The study of the neural basis of emotional empathy has received a surge of interest in recent years but mostly employing human neuroimaging. A simpler animal model would pave the way for systematic single cell recordings and invasive manipulations of the brain regions implicated in empathy. Recent evidence has been put forward for the existence of empathy in rodents. In this study, we describe a potential model of empathy in female rats, in which we studied interactions between two rats: a witness observes a demonstrator experiencing a series of footshocks. By comparing the reaction of witnesses with or without previous footshock experience, we examine the role of prior experience as a modulator of empathy. We show that witnesses having previously experienced footshocks, but not naïve ones, display vicarious freezing behavior upon witnessing a cage-mate experiencing footshocks. Strikingly, the demonstrator's behavior was in turn modulated by the behavior of the witness: demonstrators froze more following footshocks if their witness froze more. Previous experiments have shown that rats emit ultrasonic vocalizations (USVs) when receiving footshocks. Thus, the role of USV in triggering vicarious freezing in our paradigm is examined. We found that experienced witness-demonstrator pairs emitted more USVs than naïve witness-demonstrator pairs, but the number of USVs was correlated with freezing in demonstrators, not in witnesses. Furthermore, playing back the USVs, recorded from witness-demonstrator pairs during the empathy test, did not induce vicarious freezing behavior in experienced witnesses. Thus, our findings confirm that vicarious freezing can be triggered in rats, and moreover it can be modulated by prior experience. Additionally, our result suggests that vicarious freezing is not triggered by USVs per se and it influences back onto the behavior of the demonstrator that had elicited the vicarious freezing in witnesses, introducing a paradigm to study empathy as a social loop.
The ways in which aging affects social economic decision-making is a central issue in the psychology of aging. To examine age-related differences in social economic decision-making as a function of empathy, 80 healthy volunteers participated in the Repeated Fixed Opponent Ultimatum Game (UG-R). Previous economic decision making research has shown that in younger adults empathy is associated with prosocial behavior. The effects of empathy on older adult social economic decision-making are not well understood.
On each of 20 consecutive trials in the UG-R, one player (“Proposer”) splits ten dollars with another player (“Responder”) who chooses either to accept (whereby both receive the proposed division) or reject (whereby neither receives anything). Trait cognitive and emotional empathy were measured using the Interpersonal Reactivity Index.
UG-R data were examined as a function of age and cognitive empathy. For unfair offers (i.e., offers less than $5), older Responders with high cognitive empathy showed less prosocial behavior and obtained greater payoffs than younger Responders with high cognitive empathy.
High levels of cognitive empathy may differentially affect economic decision making behavior in younger and older adults. For older adults, high cognitive empathy may be involved in obtaining high financial payoffs while for younger adults it may instead facilitate social relationships.
Aging; Economic Decision-Making; Social Cognition; Empathy
This study examined the correlates and predictors of prosocial behavior among Chinese adolescents in Hong Kong. A sample of 518 high school students responded to a questionnaire containing measures of antisocial and prosocial behavior, prosocial norms, pragmatic values, moral reasoning, and empathy. Preliminary analyses showed that there were gender differences in some of the measures. While correlation analyses showed that parental education, prosocial norms, pragmatic values, moral reasoning, and empathy were related to prosocial behavior, regression analyses showed that prosocial norms, pragmatic values, and empathy dimensions (personal distress and empathy) were key predictors of it. The findings are largely consistent with theoretical predictions and previous research findings, other than the negative relationship between personal distress and prosocial behavior. The study also underscores the importance of values and norms in predicting prosocial behavior, which has been largely neglected in previous studies.
Empathy, which implies a shared interpersonal experience, is implicated in many aspects of social cognition, notably prosocial behavior, morality and the regulation of aggression. The purpose of this paper is to critically examine the current knowledge in developmental and affective neuroscience with an emphasis on the perception of pain in others. It will be argued that human empathy involves several components: affective arousal, emotion understanding and emotion regulation, each with different developmental trajectories. These components are implemented by a complex network of distributed, often recursively connected, interacting neural regions including the superior temporal sulcus, insula, medial and orbitofrontal cortices, amygdala and anterior cingulate cortex, as well as autonomic and neuroendocrine processes implicated in social behaviors and emotional states. Decomposing the construct of empathy into subcomponents that operate in conjunction in the healthy brain and examining their developmental trajectory provides added value to our current approaches to understanding human development. It can also benefit our understanding of both typical and atypical development.
