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
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.
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
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.
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
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
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
The error-related and feedback-related negativities (ERN and FRN) represent negative event-related potentials associated with the processing of errors and (negative) response outcomes. The neuronal source of these components is considered to be in the anterior cingulate cortex (ACC). Monitoring one’s own behavior and the impact it may have on other people or observing other individuals perform and receive feedback for their actions may also engage empathy-related processes. Empathy is conceived of as a multifaceted construct involving both cognitive and affective components, partly also supported by the ACC. The present mini-review aims to summarize the sparse database linking the electrophysiological correlates of performance monitoring to empathy. While most studies so far provide largely indirect evidence for such an association – e.g., by pointing toward altered ERN/FRN signaling in populations characterized by deviations in empathic responding – fewer investigations establish more explicit links between the two concepts. The relationship between state and, less consistently, trait measures of empathy and action monitoring might be more pronounced for observational than for active participation.
error negativity; feedback negativity; empathy; perspective taking; observation learning
Adopting another person’s visuospatial perspective has been associated with empathy, which involves adopting the psychological perspective of another individual. Both reduced empathy and abnormal visuospatial processing have been observed in those with schizophrenia and schizophrenia-related personality traits. In the current study, we sought to explore the relationship between empathy, schizotypy, and visuospatial transformation ability.
32 subjects (16 women) performed a visuospatial perspective-taking task and a mental letter rotation task. Response times and accuracy were analysed in relation to dimensions of self-reported empathy, indexed using the Interpersonal Reactivity Index, and schizotypy, as measured by the Schizotypal Personality Questionnaire.
We found that: (1) greater cognitive and affective empathy were associated with reduced negative schizotypy, and, in men, greater cognitive empathy was associated with reduced positive schizotypy; (2) improved accuracy for imagined self–other transformations in the perspective-taking task was associated with greater self-reported cognitive empathy in women and higher positive schizotypy across genders; (3) faster mental letter rotation was associated with reduced cognitive empathy and increased negative schizotypy in women.
Together, the findings partially support the commonalities in visuospatial transformation ability, empathy, and schizotypy, and posit an interesting link between spatial manipulations of our internal representations and interactions with the physical world.
Empathy; Gender differences; Mental rotation; Perspective taking; Schizotypy; Spatial ability
Studies show that measures of physician and medical students’ empathy decline with clinical training. Presently, there are limited data relating self-reported measures to observed behavior. This study explores a self-reported measure and observed empathy in medical students.
Students in the Class of 2009, at a university-based medical school, were surveyed at the end of their 2nd and 3rd year. Students completed the Jefferson Scale of Physician Empathy-Student Version (JSPE-S), a self-administered scale, and were evaluated for demonstrated empathic behavior during Objective Structured Clinical Examinations (OSCEs).
97.6% and 98.1% of eligible students participated in their 2nd and 3rd year, respectively. The overall correlation between the JSPE-S and OSCE empathy scores was 0.22, p < 0.0001. Students had higher self-reported JSPE-S scores in their 2nd year compared to their 3rd year (118.63 vs. 116.08, p < 0.0001), but had lower observed empathy scores (3.96 vs. 4.15, p < 0.0001).
Empathy measured by a self-administered scale decreased, whereas observed empathy increased among medical students with more medical training.
Electronic supplementary material
The online version of this article (doi:10.1007/s11606-009-1193-4) contains supplementary material, which is available to authorized users.
empathy; JSPE; OSCE
The current study investigated whether fiction experiences change empathy of the reader. Based on transportation theory, it was predicted that when people read fiction, and they are emotionally transported into the story, they become more empathic. Two experiments showed that empathy was influenced over a period of one week for people who read a fictional story, but only when they were emotionally transported into the story. No transportation led to lower empathy in both studies, while study 1 showed that high transportation led to higher empathy among fiction readers. These effects were not found for people in the control condition where people read non-fiction. The study showed that fiction influences empathy of the reader, but only under the condition of low or high emotional transportation into the story.
Empathy is a concept central to psychiatry, psychotherapy and clinical psychology. The construct of empathy involves not only the affective experience of the other person's actual or inferred emotional state but also some minimal recognition and understanding of another's emotional state. It is proposed, in the light of multiple levels of analysis including social psychology, cognitive neuroscience and clinical neuropsychology, a model of empathy that involves both bottom-up and top-down information processing underpinned by parallel and distributed computational mechanisms. The predictive validity of this model is explored with reference to clinical conditions. As many psychiatric conditions are associated with deficits or even lack of empathy, we discuss a limited number of these disorders including psychopathy/antisocial personality disorders, borderline and narcissistic personality disorders, autistic spectrum disorders, and alexithymia. We argue that future clinical investigations of empathy disorders can only be informative if behavioral, dispositional and biological factors are combined.
Empathy is a critical function regulating human social life. In particular, empathy for pain is a source of deep emotional feelings and a strong trigger of pro-social behavior. We investigated the existence of a racial bias in the emotional reaction to other people's pain and its link with implicit racist biases. Measuring participants’ physiological arousal, we found that Caucasian observers reacted to pain suffered by African people significantly less than to pain of Caucasian people. The reduced reaction to the pain of African individuals was also correlated with the observers’ individual implicit race bias. The role of others’ race in moderating empathic reactions is a crucial clue for understanding to what extent social interactions, and possibly integration, may be influenced by deeply rooted automatic and uncontrollable responses.
racism; empathy; prejudice; pain; skin conductance
In order to formulate a parsimonious tool to assess empathy, we used factor analysis on a combination of self-report measures to examine consensus and developed a brief self-report measure of this common factor. The Toronto Empathy Questionnaire (TEQ) represents empathy as a primarily emotional process. In three studies, the TEQ demonstrated strong convergent validity, correlating positively with behavioral measures of social decoding, self-report measures of empathy, and negatively with a measure of Autism symptomatology. Moreover, it exhibited good internal consistency and high test-retest reliability. The TEQ is a brief, reliable, and valid instrument for the assessment of empathy.
Empathy; Self-report; Questionnaire; Factor analysis