ArticlePDF AvailableLiterature Review

The Neural Basis of Empathy

DOI:10.1146/annurev-neuro-062111-150536
Authors:
Boris Bernhardt at McGill University
Boris Bernhardt
Tania Singer at Max Planck Society
Tania Singer
Download full-text PDF
Read full-text
Download citation

Abstract

Empathy--the ability to share the feelings of others--is fundamental to our emotional and social lives. Previous human imaging studies focusing on empathy for others' pain have consistently shown activations in regions also involved in the direct pain experience, particularly anterior insula and anterior and midcingulate cortex. These findings suggest that empathy is, in part, based on shared representations for firsthand and vicarious experiences of affective states. Empathic responses are not static but can be modulated by person characteristics, such as degree of alexithymia. It has also been shown that contextual appraisal, including perceived fairness or group membership of others, may modulate empathic neuronal activations. Empathy often involves coactivations in further networks associated with social cognition, depending on the specific situation and information available in the environment. Empathy-related insular and cingulate activity may reflect domain-general computations representing and predicting feeling states in self and others, likely guiding adaptive homeostatic responses and goal-directed behavior in dynamic social contexts.
Content uploaded by Boris Bernhardt
Author content
All content in this area was uploaded by Boris Bernhardt on Jun 30, 2015
Content may be subject to copyright.
Many thanks for your interest in our review on the neural basis of empathy. The pdf of
the document is:
http://www.annualreviews.org/eprint/dRDAUj5ykYken4M7VW6W/full/10.1146/annurev-neuro-062111-150536
Annual reviews kindly asked us to also add the following statement to the pdf:
"I am pleased to provide you complimentary one-time access to my Annual Reviews
article as a PDF file, for your own personal use. Any further/multiple distribution,
publication, or commercial usage of this copyrighted material requires submission of a
permission request addressed to the Copyright Clearance Center
(http://www.copyright.com/).”

Supplementary resource (1)

Annrev statement
Data
June 2015
Boris Bernhardt · Tania Singer
... Remarkably, these activity patterns are highly similar to those measured when pain is experienced directly by oneself (Berluti et al., 2020;Braboszcz et al., 2017;Corradi-Dell'Acqua et al., 2011O'Connell et al., 2019;Qiao-Tasserit et al., 2018;Wagner et al., 2020;Zhou et al., 2020), and they are attenuated by those same analgesic procedures that regulate firsthand nociception, such as placebo or hypnosis (Braboszcz et al., 2017;Rütgen et al., 2015Rütgen et al., , 2021. These results suggest that others' pain is at least partly processed in an embodied (or empathetic) fashion, that is, by simulating its somatic and affective properties on one's own body (Bastiaansen et al., 2009;Bernhardt & Singer, 2012). Critically, medical practitioners and students exhibit lower activity in these regions to the sight of injuries and painful expressions (Chen et al., 2022;Cheng et al., 2007Cheng et al., , 2017Dirupo et al., 2021;Jackson et al., 2017). ...
... Representational similarity between responses to one's and others' pain in regions such AI has been often interpreted as a neural substrate for the ability to embody, and empathize with, others' states (Bastiaansen et al., 2009;Bernhardt & Singer, 2012). In the current study we did not measure individual empathy traits to corroborate this claim. ...
Healthcare experience affects pain-specific responses to others' suffering in the anterior insula
Article
Full-text available
Medical students and professional healthcare providers often underestimate patients' pain, together with decreased neural responses to pain information in the anterior insula (AI), a brain region implicated in self-pain processing and negative affect. However, the functional significance and specificity of these neural changes remains debated. Across two experiments, we recruited university medical students and emergency nurses to test the role of healthcare experience on the brain reactivity to other's pain, emotions, and beliefs, using both pictorial and verbal cues. Brain responses to self-pain was also assessed and compared with those to observed pain. Our results confirmed that healthcare experience decreased the activity in AI in response to others' suffering. This effect was independent from stimulus modality (pictures or texts), but specific for pain, as it did not generalize to inferences about other mental or affective states. Furthermore, representational similarity and multivariate pattern analysis revealed that healthcare experience impacted specifically a component of the neural representation of others' pain that is shared with that of first-hand nociception, and related more to AI than to other pain-responsive regions. Taken together, our study suggests a decreased propensity to appraise others' suffering as one's own, associated with a reduced recruitment of pain-specific information in AI. These findings provide new insights into neural mechanisms leading to pain underestimation by caregivers in clinical settings.
