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.
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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. Among the psychological processes that are the basis for much of social perception and smooth social interaction, empathy plays a key role.
Empathy-related responding, including caring and sympathetic concern, is thought to motivate prosocial behavior, inhibit aggression and pave the way to moral reasoning [ Eisenberg and Eggum, ]. On the other hand, children suffering from certain developmental disorders such as conduct disorder and disruptive behavior disorders are considered to have little empathy and concern for the feelings and wellbeing of others, as well as a lack of remorse and guilt, all of which are regarded as risk factors in developing hostile, aggressive or even violent behavior [ de Wied et al.
This paper critically examines our current knowledge about the development of the mechanisms that support the experience of empathy and associated behavioral responses such as sympathy in the human brain. I begin by clarifying some definitional issues of empathy and associated phenomena.
Next I address the neurodevelopment of empathy in relation to a model that distinguishes a bottom-up processing of affective communication, b emotion understanding, c top-down reappraisal processing in which the perceiver's motivation, intentions and attitudes moderate the extent of an empathic experience, and d an awareness of a self-other differentiation.
I argue that studying subcomponents of more complex sociopsychological constructs like empathy can be particularly useful from a neurodevelopmental perspective when only some of its components or precursors may be observable. Developmental studies provide unique opportunities to see how the components of the system interact in ways that are not possible in adults when all the components are fully mature and operational [ de Haan and Gunnar, ].
Until quite recently, research on the development of empathy-related responding from a neurobiological level of analysis has been relatively sparse. Integrating this neuroperspective with behavioral work can shed light upon the neurobiological mechanisms underpinning the basic building blocks of empathy and sympathy and their age-related functional changes.
Such integration can help us understand the neural processes that underpin prosocial behavior and can also benefit interventions in individuals with atypical development such as antisocial behavior problems.
The term empathy is applied to various phenomena which cover a broad spectrum ranging from feelings of concern for other people that create a motivation to help them, experiencing emotions that match another individual's emotions, knowing what the other is thinking or feeling, to blurring the line between self and other [ Hodges and Klein, ].
In developmental psychology, empathy is generally defined as an affective response stemming from the understanding of another's emotional state or condition similar to what the other person is feeling or would be expected to feel in the given situation [ Eisenberg et al. Very often, empathy and sympathy are conflated. Here, I distinguish between empathy, simply defined as the ability to recognize the emotions and feelings of others with a minimal distinction between self and other, and sympathy, i.
While empathy and sympathy are often confused, the two can be dissociated, and although sympathy may stem from the apprehension of another's emotional state, it does not have to be congruent with the affective state of the other.
Given the complexity of what encompasses the phenomenological experience of empathy, investigation of its neurobiological underpinnings would be worthless without breaking down this construct into component processes fig. In spite of reports in the popular press that give the appealing, yet wrong, notion that the organization of psychological phenomena maps in a fashion into the organization of the underlying neural substrate, in reality, empathy, like other social cognitive processes, draws on a large array of brain structures and systems which are not limited to the cortex but also include subcortical pathways, the autonomic nervous system, hypothalamic-pituitary-adrenal axis, and endocrine systems that regulate bodily states, emotion and reactivity [ Carter et al.
Moreover, sympathy or empathic concern has multiple antecedents within and across levels of organization, and a comprehensive social neuroscience theory of empathy requires the specification of various causal mechanisms producing some outcome variable e. Schematic illustration of the macrocomponents involved in human empathy. These different components are intertwined and contribute to different aspects of the experience of empathy.
They can be dissociated by brain lesions. Affective arousal: first component in place in development having evolved to differentiate hostile from hospitable stimuli and to organize adaptive responses to these stimuli. This component refers to the automatic discrimination of a stimulus — or features of a stimulus — as appetitive or aversive, hostile or hospitable, pleasant or unpleasant, threatening or nurturing.
Subcortical circuits including the amygdala, hypothalamus, hippocampus and orbitofrontal cortex OFC are the essential neural components of affective arousal.
The amygdala and OFC with reciprocal connection with the superior temporal sulcus STS underlie rapid and prioritized processing of the emotion signal. Emotion understanding: develops later, and begins to be really mature around the age of 2—3 years. This component largely overlaps with theory-of-mind-like processing and draws on the ventromedial vm and medial m prefrontal cortex PFC as well as executive functions.
The latter allow the child to entertain several perspectives and a decoupling mechanism between first-person and second-person information. Emotion regulation: enables the control of emotion, affect, drive and motivation. This component develops throughout childhood and adolescence, and parallels the maturation of execution functions. Humans also have the capacity to appraise and reappraise emotions and feelings.