Affective neuroscience; Amygdala; Empathy; Theory of mind; Neurodevelopment; Orbitofrontal cortex; Ventromedial prefrontal cortex
People are able to rapidly infer complex personality traits and mental states even from the most minimal person information. Research has shown that when observers view a natural scene containing people, they spend a disproportionate amount of their time looking at the social features (e.g., faces, bodies). Does this preference for social features merely reflect the biological salience of these features or are observers spontaneously attempting to make sense of complex social dynamics? Using functional neuroimaging, we investigated neural responses to social and nonsocial visual scenes in a large sample of participants (n = 48) who varied on an individual difference measure assessing empathy and mentalizing (i.e., empathizing). Compared with other scene categories, viewing natural social scenes activated regions associated with social cognition (e.g., dorsomedial prefrontal cortex and temporal poles). Moreover, activity in these regions during social scene viewing was strongly correlated with individual differences in empathizing. These findings offer neural evidence that observers spontaneously engage in social cognition when viewing complex social material but that the degree to which people do so is mediated by individual differences in trait empathizing.
empathy; fMRI; individual differences; mentalizing; theory of mind
Studies on memory, imagination, and empathy have largely progressed in isolation. Consequently, humans’ empathic tendencies to care about and help other people are considered independent of our ability to remember and imagine events. Despite this theoretical autonomy, work from across psychology, and neuroscience suggests that these cognitive abilities may be linked. In the present paper, I tentatively propose that humans’ ability to vividly imagine specific events (as supported by constructive memory) may facilitate prosocial intentions and behavior. Evidence of a relationship between memory, imagination, and empathy comes from research that shows imagination influences the perceived and actual likelihood an event occurs, improves intergroup relations, and shares a neural basis with memory and empathy. Although many questions remain, this paper outlines a new direction for research that investigates the role of imagination in promoting empathy and prosocial behavior.
episodic memory; episodic simulation; mental simulation; imagination; functional magnetic resonance imaging; empathy; prosocial behavior
In this study, we tested the validity of 2 popular assumptions about empathy: (a) empathy can be enhanced by oxytocin, a neuropeptide known to be crucial in affiliative behavior, and (b) individual differences in prosocial behavior are positively associated with empathic brain responses. To do so, we measured brain activity in a double-blind placebo-controlled study of 20 male participants either receiving painful stimulation to their own hand (self condition) or observing their female partner receiving painful stimulation to her hand (other condition). Prosocial behavior was measured using a monetary economic interaction game with which participants classified as prosocial (N = 12) or selfish (N = 6), depending on whether they cooperated with another player. Empathy-relevant brain activation (anterior insula) was neither enhanced by oxytocin nor positively associated with prosocial behavior. However, oxytocin reduced amygdala activation when participants received painful stimulation themselves (in the nonsocial condition). Surprisingly, this effect was driven by “selfish” participants. The results suggest that selfish individuals may not be as rational and unemotional as usually suggested, their actions being determined by their feeling anxious rather than by reason.
empathy; pain; prosocial behavior; oxytocin; amygdala
First- and third-person experiences of bodily sensations, like pain and touch, recruit overlapping neural networks including sensorimotor, insular, and anterior cingulate cortices. Here we illustrate the peculiar role of these structures in coding the sensory and affective qualities of the observed bodily sensations. Subsequently we show that such neural activity is critically influenced by a range of social, emotional, cognitive factors, and importantly by inter-individual differences in the separate components of empathic traits. Finally we suggest some fundamental issues that social neuroscience has to address for providing a comprehensive knowledge of the behavioral, functional and anatomical brain correlates of empathy.
empathy; personality; social cognition; somatosensory cortex; insula; ACC
Separate lines of research have noted recruitment of parietal cortex during tasks involving visuo-spatial processes and empathy. To explore the relationship between these two functions, a self-other perspective transformation task and a task of spatial attention (line bisection) were administered to 40 healthy participants (19 women). Performance on these tasks was examined in relation to self-reported empathy. Rightward biases in line bisection correlated positively with trait-level self-reported empathic concern, suggesting a left hemisphere mediation of this prosocial personality trait. Unexpectedly, speed of perspective taking in the self-other transformation task correlated negatively with empathic concern, but only in women, which we interpret in light of gender differences in empathy and strategies for egocentric mental transformations. Together, the findings partially support the commonalities in visuo-spatial attention, perspective-taking and empathy. More broadly, they shed additional light on the relationship between basic cognitive functions and complex social constructs.
