Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood

Developmental Science, 2009

Empathy and sympathy play crucial roles in much of human social interaction and are necessary components for healthy coexistence. Sympathy is thought to be a proxy for motivating prosocial behavior and providing the affective and motivational base for moral development. The purpose of the present study was to use functional MRI to characterize developmental changes in brain activation in the neural circuits underpinning empathy and sympathy. Fifty-seven individuals, whose age ranged from 7 to 40 years old, were presented with short animated visual stimuli depicting painful and non-painful situations. These situations involved either a person whose pain was accidentally caused or a person whose pain was intentionally inflicted by another individual to elicit empathic (feeling as the other) or sympathetic (feeling concern for the other) emotions, respectively. Results demonstrate monotonic age-related changes in the amygdala, supplementary motor area, and posterior insula when participants were exposed to painful situations that were accidentally caused. When participants observed painful situations intentionally inflicted by another individual, age-related changes were detected in the dorsolateral prefrontal and ventromedial prefrontal cortex, with a gradual shift in that latter region from its medial to its lateral portion. This pattern of activation reflects a change from a visceral emotional response critical for the analysis of the affective significance of stimuli to a more evaluative function. Further, these data provide evidence for partially distinct neural mechanisms subserving empathy and sympathy, and demonstrate the usefulness of a developmental neurobiological approach to the new emerging area of moral neuroscience.

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

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.

Empathy reflects an innate ability to perceive and be sensitive to the emotional states of others coupled with a motivation to care for their wellbeing. It has evolved in the context of parental care for offspring as well as within kinship. Current work demonstrates that empathy is underpinned by circuits connecting the brainstem, amygdala, basal ganglia, anterior cingulate cortex, insula and orbitofrontal cortex, which are conserved across many species. Empirical studies document that empathetic reactions emerge early in life, and that they are not automatic. Rather they are heavily influenced and modulated by interpersonal and contextual factors, which impact behavior and cognitions. However, the mechanisms supporting empathy are also flexible and amenable to behavioral interventions that can promote caring beyond kin and kith.

Social Cognitive and Affective Neuroscience, 2014

Previous neuroimaging studies on empathy have not clearly identified neural systems that support the three components of empathy: affective congruence, perspective-taking, and prosocial motivation. These limitations stem from a focus on a single emotion per study, minimal variation in amount of social context provided, and lack of prosocial motivation assessment. In the current investigation, 32 participants completed a functional magnetic resonance imaging session assessing empathic responses to individuals experiencing painful, anxious, and happy events that varied in valence and amount of social context provided. They also completed a 14-day experience sampling survey that assessed real-world helping behaviors. The results demonstrate that empathy for positive and negative emotions selectively activates regions associated with positive and negative affect, respectively. In addition, the mirror system was more active during empathy for context-independent events (pain), whereas the mentalizing system was more active during empathy for context-dependent events (anxiety, happiness). Finally, the septal area, previously linked to prosocial motivation, was the only region that was commonly activated across empathy for pain, anxiety, and happiness. Septal activity during each of these empathic experiences was predictive of daily helping. These findings suggest that empathy has multiple input pathways, produces affect-congruent activations, and results in septally mediated prosocial motivation.

When we attend to other people in pain, the neural circuits underpinning the processing of first-hand experience of pain are activated in the observer. This basic somatic sensorimotor resonance plays a critical role in the primitive building block of empathy and moral reasoning that relies on the sharing of others' distress. However, the full-blown capacity of human empathy is more sophisticated than the mere simulation of the target's affective state. Indeed, empathy is about both sharing and understanding the emotional state of others in relation to oneself. In this functional magnetic resonance imaging (fMRI) study, 17 typically developing children (range 7-12 yr) were scanned while presented with short animated visual stimuli depicting painful and non-painful situations. These situations involved either a person whose pain was accidentally caused or a person whose pain was intentionally inflicted by another individual. After scanning, children rated how painful these situations appeared. Consistent with previous fMRI studies of pain empathy with adults, the perception of other people in pain in children was associated with increased hemodynamic activity in the neural circuits involved in the processing of first-hand experience of pain, including the insula, somatosensory cortex, anterior midcingulate cortex, periaqueductal gray, and supplementary motor area. Interestingly, when watching another person inflicting pain onto another, regions that are consistently engaged in representing social interaction and moral behavior (the temporo-parietal junction, the paracingulate, orbital medial frontal cortices, amygdala) were additionally recruited, and increased their connectivity with the fronto-parietal attention network. These results are important to set the standard for future studies with children who exhibit social cognitive disorders (e.g., antisocial personality disorder, conduct disorder) and are often deficient in experiencing empathy or guilt.

