Defining Empathy
Empathy, or “feeling as another does,”
2 functionally comprises four dimensions. Empathy is (a) an affective state that is (b) isomorphic to another person’s affective state, (c) is elicited by observing or imagining another person’s affective state, and (d) is experienced while remaining cognizant that the other person’s affective state is the source of one’s own affective state.
3,4 The development of empathy is preceded by, and emerges from, more elementary functions such as brainstem-mediated mimicry, which is present at birth, and mirror-neuron–mediated emotional resonance, which emerges in the very first months of life.
5 Both of these functions induce physiological changes, such as facial grimacing or pupillary dilation, in response to the expressions, vocalizations, postures, and movements of another person.
6 During the second year of life, at the same time as frontally mediated self/other cognitive awareness begins to develop, this capacity to send and respond to limbic-modulated emotional signals evolves into more mature forms of empathy. Our capacity to distinguish whether the source of an affective experience is triggered by another or lies within ourselves is a key characteristic of empathy
7 and is part of a broader capacity for perspective taking. Although compassion (i.e., sympathy or empathic concern) also induces affective changes in the observer, empathy denotes that the observer’s emotions reflect affective sharing (“feeling as” the other person), whereas compassion denotes that the observer’s emotions are inherently other oriented (“feeling for” the other person).
8 Empathic perspective taking also partially differs from mentalizing and theory-of-mind functions, which involve taking another person's perspective and attributing to them particular cognitive states, in that it is more involved in attributing emotional states.
9The Neurobiology of Empathy
The PFC is subdivided into five frontal-subcortical regions, two of which have most consistently been implicated in violent and empathic behavior: the dorsolateral prefrontal circuit, which connects pathways that modulate executive functions, including the ability to plan, problem solve, sequence events, and adaptively change cognitive and behavioral sets; and the orbitofrontal circuit, which connects frontal monitoring pathways to the limbic system and governs appropriate responses to social cues and interpersonal sensitivity.
10 Corticolimbic networks subserving distinct social functions can be further divided into three partially dissociable networks: perceptual, subserving awareness/understanding of others’ socioemotional behavior (lateral orbitofrontal cortex [OFC], ventrolateral temporal pole, fusiform gyrus, superior temporal sulcus); reward/affiliation, subserving socioemotional responsiveness/detachment (dorsomedial temporal pole, rostral anterior cingulate cortex, subgenual anterior cingulate cortex, ventromedial PFC [vmPFC], entorhinal cortex, parahippocampal cortex, ventromedial striatum); and pain/aversion, subserving threat detection and approach-avoidance behaviors (caudal anterior cingulate cortex, insula, somatosensory operculum, ventrolateral striatum).
11 The limbic system includes the amygdala, which attributes emotional valence to memories; the hypothalamus, which receives information about the internal state of the body and orchestrates endocrine/hormonal responses through its control of the pituitary gland; and the cingulate gyrus, which is involved in autonomic regulatory functions such as heart rate and blood pressure.
1The affective and cognitive components of empathy are dissociable, as indicated by neurological
12,13 and functional
14,15 studies as well as by their different developmental trajectories.
16,17 Mature empathic sensitivity depends on the functional integration of these components, expressed via emotional regulation and attachment behaviors, which typically develop in tandem.
The affective component of empathy relies on a neural resonance system by which an observer engages motor intention,
18 sensory experience,
19 and visceral state
20 neural mechanisms, which overlap with those that the individual would engage if he or she were directly experiencing a given internal state. The cognitive component of empathy engages the ability to represent affective states outside of a perceiver's present experience to include anticipated experiences or the experiences of another (self-projection).
21,22 Brain regions most typically associated with affective empathy include the inferior parietal lobule, anterior insula, posterior superior temporal sulcus, and anterior cingulate cortex. Cognitive empathy engages a system of midline and superior temporal structures broadly involved in “self-projection” and mentalizing. These include the temporoparietal junction, temporal poles, medial PFC, posterior cingulate cortex, and precuneus.
4Although these brain regions that subserve affective and cognitive components constitute a complex distributed and recursively interconnected network, further activating autonomic and neuroendocrine processes implicated in social behaviors and emotional states,
8 recent studies have begun to detect temporal dynamics within the process of empathic experience that indicate brain activity associated with affective sharing comes online earlier than the mentalizing-related activity.
23Developmental shifts take place within this network, which allow for the transition from emotional arousal and self-distress to more mature empathic responsiveness.
24 As a child matures from 6 to 11 years old, the self/other awareness circuit becomes more selectively responsive to perspective-taking situations that require inferring the mental states of others.