Affective empathy (AE) is distinguished clinically and neurally from cognitive empathy (CE). While AE is selectively disrupted in psychopathy, autism is associated with deficits in CE. Despite such dissociations, AE and CE together contribute to normal human empathic experience. A dimensional measure of individual differences in AE ‘relative to’ CE captures this interaction and may reveal brain–behavior relationships beyond those detectable with AE and CE separately. Using resting-state fMRI and measures of empathy in healthy adults, we show that relative empathic ability (REA) is reflected in the brain's intrinsic functional dynamics. Dominance of AE was associated with stronger functional connectivity among social–emotional regions (ventral anterior insula, orbitofrontal cortex, amygdala, perigenual anterior cingulate). Dominance of CE was related to stronger connectivity among areas implicated in interoception, autonomic monitoring and social–cognitive processing (brainstem, superior temporal sulcus, ventral anterior insula). These patterns were distinct from those observed with AE and CE separately. Finally, REA and the strength of several functional connections were associated with symptoms of psychopathology. These findings suggest that REA provides a dimensional index of empathic function and pathological tendencies in healthy adults, which are reflected in the intrinsic functional dynamics of neural systems associated with social and emotional cognition.
affective empathy; cognitive empathy; fMRI; resting-state functional connectivity; social cognition
Empathy facilitates prosocial behavior and social understanding. Here, however, we suggest that the most basic mechanism of empathy—the intuitive sharing of other’s emotional and motivational states—is limited to those we like. Measuring electroencephalographic (EEG) alpha oscillations as people observed ingroup vs outgroup members, we found that participants showed similar activation patterns when feeling sad as when they observed ingroup members feeling sad. In contrast, participants did not show these same activation patterns when observing outgroup members and even less so the more they were prejudiced. These findings provide evidence from brain activity for an ingroup bias in empathy: empathy may be restricted to close others and, without active effort, may not extend to outgroups, potentially making them likely targets for prejudice and discrimination.
empathy; prejudice; EEG; frontal asymmetries
Empathy is the combined ability to interpret the emotional states of others and experience resultant, related emotions. The relation between prefrontal electroencephalographic asymmetry and emotion in infants and children is well known. The relationship between positive emotion (assessed via parent-report), empathy (measured via observation) and second-by-second brain electrical activity (recorded during a pleasurable task) was investigated using a sample of 128 six to ten year olds. Contentment predicted increasing left-sided frontopolar activation (p<.05). Empathic concern and one form of positive empathy predicted increasing right-sided frontopolar activation (ps<.05). A second form of positive empathy predicted increasing left-sided dorsolateral activation (p<.05). This suggests that positive emotion and (negative and positive) empathy predict changes in prefrontal activity in children during a pleasurable task.
Empathy is a longstanding issue in economics, especially for welfare economics, but one which has faded from the scene in recent years. However, with the rise of neuroeconomics, there is now a renewed interest in this subject. Some economists have even gone so far as to suggest that neuroscientific experiments reveal heterogeneous empathy levels across individuals. If this were the case, this would be in line with economists' usual assumption of stable and given preferences and would greatly facilitate the study of prosocial behaviour with which empathy is often associated. After reviewing some neuroscientific psychological and neuroeconomic evidence on empathy, we will, however, criticize the notion of a given empathy distribution in the population by referring to recent experiments on a public goods game that suggest that, on the contrary, the degree of empathy that individuals exhibit is very much dependent on context and social interaction.