There is strong evidence that empathy has deep evolutionary, biochemical, and neurological underpinnings. Even the most advanced forms of empathy in humans are built on more basic forms and remain connected to core mechanisms associated with affective communication, social attachment, and parental care. Social neuroscience has begun to examine the neurobiological mechanisms that instantiate empathy, especially in response to signals of distress and pain, and how certain dispositional and contextual moderators modulate its experience. Functional neuroimaging studies document a circuit that responds to the perception of others' distress. Activation of this circuit reflects an aversive response in the observer, and this information may act as a trigger to inhibit aggression or prompt motivation to help. Moreover, empathy in humans is assisted by other domain-general high-level cognitive abilities, such as executive functions, mentalizing, and language, which expand the range of behaviors that can be driven by empathy.

Despite empathy's importance for promoting social interactions, neuroimaging research has largely overlooked empathy during social experiences. Here, we examined neural activity during empathy for social exclusion and assessed how empathy-related neural processes might relate to subsequent prosocial behavior toward the excluded victim. During an fMRI scan, participants observed one person being excluded by two others, and afterwards sent emails to each of these 'people.' Later, a group of raters assessed how prosocial (e.g., helpful, comforting) the emails were. Observing exclusion (vs. inclusion) activated regions associated with mentalizing (dorsomedial prefrontal cortex, medial prefrontal cortex, precuneus), and highly empathic individuals activated both mentalizing regions and social pain-related regions (anterior insula, dorsal anterior cingulate cortex). Additionally, the empathy-related activity in the anterior insula and medial prefrontal cortex was associated with later prosocial behavior toward the victim, and exploratory mediation analyses indicated that medial prefrontal cortex activity, in particular, may support the link between trait empathy and prosocial behavior. Overall, findings suggest that empathy-related neural responses to social experiences may promote spontaneous prosocial treatment of those in need.

Annual Review of Neuroscience, 2012

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Journal of Cognitive Neuroscience, 2012

■ Empathy is a critical aspect of human emotion that influences the behavior of individuals as well as the functioning of society. Although empathy is fundamentally a subjective experience, no studies have yet examined the neural correlates of the self-reported experience of empathy. Furthermore, although behavioral research has linked empathy to prosocial behavior, no work has yet connected empathy-related neural activity to everyday, realworld helping behavior. Lastly, the widespread assumption that empathy is an automatic experience remains largely untested. It is also unknown whether differences in trait empathy reflect either variability in the automaticity of empathic responses or the capacity to feel empathy. In this study, 32 participants completed a diary study of helping behavior followed by an fMRI session, assessing empathic responses to sad images under three conditions: watching naturally, under cognitive load, and while empathizing. Across conditions, higher levels of self-reported experienced empathy were associated with greater activity in medial PFC (MPFC). Activity in MPFC was also correlated with daily helping behavior. Self-report of empathic experience and activity in empathy-related areas, notably MPFC, were higher in the empathize condition than in the load condition, suggesting that empathy is not a fully automatic experience. Additionally, high trait empathy participants displayed greater experienced empathy and stronger MPFC responses than low trait empathy individuals under cognitive load, suggesting that empathy is more automatic for individuals high in trait empathy. These results underline the critical role that MPFC plays in the instantiation of empathic experience and consequent behavior. ■