25 At the same time, the development of affective processing from childhood to adulthood is accompanied by reduced activity within the brainstem and limbic affective systems and by the increased involvement of the PFC.
26 In response to others’ distress, younger children recruit the amygdala, medial OFC, and posterior portion of the insula more so than adults.
27 As children mature, the activity of the medial OFC, which is involved in regulating motor and visceral responses, decreases and the activity of the lateral OFC, which is involved in executive control of emotion reactivity, increases.
28 This pattern of developmental change is indicative of a gradual shift from the monitoring of somatovisceral responses in young children to a more cognitive, evaluative level, which is associated with executive control of emotions in adults.
29 As cortical executive functions mature through childhood and adolescence, inhibitory capacities and attentional control strengthen, allowing for more fine-tuned emotional regulation. Activation of these prefrontal functions reduces amygdala and autonomic reactivity.
30 Overall, as children mature, there is a progressive shift from more limbic to more frontal activation. Inhibitory control and emotional regulation are linked to the ventral and dorsal aspects of the PFC and to the dorsal anterior cingulate cortex, both through their reciprocal connections with limbic areas.
31 Emotional regulation is fundamental for the capacity to experience empathy rather than personal distress.
27 Well-regulated children are more prone to empathy, regardless of their emotional reactivity, because they have learned, in part through the support of their caregivers, to modulate their negative vicarious emotions to maintain an optimal level of emotional arousal. By contrast, children who are unable to regulate their emotions tend to be low in empathy and to become overwhelmed by their negative emotions when witnessing another in distress.
16Empathy evolves in the service of attachment for self-preservation. Empathy enhances survival by bonding individuals, especially mother and infant, thereby increasing defenses against predators.
32 By reducing personal distress and avoidance behaviors, secure attachment facilitates affect regulation, in turn increasing empathic behaviors.
16 Children with secure attachment are more empathic toward others, regardless of relatedness.
33 Conversely, lack of secure attachment increases avoidant behavior, emotional distress, and lack of empathy.
34 The degree of empathic responsiveness directly correlates with approach-avoidance behaviors, which directly modulate attachment. Approach-avoidance behaviors are hormonally modulated.
35 In humans, the hypothalamus-pituitary-adrenal (HPA) axis and oxytocin are particularly relevant. The HPA axis is functional at birth and matures rapidly during the early years, lessening emotional lability and increasing self-control.
36 This process is strictly linked to the presence and responsiveness of an attachment figure in the child’s life, which specifically triggers up/down HPA regulation,
37 with gender- and parental-status differences in neurohemodynamic brain responses to infants. Female, but not male, individuals exhibit regulatory changes in response to infant stimuli, with mothers showing greater modulation in response to crying and nonmothers in response to laughing.
38 The social modulation of physiological stress responses continues to influence HPA activity in adults and provides a buffer against stress.
39 The extent of this shift is also affected by individual predisposition toward autonomic arousal, emotional reactivity, and strength of executive functions. Oxytocin, which is released in the context of supportive relationships, has specific modulatory effects on the HPA axis. By downregulating the HPA axis, it induces increased tolerance to stressful stimuli by reducing pain sensitivity, fear/anxiety, and defensive avoidance, thereby enabling greater trust, attachment, and empathy.
40 Both secure attachment and higher degrees of empathic capacity hormonally activate the brain reward system, which, in turn, sustains attachment and nurturance. Because empathy and attachment are linked to the same hormonal events, they are both behaviorally and physiologically interdependent. The hormonal shifts of pregnancy predispose the brain reward system to form mother-infant bonds at birth,
41 while securely attached mother-child interactions increase the production of oxytocin, activating the brain reward regions.
42 Even when empathic behaviors are extended to nonkin, these behaviors activate the reward system, inducing feelings of well-being.
43 Thus, empathic behaviors are physiologically rewarding, if not addictive.
44Aggression, Violence, and the Lack of Empathy
Aggression is “an intentional act that inflicts bodily or mental harm on others,”
45 which is legitimate in certain contexts (e.g., self-defense) and may occur without bodily damage (e.g., verbal aggression). By contrast, violence is “an aggressive act that causes physical injury” and is the subset of aggression “characterized by the unwarranted infliction of physical harm.”
45(p. 2) This review focuses on interpersonal violence, excluding socially sanctioned types of violence (e.g., sports), warfare, totalitarian regimes, and organized crime (e.g., gangs, terrorism, and the Mafia). The literature on interpersonal violence distinguishes two main types of violence: impulsive violence (IV; “expressive,” “affective,” or “reactive”), which is characterized by rage or other intense emotions, and predatory violence (PV; “calculated/instrumental,” “callous-unemotional” [CU], or “proactive”).