empathy; rationality; other-regarding preferences; identity; public goods game; social interaction
Empathy is an important psychological capacity that involves the ability to recognize and share emotions with others. In humans, empathy for others is facilitated by having had a similar prior experience. It increases with the intensity of distress that observers believe is occurring to others, and is associated with acute emotional responses to witnessing others’ distress. We sought to develop a relatively simple and fast mouse model of human empathy that resembled these characteristics. We modeled empathy by measuring the freezing of observer mice to observing the footshock of a subject mouse. Observer mice froze to subject footshocks only when they had a similar shock experience 24 hours earlier. Moreover, this freezing increased with the number of footshocks given to the subject and it was accentuated within seconds after footshock delivery. Freezing was not seen in naïve observers or in experienced observers that observed a subject who was spared footshock. Observers did not freeze to a subject’s footshock when they had experienced a swim stress 24 hours prior, demonstrating a specific effect for shared experience, as opposed to a generalized stressor in eliciting observer mouse freezing. We propose that this two-day experimental protocol resembles many aspects of human empathy in a mouse model that is amenable to transgenic analysis of neural substrates for empathy and its impairment in certain clinical disorders.
Empathy is a multi-faceted concept consisting of our ability not only to share emotions but also to exert cognitive control and perspective taking in our interactions with others. Here we examined whether inter-individual variability in different components of empathy was related to differences in brain structure assessed using voxel-based morphometry. Following a magnetic resonance imaging (MRI) scan, participants completed the Interpersonal Reactivity Index (IRI). Multiple regression was then used to assess the relationship between individual differences in grey matter volume and individual differences in empathy traits. We found that individual differences in affective empathic abilities oriented towards another person were negatively correlated with grey matter volume in the precuneus, inferior frontal gyrus, and anterior cingulate. Differences in self-oriented affective empathy were negatively correlated with grey matter volume of the somatosensory cortex, but positively correlated with volume in the insula; cognitive perspective taking abilities were positively correlated with grey matter volume of the anterior cingulate; and the ability to empathise with fictional characters was positively related to grey matter changes in the right dorsolateral prefrontal cortex. These findings are discussed in relation to neurocognitive models of empathy.
► We studied how individual variability in empathy is linked to brain structure. ► Affective empathy was linked to changes in the precuneus and anterior cingulate. ► Changes in the inferior frontal gyrus were also linked with affective empathy. ► Perspective taking was related to changes in the anterior cingulate. ► Personal distress was linked to changes in the somatosensory cortex and insula.
Empathy; Voxel based morphometry; Interpersonal reactivity index; Structure; Individual differences; Social neuroscience
Emotional empathy and prosocial behavior were assessed in older, middle-aged, and young adults. Participants watched two films depicting individuals in need, one uplifting and the other distressing. Physiological responses were monitored during the films and participants rated their levels of emotional empathy following each film. As a measure of prosocial behavior, participants were given an additional payment they could contribute to charities supporting the individuals in the films. Age-related linear increases were found for both emotional empathy (self-reported empathic concern and cardiac and electrodermal responding) and prosocial behavior (size of contribution) across both films and in self-reported personal distress to the distressing film. Empathic concern and cardiac reactivity to both films, along with personal distress to the distressing film only, were associated with greater prosocial behavior. Empathic concern partially mediated the age-related differences in prosocial behavior. Results are discussed in terms of our understanding both of adult development and of the nature of these vital aspects of human emotion.
emotional empathy; prosocial behavior; emotion; physiological responses; aging
The neural processes underlying empathy are a subject of intense interest within the social neurosciences1-3. However, very little is known about how brain empathic responses are modulated by the affective link between individuals. We show here that empathic responses are modulated by learned preferences, a result consistent with economic models of social preferences4-7. We engaged male and female volunteers in an economic game, in which two confederates played fairly or unfairly, and then measured brain activity with functional magnetic resonance imaging while these same volunteers observed the confederates receiving pain. Both sexes exhibited empathy-related activation in pain-related brain areas (fronto-insular and anterior cingulate cortices) towards fair players. However, these empathy-related responses were significantly reduced in males when observing an unfair person receiving pain. This effect was accompanied by increased activation in reward-related areas, correlated with an expressed desire for revenge. We conclude that in men (at least) empathic responses are shaped by valuation of other people's social behaviour, such that they empathize with fair opponents while favouring the physical punishment of unfair opponents, a finding that echoes recent evidence for altruistic punishment.