View
... Empathy, which is defined as the ability to share and understand the mental states of others [1], has been widely studied in affective and social neurosciences [1][2][3][4][5]. Although different theoretical models have been proposed to describe its underlying processes, scholars in neuroscience agree that empathy involves at least two core processes: (1) a mostly automatic emotional sharing of other people's states, called affective resonance, which allows an individual to represent what the other person might feel based on one's own, similar, affective experiences, and (2) a more controlled cognitive process, called perspective-taking (or mentalising), which refers to explicit reasoning about others' mental states [1,[5][6][7][8]. ...
Biological postural oscillations during facial expression of pain in virtual characters modulate early and late ERP components associated with empathy: A pilot study
Article
Full-text available
  • Aug 2023
There is a surge in the use of virtual characters in cognitive sciences. However, their behavioural realism remains to be perfected in order to trigger more spontaneous and socially expected reactions in users. It was recently shown that biological postural oscillations (idle motion) were a key ingredient to enhance the empathic response to its facial pain expression. The objective of this study was to examine, using electroencephalography, whether idle motion would modulate the neural response associated with empathy when viewing a pain-expressing virtual character. Twenty healthy young adults were shown video clips of a virtual character displaying a facial expression of pain while its body was either static (Still condition) or animated with pre-recorded human postural oscillations (Idle condition). Participants rated the virtual human's facial expression of pain as significantly more intense in the Idle condition compared to the Still condition. Both the early (N2-N3) and the late (rLPP) event-related potentials (ERPs) associated with distinct dimensions of empathy, affective resonance and perspective-taking, respectively, were greater in the Idle condition compared to the Still condition. These findings confirm the potential of idle motion to increase empathy for pain expressed by virtual characters. They are discussed in line with contemporary empathy models in relation to human-machine interactions.
View
... In humans, putative mirroring network is formed from collection of regions including the inferior frontal gyrus (IFG), inferior parietal lobule (IPL), superior temporal sulcus, anterior insula, ACC, and amygdala [16][17][18][19] . It is known that SC can be strongly associated with compassion for others in a general pattern 1,20,21 . ...
Self-compassion is associated with the superior longitudinal fasciculus in the mirroring network in healthy individuals
Article
Full-text available
  • Jul 2023
Self-compassion (SC) involves taking an emotionally positive attitude towards oneself when suffering. Although SC has positive effects on mental well-being as well as a protective role in preventing symptoms in healthy individuals, few studies on white matter (WM) microstructures in neuroimaging studies of SC has been studied. Brain imaging data were acquired from 71 healthy participants. WM regions of mirroring network were analyzed using tract-based spatial statistics. After the WM regions associated with SC were extracted, exploratory correlation analysis with the self-forgiveness scale, the coping scale, and the world health organization quality of life scale abbreviated version was performed. We found that self-compassion scale total scores were negatively correlated with the fractional anisotropy (FA) values of the superior longitudinal fasciculus (SLF) in healthy individuals. The self-kindness and mindfulness subscale scores were also negatively correlated with FA values of the same regions. These FA values were negatively correlated with the total scores of self-forgiveness scale, and self-control coping strategy and confrontation coping strategy. Our findings suggest levels of SC may be associated with WM microstructural changes of SLF in healthy individuals. These lower WM microstructures may be associated with positive personal attitudes, such as self-forgiveness, self-control and active confrontational strategies.
