Human empathy through the lens of social neuroscience.

“In a number of studies (see [69], for review), it has been demonstrated that the right TPJ is specifically activated when subjects focusing their attention on a certain screen location are presented with a stimulus at a nonattended location, representing a violation of their expectancy and requiring them to redirect t…”

“Various strategies have been identified to regulate emotions by means of top-down cognitive control[75].”

“Electrophysiological recordings in monkeys as well as neuroimaging experiments in humans have shown that the observation of actions performed by others activates cortical motor representations in the self (see [17] for review).”

“This system includes the insula and medial cingulate cortices[81] and codes the affective and motivational dimensions of pain.”

“Heuristically, these processes have been arranged on a continuum from attentional control to cognitive change[76].”

“Besides, empathy has evolved as an in-group phenomena[9].”

“Such a proposal is consistent with social psychology experiments showing that humans tend to nonconsciously mimic the behaviors of others[15], leading to more smooth interactions and increased liking.”

“Furthermore, recent data suggest that this region is also involved in empathy[36] and in theory of mind, i.”

“Such a simulation might both lead to the mobilization of motor areas (including the SMA) in order to prepare defensive or withdrawal behaviors, and to interoceptive monitoring associated with autonomic changes evoked by this simulation process[44].”

“• An affective response that stems from the apprehension or comprehension of another’s emotional state or condition, and which is similar to what the other person is feeling or would be expected to feel in the given situation[8]”

“Carlson and Moses[34] have convincingly documented the contribution of executive functions, especially inhibitory control, in both the emergence and expression of mental state attribution in children.”

“One fMRI experiment demonstrates that when participants are required to observe or to imitate facial expressions of various emotions, increased neurodynamic activity is detected in the superior temporal sulcus, the anterior insula, and the amygdala, as well as in areas of the premotor cortex corresponding to the repre…”

“The OFC plays an important role in the evaluation of positive and negative reinforcements[83], and is also involved in emotion reappraisal.”

“, [14]).”

“Singer and colleagues[91] engaged participants in a sequential Prisoner’s dilemma game with confederate targets, who would either play the game in a fair or unfair way.”

“For instance, one critical question debated among social psychologists is whether perspective-taking instructions induce empathic concern and/or personal distress, and to what extent prosocial motivation springs from self-other overlap (see [7,96]).”

“However, these findings are at odds with fMRI studies of empathy for pain, which did not detect any changes in the somatosensory cortex during the perception of pain in others[22,23,24].”

“Specific activation in the right inferior parietal cortex/TPJ was detected when participants mentally simulated actions from someone else’s perspective[64].”

“Interestingly, the amygdala receives nociceptive information from the spino-parabrachial pain system and the insula, and its activity appears closely tied to the context and level of aversiveness of the perceived stimuli[42].”

“It has also been demonstrated that nonconscious behavioral mimicry increases affiliation, which serves to foster relationships with others[16].”

“In another study[59], a joystick was used to drive a circle along a T-shaped path.”

“Also, the work of Downar et al.[70] suggests that the right (and left) TPJs are crucial aspects of a multimodal cortical network for the detection of changes in the sensory environment.”

“the awareness that others like the self possess mental states that can be similar or different from oneself[66,67].”

“1152 individual experiencing these situations[27].”

“Batson and colleagues[3] offered an empathy-altruism hypothesis, which claims that purely altruistic action can reliably occur provided that it is preceded by empathic concern for another.”

“Self-awareness is a necessary condition for making inference about the mental states in others[47].”

“These results reveal the similarities in neural networks representing first- and third-person information, which is consistent with the shared representations account of social interaction[38].”

“Results demonstrated a graded hemodynamic activity of the right inferior parietal lobule that parallels the degree of mismatch between the executed movements and the visual reafference[58].”

“• An affective response more appropriate to someone else’s situation than to one’s own[6]”

“Previous research has shown that emotion regulation positively relates to feelings of concern for the other person[73].”

“For instance, the right TPJ is specifically involved when participants imagine how another person would feel in everyday-life situations that elicit social emotions[37] or in painful experiences, but not when they imagine these situations for themselves[27,39].”

“There is increasingly clear evidence of a specific developmental link between theory-of-mind development and improved self-control at around the age of 4[33].”

“• An other-oriented emotional response congruent with the other's perceived welfare[7]”

“Recently, a transcranial magnetic stimulation (TMS) study reported changes in corticospinal motor representations of hand muscles in individuals observing needles penetrating hands or feet of a human model[25], indicating that the observation of pain can involve sensorimotor representations.”

“Similarly, patients with generalized social phobia, which are characterized by fear of social interactions and sensitivity to disapproval by others, show increased amygdala activation when exposed to angry or contemptuous faces[87].”

“This pattern of activation is also consistent with data collected using direct nonpainful and painful electrical stimulation of the insular cortex in neurological patients[29].”

“It has been demonstrated that individuals who can regulate their emotions are more likely to experience empathy, and also to act in morally desirable ways with others[71].”

“, delusional beliefs about the body[56]).”

“Indeed, the ability to recognize oneself as the agent of a behavior is the way one builds as an entity independent from the external world[52].”