Age changes’ measures of prosocial responding and reasoning were examined. Participants’ reports of helping, empathy-related responding, and prosocial moral reasoning were obtained in adolescence (from age 15–16 years) and into adulthood (to age 25–26 years). Perspective taking and approval/interpersonal oriented/stereotypic prosocial moral reasoning increased from adolescence into adulthood, whereas personal distress declined. Helping declined and then increased (a cubic trend). Prosocial moral judgment composite scores (and self-reflective empathic reasoning) generally increased from late adolescence into the early 20s (age 17–18 to 21–22) but either leveled off or declined slightly thereafter (i.e., showed linear and cubic trends); rudimentary needs-oriented reasoning showed the reverse pattern of change. The increase in self-reflective empathic moral reasoning was for females only. Thus, perspective taking and some aspects of prosocial moral reasoning—capacities with a strong sociocognitive basis—showed the clearest increases with age, whereas simple prosocial proclivities (i.e., helping, sympathy) did not increase with age.
Developmental research has demonstrated the harmful effects of peer rejection during adolescence; however, the neural mechanisms responsible for this salience remain unexplored. In this study, 23 adolescents were excluded during a ball-tossing game in which they believed they were playing with two other adolescents during an fMRI scan; in reality, participants played with a preset computer program. Afterwards, participants reported their exclusion-related distress and rejection sensitivity, and parents reported participants’ interpersonal competence. Similar to findings in adults, during social exclusion adolescents displayed insular activity that was positively related to self-reported distress, and right ventrolateral prefrontal activity that was negatively related to self-reported distress. Findings unique to adolescents indicated that activity in the subgenual anterior cingulate cortex (subACC) related to greater distress, and that activity in the ventral striatum related to less distress and appeared to play a role in regulating activity in the subACC and other regions involved in emotional distress. Finally, adolescents with higher rejection sensitivity and interpersonal competence scores displayed greater neural evidence of emotional distress, and adolescents with higher interpersonal competence scores also displayed greater neural evidence of regulation, perhaps suggesting that adolescents who are vigilant regarding peer acceptance may be most sensitive to rejection experiences.
peer rejection; adolescence; functional magnetic resonance imaging
There is a growing interest for the determinants of human choice behavior in social settings. Upon initial contact, investment choices in social settings can be inherently risky, as the degree to which the other person will reciprocate is unknown. Nevertheless, people have been shown to exhibit prosocial behavior even in one-shot laboratory settings where all interaction has been taken away. A logical step has been to link such behavior to trait empathy-related neurobiological networks. However, as a social interaction unfolds, the degree of uncertainty with respect to the expected payoff of choice behavior may change as a function of the interaction. Here we attempt to capture this factor. We show that the interpersonal tie one develops with another person during interaction – rather than trait empathy – motivates investment in a public good that is shared with an anonymous interaction partner. We examined how individual differences in trait empathy and interpersonal ties modulate neural responses to imposed monetary sharing. After, but not before interaction in a public good game, sharing prompted activation of neural systems associated with reward (striatum), empathy (anterior insular cortex and anterior cingulate cortex) as well as altruism, and social significance [posterior superior temporal sulcus (pSTS)]. Although these activations could be linked to both empathy and interpersonal ties, only tie-related pSTS activation predicted prosocial behavior during subsequent interaction, suggesting a neural substrate for keeping track of social relevance.
interpersonal ties; social ties; empathy; social decision-making; public good game; pSTS; ACC; insula
To better understand clinical empathy and what factors can undermine its experience and outcome in care-giving settings, a large-scale study was conducted with 7,584 board certified practicing physicians. Online validated instruments assessing different aspects of empathy, distress, burnout, altruistic behavior, emotional awareness, and well-being were used. Compassion satisfaction was strongly associated with empathic concern, perspective taking and altruism, while compassion fatigue (burnout and secondary traumatic stress) was more closely related to personal distress and alexithymia. Gender had a highly selective effect on empathic concern, with women displaying higher values, which led to a wide array of negative and devalued feelings. Years of experience did not influence dispositional measures per se after controlling for the effect of age and gender. Participants who experienced compassion fatigue with little to no compassion satisfaction showed the highest scores on personal distress and alexithymia as well as the strongest indicators of compassion fatigue. Physicians who have difficulty regulating their negative arousal and describing and identifying emotions seem to be more prone to emotional exhaustion, detachment, and a low sense of accomplishment. On the contrary, the ability to engage in self-other awareness and regulate one’s emotions and the tendency to help others, seem to contribute to the sense of compassion that comes from assisting patients in clinical practice.