View
... One of the hubs of the salience network, the ACC, is an area of particular interest as this region is involved in empathy (Bernhardt and Singer, 2012;Decety et al., 2012;Preston and de Waal, 2002), cognitive and emotional processing (Bush et al., 2000;Heilbronner and Hayden, 2016;Vogt, 2016). Because empathy is necessary to be successful in aspects of the MSCEIT , the ACC is hypothesized to be critical to performance on them. ...
View
Регуляция поведения и когнитивной деятельности в подростковом возрасте. Мозговые механизмы/Под ред. Р. И. Мачинской, Д. А. Фарбер. М. : Изд-во Московского психолого-социального университета, 2023. — 616 с
Book
Full-text available
  • Sep 2023
В книге обобщены исследования коллектива авторов, посвященные актуальным проблемам мозгового обеспечения регуляции поведения и когнитивной деятельности в подростковом возрасте. Морфологические, нейрофизиологические и нейропсихологические исследования, представленные в книге, свидетельствуют о существенных преобразованиях мозговой организации процессов регуляции познавательной деятельности и поведения у подростков. При этом направленность таких изменений — прогресс или снижение функциональных возможностей — различна для разных звеньев мозговых регуляторных систем и меняется с возрастом. Наиболее существенные изменения в подростковом возрасте претерпевают системы эмоционально-мотивационной регуляции, что в значительной степени увеличивает риск учебной и социальной дезадаптации. Книга предназначена для физиологов, психологов, педагогов и студентов биологического, психолого-педагогического и клинико-психологического профиля.
View
View
View
Empathy deficits, callous-unemotional traits and structural underpinnings in autism spectrum disorder and conduct disorder youth
Article
Distinct empathy deficits are often described in patients with conduct disorder (CD) and autism spectrum disorder (ASD) yet their neural underpinnings and the influence of comorbid Callous-Unemotional (CU) traits are unclear. This study compares the cognitive (CE) and affective empathy (AE) abilities of youth with CD and ASD, their potential neuroanatomical correlates, and the influence of CU traits on empathy. Adolescents and parents/caregivers completed empathy questionnaires (N = 148 adolescents, mean age = 15.16 years) and T1 weighted images were obtained from a subsample (N = 130). Group differences in empathy and the influence of CU traits were investigated using Bayesian analyses and Voxel-Based Morphometry with Threshold-Free Cluster Enhancement focusing on regions involved in AE (insula, amygdala, inferior frontal gyrus and cingulate cortex) and CE processes (ventromedial prefrontal cortex, temporoparietal junction, superior temporal gyrus, and precuneus). The ASD group showed lower parent-reported AE and CE scores and lower self-reported CE scores while the CD group showed lower parent-reported CE scores than controls. When accounting for the influence of CU traits no AE deficits in ASD and CE deficits in CD were found, but CE deficits in ASD remained. Across all participants, CU traits were negatively associated with gray matter volumes in anterior cingulate which extends into the mid cingulate, ventromedial prefrontal cortex, and precuneus. Thus, although co-occurring CU traits have been linked to global empathy deficits in reports and underlying brain structures, its influence on empathy aspects might be disorder-specific. Investigating the subdimensions of empathy may therefore help to identify disorder-specific empathy deficits.
