala. Consistent with previous gender-related findings, age was significantly correlated with bilateral prefrontal activity for the sample of females, but was only significantly related to right prefrontal activity for the males. In contrast, similar age-related correlations were not evident during the perception of happy faces. These results suggest that the maturation of threat-related emotional processing during adolescence is related to the progressive acquisition of greater functional activity within the prefrontal cortex. The hypothesis of age related decreases in amygdala activity was not supported, but may have been due to low signal-to-noise and inadequate power in the present sample to resolve subtle changes in this small structure.     

Emotional deficits in psychopathy and sexual sadism: implications for violent and sadistic behavior

While both psychopaths and sexual sadists engage in acts of predatory violence, little empirical work has examined the relationship between the two disorders. This paper outlines the constructs of psychopathy and sexual sadism and reviews the literature investigating the emotional lives of individuals with these disorders, paying particular attention to how emotional deficits might facilitate instrumental violence. Specifically, it is hypothesized that the emotion recognition and emotional experience deficits found among psychopaths, and perhaps present in sexual sadists, may lead to deficits in their ability to empathize with others, resulting in an increased likelihood for perpetrating instrumental violence. The relationship between empathy and aggression in psychopaths and sexual sadists is discussed, and distinctions are drawn between the two disorders with respect to their capacities to experience cognitive and affective empathy on a global level. Gaps in the literature are identified and additional areas of inquiry are suggested.     

The effects of sleep deprivation on emotional empathy

Previous studies have shown that sleep loss has a detrimental effect on the ability of the individuals to process emotional information. In this study, we tested the hypothesis that this negative effect extends to the ability of experiencing emotions while observing other individuals, i.e. emotional empathy. To test this hypothesis, we assessed emotional empathy in 37 healthy volunteers who were assigned randomly to one of three experimental groups: one group was tested before and after a night of total sleep deprivation (sleep deprivation group), a second group was tested before and after a usual night of sleep spent at home (sleep group) and the third group was tested twice during the same day (day group). Emotional empathy was assessed by using two parallel versions of a computerized test measuring direct (i.e. explicit evaluation of empathic concern) and indirect (i.e. the observer's reported physiological arousal) emotional empathy. The results revealed that the post measurements of both direct and indirect emotional empathy of participants in the sleep deprivation group were significantly lower than those of the sleep and day groups; post measurement scores of participants in the day and sleep groups did not differ significantly for either direct or indirect emotional empathy. These data are consistent with previous studies showing the negative effect of sleep deprivation on the processing of emotional information, and extend these effects to emotional empathy. The findings reported in our study are relevant to healthy individuals with poor sleep habits, as well as clinical populations suffering from sleep disturbances.     

多维共情测试中文版测评社区成年人的效度和信度

目的:引入多维共情测试(MET)并检验其效度和信度。方法:在北京市某社区招募201名被试(年龄18～89岁),使用多维共情测试(MET)中文版进行评估和施测。对所有样本进行验证性因子分析以检验结构效度;人际反应指数量表(IRI)测评用以检验效标关联效度;使用Cronbach α系数和最大下限临界值(glb)进行信度分析;间隔2周后对其中22人进行重测。结果:MET中文版包括认知共情、积极情绪共情和消极情绪共情3个维度,3因子结构模型拟合良好(χ~2/df=1.26,RMSEA=0.04,CFI=0.92,TLI=0.92,SRMR=0.10);3个维度得分均与IRI总分正相关(r=0.24、0.23、0.30,P<0.01或P<0.001),积极情绪共情和消极情绪共情得分与IRI的共情关注得分正相关(r=0.24、0.18,P<0.01或P<0.05)。总量表的Cronbach α系数为0.94,3个维度的α系数分别为0.36、0.93、0.95;总量表的glb为0.91,3个维度的glb分别为0.63、0.96、0.96;总量表的重测相关系数(ICC)为0.8...     

Negative socio-emotional resonance in schizophrenia: a functional magnetic resonance imaging hypothesis

The aim of the present study is to use neuroscience theories about brain function (mirror-neurons MN) to draw inferences about the mechanisms supporting emotional resonance in two different groups of schizophrenia patients (with flat affect FA+ n = 13 and without flat affect FA- n = 11). We hypothesize that FA+ will not activate key brain areas involved in emotional processing. Conversely, FA- will have a functional mirror system for emotional resonance confirmed by activation of the prefrontal cortex and behavioral results. To test this hypothesis, we compared the two groups using blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) displaying a passive visual task (44 negative IAPS pictures and 44 neutral pictures). A random-effects analysis, for schizophrenia patients FA-, revealed significant loci of activation in the left mesial prefrontal (MPFC), right orbitofrontal (OFC) and left anterior cingulate cortices (ACC). Correlational analyses carried out between self-report ratings of negative feelings and BOLD signal changes revealed the existence of positive correlation in the LACC, LMPFC and ROFC. Conversely, FA+ did not show significant activation in the prefrontal cortex. We propose that negative emotional resonance induced by passively viewing negative pictures may be a form of "mirroring" that grounds negative feelings via an experiential mechanism. Hence, it could be argued that FA- were able to 'feel' emotions through this resonance behavior. Conversely, we suggest that the dysfunction seen in the FA+ group is a failure or distortion in the development of the MN system. This could be due to genetic or other endogenous causes, which affected prefrontal cortex MN involved in emotional resonance.     