Morally judicious behavior forms the fabric of human sociality. Here, we sought to investigate neural activity associated with different facets of moral thought. Previous research suggests that the cognitive and emotional sources of moral decisions might be closely related to theory of mind, an abstract-cognitive skill, and empathy, a rapid-emotional skill. That is, moral decisions are thought to crucially refer to other persons’ representation of intentions and behavioral outcomes as well as (vicariously experienced) emotional states. We thus hypothesized that moral decisions might be implemented in brain areas engaged in ‘theory of mind’ and empathy. This assumption was tested by conducting a large-scale activation likelihood estimation (ALE) meta-analysis of neuroimaging studies, which assessed 2,607 peak coordinates from 247 experiments in 1,790 participants. The brain areas that were consistently involved in moral decisions showed more convergence with the ALE analysis targeting theory of mind versus empathy. More specifically, the neurotopographical overlap between morality and empathy disfavors a role of affective sharing during moral decisions. Ultimately, our results provide evidence that the neural network underlying moral decisions is probably domain-global and might be dissociable into cognitive and affective sub-systems.
Electronic supplementary material
The online version of this article (doi:10.1007/s00429-012-0380-y) contains supplementary material, which is available to authorized users.
Moral cognition; Theory of mind (ToM); Empathy; Social cognition; Meta-analysis; ALE
Empathy is a complex social behaviour mediated by a network of brain structures. Recently, several functional imaging studies have investigated the neural basis of empathy, but few corroborative human lesion studies exist. Severe empathy loss is a common feature of frontotemporal lobar degeneration (FTLD), and is also seen in other neurodegenerative diseases. In this study, the neuroanatomic basis of empathy was investigated in 123 patients with FTLD, Alzheimer's disease, corticobasal degeneration and progressive supranuclear palsy using the Interpersonal Reactivity Index (IRI). IRI Empathic Concern and Perspective taking scores were correlated with structural MRI brain volume using voxel-based morphometry. Voxels in the right temporal pole, the right fusiform gyrus, the right caudate and right subcallosal gyrus correlated significantly with total empathy score (P < 0.05 after whole-brain correction for multiple comparisons). Empathy score correlated positively with the volume of right temporal structures in semantic dementia, and with subcallosal gyrus volume in frontotemporal dementia. These findings are consistent with previous research suggesting that a primarily right frontotemporal network of brain regions is involved in emotion processing, and highlights the roles of the right temporal pole and inferior frontal/striatal regions in regulating complex social interactions. This is the first large-scale lesion study to investigate the neural basis of empathy using correlational analytic methods. The results suggest that the right anterior temporal and medial frontal regions are essential for real-life empathic behaviour.
dementia; empathy; frontotemporal lobar degeneration; temporal pole; VBM
The fear facial expression is a distress cue that is associated with the provision of help and prosocial behavior. Prior psychiatric studies have found deficits in the recognition of this expression by individuals with antisocial tendencies. However, no prior study has shown accuracy for recognition of fear to predict actual prosocial or antisocial behavior in an experimental setting. In 3 studies, the authors tested the prediction that individuals who recognize fear more accurately will behave more prosocially. In Study 1, participants who identified fear more accurately also donated more money and time to a victim in a classic altruism paradigm. In Studies 2 and 3, participants’ ability to identify the fear expression predicted prosocial behavior in a novel task designed to control for confounding variables. In Study 3, accuracy for recognizing fear proved a better predictor of prosocial behavior than gender, mood, or scores on an empathy scale.
prosocial behavior; fear; facial expression; accuracy; nonverbal sensitivity
Objective and Method
Research on emotion and pain has burgeoned. We review the last decade’s literature, focusing on links between emotional processes and persistent pain.
Neurobiological research documents the neural processes that distinguish affective from sensory pain dimensions, link emotion and pain, and generate central nervous system pain sensitization. Psychological research demonstrates that greater pain is related to emotional stress and limited emotional awareness, expression, and processing. Social research shows the potential importance of emotional communication, empathy, attachment, and rejection.
Emotions are integral to the conceptualization, assessment, and treatment of persistent pain. Research should clarify when to eliminate or attenuate negative emotions, and when to access, experience, and express them. Theory and practice should integrate emotion into cognitive-behavioral models of persistent pain.
Persistent pain; chronic pain; emotion; biopsychosocial model