View
Stress and Pain
Chapter
  • Aug 2023
The stress reaction system consists of two different levels, the soma, and the mind. In response to critical life events, so-called stressors, there is a coordinated and energizing response, which maintains physical integrity and psychic well-being. Stressful adverse experiences in early childhood are associated with decreased stress reactivity and increased impulsive behavior. In young children, regardless of the actual stressors, three different types of stress reactions are distinguished, based on their potential to cause lasting physiological disorders: a positive, a tolerable and a toxic stress. Prenatal stress, stress in infancy and in separation situations are discussed.Pain contains both sensory and affective dimensions. Pain and stress are processed in the same brain regions. Prefrontal cortical areas as well as subcortical areas contribute to the conscious awareness and the affective and cognitive evaluation of pain. Infants and toddlers have not yet acquired the ability to reflectively perceive and express their feelings in a stressful situation. An emotionally too violent or painful experience may be expressed by the body in behavioral manifestations, psychosomatic disorders, or developmental dysfunctions. Unrecognized, or poorly treated pain in childhood leads to serious and long-lasting negative consequences that persist into adulthood.KeywordsStress responseDifferent types of stressSeparation stressPainPain expressions
View
Measuring perceived empathy in dialogue systems
Article
Full-text available
Dialogue systems, from Virtual Personal Assistants such as Siri, Cortana, and Alexa to state-of-the-art systems such as BlenderBot3 and ChatGPT, are already widely available, used in a variety of applications, and are increasingly part of many people’s lives. However, the task of enabling them to use empathetic language more convincingly is still an emerging research topic. Such systems generally make use of complex neural networks to learn the patterns of typical human language use, and the interactions in which the systems participate are usually mediated either via interactive text-based or speech-based interfaces. In human–human interaction, empathy has been shown to promote prosocial behaviour and improve interaction. In the context of dialogue systems, to advance the understanding of how perceptions of empathy affect interactions, it is necessary to bring greater clarity to how empathy is measured and assessed. Assessing the way dialogue systems create perceptions of empathy brings together a range of technological, psychological, and ethical considerations that merit greater scrutiny than they have received so far. However, there is currently no widely accepted evaluation method for determining the degree of empathy that any given system possesses (or, at least, appears to possess). Currently, different research teams use a variety of automated metrics, alongside different forms of subjective human assessment such as questionnaires, self-assessment measures and narrative engagement scales. This diversity of evaluation practice means that, given two DSs, it is usually impossible to determine which of them conveys the greater degree of empathy in its dialogic exchanges with human users. Acknowledging this problem, the present article provides an overview of how empathy is measured in human–human interactions and considers some of the ways it is currently measured in human–DS interactions. Finally, it introduces a novel third-person analytical framework, called the Empathy Scale for Human–Computer Communication (ESHCC), to support greater uniformity in how perceived empathy is measured during interactions with state-of-the-art DSs.
View
The Social Neuroscience of Empathy
Article
Full-text available
  • Mar 2009
The phenomenon of empathy entails the ability to share the affective experiences of others. In recent years social neuroscience made considerable progress in revealing the mechanisms that enable a person to feel what another is feeling. The present review provides an in-depth and critical discussion of these findings. Consistent evidence shows that sharing the emotions of others is associated with activation in neural structures that are also active during the first-hand experience of that emotion. Part of the neural activation shared between self- and other-related experiences seems to be rather automatically activated. However, recent studies also show that empathy is a highly flexible phenomenon, and that vicarious responses are malleable with respect to a number of factors--such as contextual appraisal, the interpersonal relationship between empathizer and other, or the perspective adopted during observation of the other. Future investigations are needed to provide more detailed insights into these factors and their neural underpinnings. Questions such as whether individual differences in empathy can be explained by stable personality traits, whether we can train ourselves to be more empathic, and how empathy relates to prosocial behavior are of utmost relevance for both science and society.