Moral decision-making, ToM, empathy and the default mode network

Automatic intuitions and deliberate reasoning, sourcing internal representations of our personal norms and values, contribute to our beliefs of what is right and wrong. We used fMRI to directly compare moral (M) and non-moral (NM) decision-making processes using scenarios requiring conscious deliberation, whereby the main character declared an intention to take a course of action. Furthermore, we examined the relationship between BOLD signal, associated with M>NM decision-making, and moral judgment competence, psychopathy, and empathy. We observed greater activity in various parts of Theory of Mind, empathy and default mode networks during M>NM decision-making. There was a trend for high scores on primary psychopathy to correlate with decreased M>NM BOLD activation in an area extending from dorsolateral prefrontal cortex to medial prefrontal cortex. We suggest that moral decision-making entails a greater degree of internally directed processing, such as self-referential mental processing and the representation of intentions and feelings, than non-moral decision-making.     

Neurocognitive basis of impaired empathy in schizophrenia

Patients with schizophrenia show impaired emotional and social behavior, such as lack of theory of mind and misinterpretation of social situations. However, there is a paucity of work focusing on the empathic abilities of these patients. The present study was designed to examine the degree of impairment in cognitive and affective empathy in schizophrenia and to evaluate the contribution of executive prefrontal functions to empathy in these patients. To explore the neurocognitive processes that underlie the empathic ability in schizophrenic patients, the relationship between empathy scores and the performance on a cognitive flexibility task that assesses dorsolateral and orbitofrontal functioning (set shifting and reversal, respectively) was examined in 26 patients with schizophrenia and 31 healthy control subjects. Results indicated that patients with schizophrenia were significantly impaired in both cognitive and affective empathy compared with healthy control subjects. The degree of impaired empathy related to the severity of negative symptoms. In addition, patients showed impaired performance on measures of both shifting and reversal. However, while cognitive empathy was particularly related to measurements of orbitofrontal (rather than dorsolateral) functioning, affective empathy was related to measures of social functioning.     

Aging is associated with changes in the neural circuits underlying empathy

Although the neurodevelopment of empathy from childhood to adolescence has been documented, no study has yet examined it across a life span aging perspective. Sixty-five healthy participants from 3 age groups (young, middle-aged, old) underwent functional magnetic resonance imaging while presented with visual stimuli depicting body parts being injured, either accidentally by oneself or intentionally by another, thus isolating pain and agency as 2 variables of interest. Older adults reported less dispositional emotional empathy as assessed by the interpersonal reactivity index, and their unpleasantness ratings were more sensitive to intentional harm. The response in anterior insula and anterior mid-cingulate cortex to others' pain, indicative of emotional empathy, showed an age-related decline, whereas the response in medial prefrontal cortex and posterior superior temporal sulcus to perceived agency did not change with age. Dynamic causal modeling demonstrated that their effective connectivity remained stable. The pattern of hemodynamic response was not related to regional gray matter volume loss. These findings suggest that the neural response associated with emotional empathy lessened with age, whereas the response to perceived agency is preserved.     

情绪特异性共情问卷在中国大学生中的信效度检验

目的:初步检验情绪特异性共情问卷(Emotion Specific Empathy Questionnaire,ESEQ)在中国大学生中的信效度。方法:采用方便取样法在369名大学生中,测量中文版ESEQ、人际反应指针量表(IRI)和人际综合诊断量表(IRAS),间隔4周后重测ESEQ。结果:多质多法的验证性因子分析显示,中文版ESEQ与原英文版ESEQ的拟合结果一致,即ESEQ可评估认知共情和情绪共情两种特质,每种特质包含生气、厌恶、恐惧、高兴、悲伤和惊奇六种情绪,总量表拟合指数为:CFA=0.99,TLI=0.98,χ²/df=2.28,RMSEA=0.059,SRMR=0.066;总量表Cronbach’sα系数0.95,分量表Cronbach’sα系数0.65~0.84;总量表重测信度0.79,分量表重测信度0.47~0.73。ESEQ的效标效度检验显示,认知共情得分与观点采择显著正相关(r=0.50),情绪共情得分与共情关注显著正相关(r=0.45);六种情绪的认知共情得分与各人际困扰显著负相关(r=-0.32~-0.11),情绪共情中仅有高兴情绪得分与各人际困扰显著负相关(r=-0.33~-0.16)。结论:中文版情绪特异性共情问卷(ESEQ)的信效度良好,可用于大学生的共情测量。     

The prefrontal-limbic network in depression: Modulation by hypothalamus, basal ganglia and midbrain

The anterior cingulate cortex, amygdala and hippocampus form part of an interconnected prefrontal neocortical and limbic archicortical network that is dysregulated in major depressive disorders (MDD). Modulation of this prefrontal-limbic network (PLN) is principally through the hypothalamus, basal ganglia and midbrain. Here the likely mechanisms by which these modulations are affected are described and the implications of their failure for depression associated with suicidal diathesis, late-life and psychoses discussed.     