46,47 Perpetrators who exhibit IV tend to target individuals with whom they have a connection: spouses, family members, coworkers, and schoolmates. Individuals who exhibit PV may target proximity victims, but they more often perpetrate PV against unknown others. We will make reference to IV only to the extent that it speaks to the understanding of PV. Although overt sexual violence is more present in IV, sexual arousal without overt sexual behavior is thought to be more present in PV, possibly as a motivating factor for the violent act. Acts without direct sexual contact may be arousing or otherwise intensely stimulating to the perpetrator. However, in the absence of scientific methods or criteria to distinguish impulsive versus predatory sexual violence, we will not consider the potential role of sexual violence in PV in this review.
PV may closely represent the inverse of empathy. Cold-blooded, purposeful PV is the hallmark of psychopathy.
48–50 Although they are not equivalent concepts, there is a substantial overlap between psychopathy and PV. Although not all psychopathic domains include opportunism and instrumentalism,
51 the literature on psychopathy consistently identifies both empathic deficits and predatory behaviors as the core signature of a psychopathic personality.
52 PV has also been found to correlate with an individual’s total score on the Hare Psychopathy Checklist–Youth Version and interpersonal features of psychopathy.
50 The psychopathic behavior of PV is found in individuals who present with a dysfunction in either experiencing or sharing feelings with others, which is associated with deficits in affective empathy.
53,54 By contrast, individuals who exhibit IV tend to display disinhibition and intense emotions and more typically retain a capacity for empathy and remorse.
55 Unfortunately, the systematic investigation of psychopathy has been pursued only very recently, notwithstanding the descriptive reports of behavioral presentations such as the numerous editions of Cleckley’s
56 Mask of Sanity.
Discussion
Review of the neurobiology of empathy has revealed that significant aspects of empathic responsiveness are present at birth and continue to mature throughout childhood and adolescence, in the context of interpersonal relationships. Maturation involves a progressive shift along the dorsolateral PFC-limbic pathway, from more activation of limbic structures early in development to more activation of frontal regions later in development. The extent of this shift is affected by individual predisposition toward autonomic arousal, emotional reactivity, and strength of executive functions.
Although the affective and cognitive components of empathy are dissociable, their interplay allows for emotional regulation. Mature empathic sensitivity depends on the functional integration of these components in the service of relationships and goal-directed social behavior. Social bonding, attachment, and empathy are interconnected at the neurobiological level by the modulatory effects of hormones, with increased oxytocin levels and increased HPA activity correlating positively with more secure attachment and an increased capacity for empathy. Secure attachment and empathic responsiveness alike stimulate the brain reward pathways, which become self-reinforcing.
Whereas IV has been more clearly linked to increased limbic activation with resulting heightened emotional arousal and diminished frontal activation with resulting disinhibition, PV presents a more complex profile. No single region, whether structurally impaired or functionally diminished, will result in psychopathy or in specific cognitive or affective aspects of psychopathy. A recent theoretical paradigm points to limbic hypoarousal, leading to shallow affect and diminished fear, paired with intact or even overactive frontal circuitry, resulting in increased cognitive rigidity, increased hyperattention to selective targets, and difficulties with attention shifting and flexible behavior, possibly leading to obsessive fixations and calculated actions. Further findings, although limited, suggest that psychopathic individuals’ reduced fear, reduced sensitivity to punishment, enhanced sensitivity to reward, and hyporesponsivity to stressors—all of which affect their decision-making behavior—may be linked to the combined effect of reduced cortisol, increased testosterone levels, and reduced HPA activity.
The frontotemporal/limbic/hormonal interplay is likely the main factor in the emergence of PV, but this explanation may still be too simplistic. Whereas impulsive perpetrators typically feel remorse or guilt, predatory perpetrators typically do not. Instead, they tend to feel most engaged and perhaps most “alive” while executing their plans or reliving their experiences through crime-scene revisitations, photos, or other types of “souvenirs” from their crimes and in ways that suggest a radical distortion of the experience of bonding. Such distortions—which, to the best of our knowledge, are poorly understood and scarcely acknowledged—may be what ultimately lead to those behavioral expressions of PV that are described as “evil.”
Such radical deficits of bonding point to a very early etiology of psychopathy and support proposed neurodevelopmental hypotheses.
46 Such hypotheses take into account the fact that psychopathic behaviors manifest early in life; continue relatively consistently during childhood, adolescence, and, overall, across time
181; and are mostly resistant to conventional treatments.