View
REVIEW ARTICLE: Contributions of anterior cingulate cortex to behaviour
Article
Full-text available
Assessments of anterior cingulate cortex in experimental animals and humans have led to unifying theories of its structural organization and contributions to mammalian behaviour The anterior cingulate cortex forms a large region around the rostrum of the corpus callosum that is termed the anterior executive region. This region has numerous projections into motor systems, however since these projections originate from different parts of anterior cingulate cortex and because functional studies have shown that it does not have a uniform contribution to brain functions, the anterior executive region is further subdivided into 'affect' and 'cognition' components. The affect division includes areas 25, 33 and rostral area 24, and has extensive connections with the amygdala and periaqueductal grey, and parts of it project to autonomic brainstem motor nuclei. In addition to regulating autonomic and endocrine functions, it is involved in conditioned emotional learning, vocalizations associated with expressing internal states, assessments of motivational content and assigning emotional valence to internal and external stimuli, and maternal-infant interactions. The cognition divi sion includes caudal areas 24' and 32', the cingulate motor areas in the cingulate sulcus and nociceptive cortex. The cingulate motor areas project to the spinal cord and red nucleus and have premotor functions, while the nociceptive area is engaged in both response selection and cognitively demanding information processing. The cingulate epilepsy syndrome provides important support of experimental animal and human functional imaging studies for the role of anterior cingulate cortex in movement affect and social behaviours. Excessive cingulate activity in cases with seizures confirmed in anterior cingulate cortex with subdural electrode recordings, can impair consciousness alter affective stare and expression, and influence skeletomotor and autonomic activity. Interictally, patients with anterior cingulate cortex epilepsy often display psychopathic or sociopathic behaviours. In other clinical examples of elevated anterior cingulate cortex activity it may contribute to ties, obsessive-compulsive behaviours, and aberrent social behaviour. Conversely, reduced cingulate activity following infarcts or surgery can contribute to behavioural disorders including akinetic mutism, diminished self-awareness and depression, motor neglect and impaired motor initiation, reduced responses to pain, and aberrent social behaviour. The role of anterior cingulate cortex in pain responsiveness is suggested by cingulumotomy results and functional imaging studies during noxious somatic stimulation. The affect division of anterior cingulate cortex modulates autonomic activity and internal emotional responses, while the cognition division is engaged in response selection associated with skeletomotor activity and responses to noxious stimuli. Over-all, anterior cingulate cortex appears to play a crucial role in initiation, motivation, and goal-directed behaviours. The anterior cingulate cortex is part of a larger matrix of structures that are engaged in similar functions. These structures from the rostral limbic system and include the amygdala, periaqueductal grey, ventral striatum, orbitofrontal and anterior insular cortices. The system formed by these interconnected areas assesses the motivational content of internal and external stimuli and regulates context-dependent behaviours.
View
Measuring individual differences in empathy: Evidence for multidimensional approach.
Article
  • Jan 1983
To facilitate a multidimensional approach to empathy the Interpersonal Reactivity Index (IRI) includes 4 subscales: Perspective-Taking (PT) Fantasy (FS) Empathic Concern (EC) and Personal Distress (PD). The aim of the present study was to establish the convergent and discriminant validity of these 4 subscales. Hypothesized relationships among the IRI subscales between the subscales and measures of other psychological constructs (social functioning self-esteem emotionality and sensitivity to others) and between the subscales and extant empathy measures were examined. Study subjects included 677 male and 667 female students enrolled in undergraduate psychology classes at the University of Texas. The IRI scales not only exhibited the predicted relationships among themselves but also were related in the expected manner to other measures. Higher PT scores were consistently associated with better social functioning and higher self-esteem; in contrast Fantasy scores were unrelated to these 2 characteristics. High EC scores were positively associated with shyness and anxiety but negatively linked to egotism. The most substantial relationships in the study involved the PD scale. PD scores were strongly linked with low self-esteem and poor interpersonal functioning as well as a constellation of vulnerability uncertainty and fearfulness. These findings support a multidimensional approach to empathy by providing evidence that the 4 qualities tapped by the IRI are indeed separate constructs each related in specific ways to other psychological measures.
View
View
Empathic Distress Fatigue Rather Than Compassion Fatigue? Integrating Findings from Empathy Research in Psychology and Social Neuroscience
Chapter
  • Dec 2011
In this chapter, we discuss the role of empathy as the main precursor for prosocial behavior, taking perspectives that span from social and developmental psychology to social neuroscience. We begin by introducing compassion fatigue in caregivers as a form of pathological altruism. We move on to introduce such relevant concepts as empathy, compassion, empathic concern, and distress; we then review relevant empirical findings from social and developmental psychology and social neuroscience. Finally, we propose a new integrative model that suggests that the term compassion fatigue should be replaced by the term empathic distress fatigue to more accurately account for symptoms of withdrawal and burnout. We conclude by outlining potential ways to circumvent the downside of too much empathy.