Empathy and error processing

Recent research suggests a relationship between empathy and error processing. Error processing is an evaluative control function that can be measured using post‐error response time slowing and the error‐related negativity (ERN) and post‐error positivity (Pe) components of the event‐related potential (ERP). Thirty healthy participants completed two measures of empathy, the Interpersonal Reactivity Index (IRI) and the Empathy Quotient (EQ), and a modified Stroop task. Post‐error slowing was associated with increased empathic personal distress on the IRI. ERN amplitude was related to overall empathy score on the EQ and the fantasy subscale of the IRI. The Pe and measures of empathy were not related. Results remained consistent when negative affect was controlled via partial correlation, with an additional relationship between ERN amplitude and empathic concern on the IRI. Findings support a connection between empathy and error processing mechanisms.     

Sex differences in empathy for pain: What is the role of autonomic regulation?

Empathy involves both affective and cognitive components whereby we understand, and express concerns for, the experiences of others. Women typically have superior trait empathy compared with men, which seems to have a neurological basis with sex differences in the structure and function of neural networks involved in empathy. This study investigated sex differences in empathy for pain using the Empathy for Pain Scale, and examined whether these trait differences were associated with disruptions in autonomic regulation, specifically via the parasympathetic nervous system (measured through the square root of the mean squared differences of successive R‐R intervals; RMSSD) both at rest and during a socioevaluative stress task (i.e., the serial sevens task). Compared with men, women reported higher empathic concern (Cohen's r = .25) and affective distress (Cohen's d = 0.65) toward another in pain. In both men and women, there was a decrease in lnRMSSD in the stress task compared to rest. Sex moderated the relationship between resting lnRMSSD and self‐reported empathic concern. Specifically, there was no clear association between empathic concern and lnRMSSD in men whereas in women there was a negative relationship, with lower resting lnRMSSD associated with higher empathic concern, and higher lnRMSSD associated with lower levels of empathic concern that were similar to men. These findings suggest that empathic feelings may result from poorer psychophysiological regulation, and concur with previous research displaying sex‐specific relationships between resting heart rate variability and emotion regulation abilities.     

Social cognition, brain networks and schizophrenia

BACKGROUND: A better understanding of the neural basis of social cognition including mindreading (or theory of mind) and empathy might help to explain some deficits in social functioning in people with schizophrenia. Our aim was to review neuroimaging and neuropsychological studies on social cognition, as they may shed light on the neural mechanisms of social cognition and its dysfunction in patients with schizophrenia. METHOD: A selective literature review was undertaken. RESULTS: Neuroimaging and neuropsychological studies suggest convergence upon specific networks for mindreading and empathy (the temporal cortex, amygdala and the prefrontal cortex). The frontal lobe is likely to play a central role in enabling social cognition, but mindreading and empathic abilities may require relatively different weighting of subcomponents within the same frontal-temporal social cognition network. CONCLUSIONS: Disturbances in social cognition may represent an abnormal interaction between frontal lobe and its functionally connected cortical and subcortical areas. Future studies should seek to explore the heterogeneity of social dysfunction within schizophrenia.     

Impaired prefrontal–amygdala effective connectivity is responsible for the dysfunction of emotion process in major depressive disorder: A dynamic causal modeling study on MEG

Depression is proved to be associated with the dysfunction of prefrontal-limbic neural circuit, especially during emotion processing procedure. Related explorations have been undertaken from the aspects of abnormal activation and functional connectivity. However, the mechanism of the dysfunction of coordinated interactions remains unknown and is still a matter of debate. The present study gave direct evidence of this issue from the aspect of effective connectivity via dynamic causal modeling (DCM). 20 major depressive disorder (MDD) patients and 20 healthy controls were recruited to attend facial emotional stimulus during MEG recording. Bayesian model selection (BMS) was applied to choose the best model. Results under the optimal model showed that top-down endogenous effective connectivity from the dorsolateral prefrontal cortex (DLPFC) to the amygdala was greatly impaired in patients relative to health controls; while bottom-up endogenous effective connectivity from the amygdala to the anterior cingulate cortex (ACC) as well as modulatory effective connectivity from ACC to DLPFC was significantly increased. We inferred the incapable DLPFC failed to exert influence on amygdala, and finally lead to enhanced amygdala-ACC and ACC–DLPFC bottom-up effects. Such impaired prefrontal–amygdala connectivity was supposed to be responsible for the dysfunction in MDD when dealing with emotional stimuli.