163 Significantly, people who suffer neurological damage at a very early age exhibit characteristics that most closely resemble psychopathy, suggesting that psychopathy is associated with impairments in brain functioning before moral socialization and social bonding.
127 In addition, psychosocial, demographic, and head-injury measures alone have not accounted for the structural and functional brain impairments observed in psychopathy.
46 A neurodevelopmental hypothesis must also consider the fact that male individuals are much more likely than female individuals to commit certain types of violent crimes.
182 Female individuals tend to be more empathic as a result of their evolutionary biological role in the reproduction and care of infants.
183 This is true for female children as well, who score higher than male children in empathic concern.
184 Although they are still speculative, recent observations suggest neurodevelopmental abnormalities in both juvenile and adult psychopathic offenders.
46Only very recent studies have compared predatory versus impulsive offenders, basing group classification on volumetric measures of gray matter.
172,173 These studies show that whereas impulsive offenders can be treated with existing therapies, traditional treatments for predatory offenders may be useless. The interpersonal and affective aspects of psychopathy have only very recently come to the attention of treatment theories and remain to be addressed in actual interventions.
Given that mindfulness training induces neuroplastic changes in the frontolimbic network and increases emotional regulation, attentional skills, and empathic responsiveness, it potentially represents, at least in theory, a more comprehensive and targeted approach to treating the interpersonal/affective empathic deficits in psychopathy. However, because neuroplastic and behavioral changes are a slow process, requiring years of sustained mindfulness practice, this approach is likely suitable only as a very early intervention.
Within this context, the use of prospective longitudinal studies to identify and assess children and adolescents with CU traits has important implications for the prevention and management of adult psychopathy. Increasing the specificity of target theoretical constructs may increase the replicability of findings and produce more converging results. PV and IV distinction, cognitive and affective empathy dissociation, antisocial and psychopathic personality differences should all be taken into consideration in designing future research. Studies are needed that investigate the role of hormones and neurotransmitters and their interplay with neural mechanisms, as well as the precursors, risk factors, and correlates of CU traits in early infancy and in longitudinal designs.
In terms of treatment, we recommend careful assessment of participants in order to better tailor interventions. Best results may be expected when assessments and treatments take place before the second critical period of neuronal plasticity of early adolescence
185,186 and differentially target the cognitive and affective aspects of empathic deficits in psychopathy.
Studies are needed that assess the behavioral, psychological, and neurological outcomes of mindfulness training and related types of cognitive-behavioral therapies among incarcerated youth who do or do not exhibit CU traits and/or PV. Such studies should aim to evaluate changes in neural connectivity, cognitive function, cortical thickness, affective reactivity, self-regulation, and social relationships as a result of treatment. This has the potential to uncover an important behavioral intervention, with implications for neural plasticity.
More broadly, we hope that the growing understanding of the neurobiological basis of PV and associated criminal behavior encourages a dialogue on the role of neuroscience in criminal justice, on the implications for punishment versus potential prevention and treatments, and on prediction of violence and risk assessment
187 and leads to educational outreach efforts to targeted audiences spanning legal, scientific, and policy fields.
Conclusions
The behavioral expressions of empathy in bonding, attachment, and prosocial behaviors and of deficits in empathy in PV and psychopathic behaviors share significant neural substrates. This, in turn, points to a new way of thinking about their genesis.
Empathic processing is primarily related to the homeostatic functioning of the OFC/vmPFC-limbic pathways and to the reciprocal influence of the HPA axis, oxytocin, and brain reward mechanisms. CU traits, PV, and psychopathic behaviors are tightly linked to these same structures. The functional imbalance of the OFC/vmPFC-limbic pathways leads to the cognitive and interpersonal/affective aspects of psychopathy. Diminished HPA activation and reduced cortisol levels result in increased stress tolerance and diminished fear. This may also potentially affect the ongoing capacity to form attachments and activate the brain reward system during interpersonal interactions. Thus, the inverse relationship between empathy and PV shares similar neuroanatomical substrates. A corollary of this is that strengthening empathy, which enhances bonding, might result in diminished PV.
Individuals with psychopathy are typically viewed as resistant to treatment. Significant conceptual advances have occurred in recent years, particularly regarding the relationship between PV and empathy. Our review suggests that more targeted interventions aimed at specific features of psychopathy might lead to better outcomes, with maximal effectiveness in the context of very early interventions. Continued efforts to identify, assess, and treat children and adolescents with CU traits have important implications for preventing and managing adult psychopathy. Although the specific aspects of deficiencies in empathic processing in psychopathy remain poorly understood, it is clear that an important relationship exists between empathy and PV, which may be essential in the development of treatments for this disorder.