Thus, empathy is not a passive affective resonance phenomenon with the emotions of others. Rather, goals, intentions, context and motivations play feed-forward roles in how emotions are perceived and experienced. From this model, it is clear that empathy is implemented by a complex network of distributed, often recursively connected, interacting neural regions STS, insula, mPFC and vmPFC, amygdala and ACC as well as autonomic and neuroendocrine processes implicated in social behaviors and emotional states.
Empathy is not unique to humans as many of the physiological mechanisms are shared with other mammalian species. Recognizing and evaluating signals of distress from newborns and infants is of primary importance in parental care for offspring survival and fitness. The thalamocingulate division of the forebrain is believed to have evolved in parallel with social behaviors related to the perception of emotional information involved in securing emotional bonding and social interactions [ MacLean, ].
However, humans are special in the sense that high-level cognitive abilities such as executive function, language and theory of mind ToM are layered on top of phylogenetically older social and emotional capacities.
These evolutionarily newer aspects of information processing expand the range of behaviors that can be driven by empathy like caring for and helping outgroup members or even individuals from different species.
Recent affective neuroscience research with children and adult participants indicates that the affective, cognitive and regulatory aspects of empathy involve interacting, yet partially nonoverlapping, neural circuits. Furthermore, there is now evidence for age-related changes in these neural circuits which, together with behavioral measures, reflect how brain maturation influences reactions to the distress of others [ Decety and Michalska, ]. Empathy typically emerges as the child comes to a greater awareness of the experience of others, during the second and third years of life, and arises in the context of a social interaction.
Each of the components of empathy affective arousal, emotion understanding and emotion regulation will be considered separately from both developmental and neuroscientific perspectives. These components are indeed dissociable, as documented in studies with neurological patients [ Decety, ; Strum et al. There is compelling evidence that prosocial behaviors such as altruistic helping emerge early in childhood.
Infants as young as 12 months of age begin to comfort victims of distress, and to month-old children display spontaneous, unrewarded helping behaviors [ Warneken and Tomasello, ]. In addition, both genetic and environmental factors contribute to the development of empathy and prosociality [ Knafo et al. Most scholars agree that empathy includes both cognitive and affective components [ Decety and Jackson, ; Eisenberg and Eggum, ; Hodges and Klein, ] that have different developmental trajectories.
Based on both theories and empirical evidence from affective neuroscience and developmental psychology, one may propose a model that includes bottom-up processing of affective sharing and top-down processing in which the perceiver's motivation, intentions and attitudes influence the extent of an empathic experience, and the likelihood of prosocial behavior [ Decety, ; Decety and Meyer, ]. In that model, a number of distinct and interacting neurocognitive components contribute to the experience of empathy: 1 affective arousal, a bottom-up process in which the amygdala, hypothalamus and orbitofrontal cortex OFC underlie rapid and prioritized processing of the emotion signal; 2 emotion understanding, which relies on self- and other-awareness and involves the medial prefrontal cortex mPFC , ventromedial vm PFC and temporoparietal junction TPJ , and 3 emotion regulation, which depends on executive functions instantiated in the intrinsic corticocortical connections of the OFC, mPFC and dorsolateral dl PFC, as well as on connections with subcortical limbic structures implicated in processing emotional information.
These networks operate as top-down mediators crucial in regulating emotions and thereby enhancing flexible and appropriate responses. There is ample behavioral evidence demonstrating that the affective component of empathy develops earlier than the cognitive components. Prior to the onset of language, the primary means by which infants can communicate with others in their environment is by reading faces [ Leppanen and Nelson, ].
Thus, it is important for an infant not only to discriminate familiar from unfamiliar individuals, but also to derive information about the individual's feelings and intentions, for example, whether the caregiver is pleased or displeased, afraid or angry [ Ludemann and Nelson, ]. Affective responsiveness is known to be present at an early age, is involuntary, and relies on mimicry and somatosensorimotor resonance between other and self.
For instance, newborns and infants become vigorously distressed shortly after another infant begins to cry [ Dondi et al. Discrete facial expressions of emotion have been identified in newborns, including joy, interest, disgust and distress [ Izard, ], suggesting that subcomponents of emotional experience and expression are present at birth, and supporting the possibility that these processes are hard-wired in the brain.
Human newborns by 10 weeks of age are capable of imitating expression of fear, sadness, and surprise [ Haviland and Lewica, ], preparing the individual for later empathic connections through affective interaction with others. One fMRI study directly examined the relationship between MNS activity and two distinct indicators of social functioning in typically developing year-olds: empathy and interpersonal competence [ Pfeifer et al. Reliable activity in the inferior frontal gyrus was associated with both observation and imitation of emotional expressions.