View
Modes of Linkage Between Perception and Action
Chapter
  • Jan 1984
The problem of understanding the nature of the linkage between perception and action can be raised at two different levels: execution and initiation. At the level of execution the linkage problem is mainly related to the conditions and mechanisms of interaction between efferent and afferent information during the execution of a given movement or response. Relevant issues such as open vs. closed loop control or feed backward vs. feed forward have recently attracted considerable interest in the field of motor learning and motor control (e.g., Adams, 1971; Schmidt, 1975; Keele, 1981; see also Shebilske and Wolff, this volume).
View
Social Preferences and the Brain
Chapter
  • Dec 2009
Social preference theories and the knowledge about the relative strength of the different motivational forces in different environments can be useful in interpreting neural data. Research on the emotional underpinnings of social preferences, and the neural networks involved in social preference emotions, may also be useful for economics, because it helps to understand when social preferences are likely to affect behavior and when not. Such research may also help to gain deeper insights into the reasons for inter-individual differences in social preferences. In this context, studies examining whether social preferences are stable attributes of individuals or stable attributes of situations are important. If social preferences are stable personality traits, it makes sense for organizations to invest resources into the screening of people; however, if social preferences are mainly an attribute of the environment, it makes sense to shape them, designing the environment appropriately.
View
The effect of negative emotional context on neural and behavioural responses to oesophageal stimulation
Article
Sensory experience is influenced by emotional context. Although perception of emotion and unpleasant visceral sensation are associated with activation within the insula and dorsal and ventral anterior cingulate gyri (ACG), regions important for attention to and perception of sensory and emotional information, the neural mechanisms underlying the effect of emotional context upon visceral sensation remain unexplored. Using functional MRI, we examined neural responses to phasic, non-painful oesophageal sensation (OS) in eight healthy subjects (seven male; age range 27-36 years) either during neutral or negative emotional contexts produced, respectively, by presentation of neutral or fearful facial expressions. Activation within right insular and bilateral dorsal ACG was significantly greater (P < 0.01) during OS with fearful than with neutral faces. In a second experiment, we measured anxiety, discomfort and neural responses in eight healthy male subjects (age range 22-41 years) to phasic, non-painful OS during presentation of faces depicting either low, moderate or high intensities of fear. Significantly greater (P < 0.01) discomfort, anxiety and activation predominantly within the left dorsal ACG and bilateral anterior insulae occurred with high-intensity compared with low-intensity expressions. Clusters of voxels were also detected in this region, which exhibited a positive correlation between subjective behaviour and blood oxygenation level-dependent effect (P < 0.05). We report the first evidence for a modulation of neural responses, and perceived discomfort during, non-painful visceral stimulation by the intensity of the negative emotional context in which the stimulation occurs, and suggest a mechanism for the effect of negative context on symptoms in functional pain disorders.
View
A Touching Sight
Article
Watching the movie scene in which a tarantula crawls on James Bond's chest can make us literally shiver—as if the spider crawled on our own chest. What neural mechanisms are responsible for this “tactile empathy”? The observation of the actions of others activates the premotor cortex normally involved in the execution of the same actions. If a similar mechanism applies to the sight of touch, movies depicting touch should automatically activate the somatosensory cortex of the observer. Here we found using fMRI that the secondary but not the primary somatosensory cortex is activated both when the participants were touched and when they observed someone or something else getting touched by objects. The neural mechanisms enabling our own sensation of touch may therefore be a window also to our understanding of touch.
View
The Distinction Between Sympathy and Empathy. To Call Forth a Concept, A Word Is Needed
Article
  • Feb 1986
Discusses the ways in which the terms sympathy and empathy have been used in psychology and suggests that these terms (a) have different historical roots, (b) have been utilized in different research paradigms, and (c) have been involved in different kinds of theorizing. It is suggested that sympathy refers to the heightened awareness of another's plight as something to be alleviated, whereas empathy refers to the attempt of one self-aware self to understand the subjective experiences of another. It is argued that these are different psychological processes and that the differences between them should not be obfuscated. (98 ref) (PsycINFO Database Record (c) 2012 APA, all rights reserved)
View