Importantly, activity in this region was significantly and positively correlated with behavioral measures, indexing the empathic behavior of children. But see a critical appraisal of the contribution of the MNS to empathy in Decety [ ]. Together, these findings indicate that, very early on, infants are able to perceive and respond to another's affective state.
This automatic emotional resonance between other and self relies on a tight coupling between perceptual processing and emotion-related neural circuits. Infant arousal in response to the affects signaled by others can serve as an instrument for social learning, reinforcing the significance of the social exchange, which then becomes associated with the infant's own emotional experience. Consequently, infants come to experience emotions as shared states and learn to differentiate their own states partly by witnessing the resonant responses that they elicit in others [ Nielsen, ].
While the capacity for two people to resonate with each other affectively, prior to any cognitive understanding, is the basis for developing shared emotional meanings, it is not enough for mature empathic understanding. Such an understanding requires the formation of an explicit representation of the feelings of another person as an intentional agent, which necessitates additional computational mechanisms beyond the affect sharing level [ Decety et al. The cognitive components that give way to empathic understanding have a more protracted course of development than the affective components, even though many precursors are already in place very early in life.
An experience of emotion is a state of mind the content of which is at once affective pleasant or unpleasant and conceptual a representation of the individual relation to the surrounding world [ Barrett et al. Emotion is also, however, an interpersonal communication system that elicits response from others.
Thus, emotions can be viewed both as intrapersonal and interpersonal states, and the construct of empathy entails both such dimensions. A number of studies have shown that the reliable perception of facial expressions, such as attention to configural rather than featural information in faces and the ability to recognize facial expressions across variations in identity or intensity, are not present until the age of 5—7 months [ Haviland and Lewica, ].
Some questions remain as to whether these early reactions represent recognition of emotion in another or simple mimicry, but by 2 years of age, most children use emotion labels for facial expressions and talk about emotion topics [ Gross and Ballif, ]. Recent work has documented that even very young children 18—25 months old can sympathize with a victim even in the absence of overt emotion cues [ Vaish et al. Regarding the causes and effects of emotion and the cues used in inferring emotion, developmental research has detailed a progression from situation-bound, behavioral explanations of emotion to broader, more mentalistic understandings [ Harris et al.
As children develop, their emotional inferences contain a more complex and differentiated use of several types of information, such as relational and contextual factors and the goals or beliefs of the target child [ Harris, ]. This development appears to be somewhat slower for complex social emotions like pride, shame or embarrassment [ Lewis, ]. Development of this understanding proceeds from lack of acknowledgement of multiple emotions in younger children, to acknowledgement of different variables such as emotion valence and emotion intensity [ Carroll and Steward, ].
These cognitive aspects of empathy are closely related to processes involved in ToM, executive function and self-regulation. There is growing evidence documenting that executive function and ToM are fundamentally linked in development and their relationship is stable [ Carlson et al. Several studies have shown that, by around 4 years of age, children can understand that the emotion a person feels about a given event depends upon that person's perception of the event and their beliefs and desires about it.
Notably, a longitudinal study of children aged 47—60 months examined developmental changes in understanding of false belief and emotion, as well as mental-state conversation with friends [ Hughes and Dunn, ]. They found that individual differences in understanding of both false belief and emotion were stable over this time period and were significantly related to each other.
Emotion recognition continues to develop into later adolescence [ Tonks et al. ToM is layered on top of affective processes and its development depends on the forging of connections between brain circuits for domain-general cognition and circuits specialized for aspects of social understanding.
Neuroimaging studies have identified a circumscribed neural network reliably underpinning the understanding of mental states self and other that links the mPFC with the posterior superior temporal sulcus at the TPJ [ Brunet et al.
These regions were activated in children aged 6—11 years while they were listening to sections of a story describing a character's thoughts compared to sections of the same story that described the physical context [ Saxe et al.
Further, change in response selectivity with age was observed in the right TPJ, which was recruited equally for mental and physical facts about people in younger children, but only for mental facts in older children. Results from a study with 4-year-old children showed that individual differences in EEG alpha activity localized to the dorsal mPFC and the right TPJ were positively associated with children's ToM performance, which suggests that the maturation of the dorsal mPFC and right TPJ is a critical constituent of the explicit ToM development of preschoolers [ Sabbagh et al.
Support for age-related changes in brain activity associated with metacognition is also provided by an fMRI investigation of ToM in participants whose age ranged between 9 and 16 years [ Moriguchi et al. Both children and adolescents demonstrated significant activation in the neural circuits associated with mentalizing tasks, including the TPJ, the temporal poles and mPFC.
The Neurodevelopment of Empathy in Humans
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Jean Decety is the Irving B. Professor Decety received a Ph. Huppert, E. Decety, J.
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