“For instance, one fMRI study showed that observing fearful body expressions not only produces increased activity in brain areas associated with emotional processes, but also in areas linked with representation of action and movement[18].”

“Interestingly, the development of self and other mental state understanding is functionally linked to that of executive functions[31,32].”

“Similar results were also reported by Morrison and colleagues[23] who scanned participants during a condition of feeling a moderately painful pinprick stimulus to the fingertips and in another condition in which they witnessed another person’s hand undergo similar stimulation.”

“Because of these anatomical characteristics, this region is a pivotal neural locus for self-processing that is involved in multisensory body-related information processing, as well as in the processing of phenomenological and cognitive aspects of the self[55].”

“Accumulating evidence from neuroimaging studies, as well as lesion studies in neurological patients, indicates that the right inferior parietal cortex, at the junction with the posterior temporal cortex (temporoparietal junction, TPJ), plays a critical role in comparing signals arising from self-produced actions with…”

“In addition, studies on imitation have documented the involvement of right inferior parietal cortex/TPJ during reciprocal imitation in which it may be difficult to keep track of agency[62,63].”

“These results indicate that the emotion-sharing component may be subject to personal experience, and/or that emotion regulation and associated caring is prepared differently in men and women (but see also [93]).”

“These results indicate that this area is not simply involved in associating actions and their sensory consequences, but, in general, contributes to distinguishing the self from others[38,65].”

“Lanzetta and coworkers[94,95] investigated the psychophysiological, behavioral, and psychological effects of attitudes on interpersonal interaction.”

“This is demonstrated by an fMRI study showing significant interactions between gender and parental status in the neural response to infant crying and laughing[92].”

“This has been demonstrated in a positron emission tomography study in which participants were instructed to focus their attention either on the unpleasantness or the location of the noxious stimuli delivered on the participants’ hands[26], with the latter condition resulting in increased regional cerebral blood flow i…”

“A similar rostrocaudal organization is observed in the insula, in which pain-specific responses are observed in more medial-posterior parts, while observation of pain leads to increases in anterior insula[28].”

“the awareness that others like the self possess mental states that can be similar or different from oneself[66,67].”

“For instance, participants instructed to imagine being in a safe, comfortable place showed reduced behavioral and physiological markers of anxiety related to the anticipation of painful stimulation[82].”

“Another study showed that the observation of everyday hand and face actions performed with an emotion recruits regions involved in the perception and the experience of emotion and/or in communication[21].”

“In addition, studies on imitation have documented the involvement of right inferior parietal cortex/TPJ during reciprocal imitation in which it may be difficult to keep track of agency[62,63].”

“Accumulating evidence from neuroimaging studies, as well as lesion studies in neurological patients, indicates that the right inferior parietal cortex, at the junction with the posterior temporal cortex (temporoparietal junction, TPJ), plays a critical role in comparing signals arising from self-produced actions with…”

“• The ability to put oneself into the mental shoes of another person to understand his or her emotions and feelings[a form of simulation, or inner imitation][4]”

“For example, promoting knowledge about the specific needs and problems of elderly people in a game situation resulted in significant increases in empathy and caring for elderly patients[89].”

“However, despite the obvious advantages of understanding another person’s thoughts and feelings, empathy does not come without costs[85].”

“Lanzetta and coworkers[94,95] investigated the psychophysiological, behavioral, and psychological effects of attitudes on interpersonal interaction.”

“However, many models of empathy assume an important role of mimicry and emotional contagion and regard these two phenomena as interacting (see Singer and Lamm, 2009, for clarification of terms, and Decety and Lamm, 2006; Preston and de Waal, 2002).”

“Decety and Lamm (2006), for example, proposed a model in which bottom-up (i.e., direct matching between perception and action) and top-down (i.e., regulation, contextual appraisal, and control) information processes are fundamentally intertwined in the generation and modulation of empathy.”

“In particular, this distinction is what separates empathy from emotional contagion (Decety & Lamm, 2006; de Vignemont & Singer, 2006; Gerdes et al., 2010; Scheler, cited in Ickes, 2003).”

“It was thus important to demonstrate both the similarities in the neural networks underlying the sharing of pain with others and the specific mechanisms that permit distinguishing the self from others, which is critical for the experience of empathy (Decety & Hodges, 2006; Decety & Lamm, 2006; Decety, 2005).”

“Both empathy and theory of mind involve an ability to simultaneously distinguish between different possible perspectives on the same situation (Decety and Jackson 2004; Decety and Lamm 2006).”

“2009), at least two different routes to the understanding of other minds can be distinguished: our ability to understand the abstract beliefs and intentions of others, which is referred to as Theory of Mind, cognitive perspective taking or mentalizing (Premack and Woodruff, 1978; Frith and Frith, 2003) and our ability…”

“Accumulating evidence has put forward the view that there are at least two different routes to put us in the shoes (the mind) of the other person [1–6].”

“Recent data from cognitive neuroscience also offer new insights regarding the neural mechanisms and brain areas that underpin empathy (Decety & Jackson, 2004, 2006; Decety & Lamm, 2006; Leiberg & Anders, 2006).”

“The dynamics of this evoked response are consistent with the two-stage model of empathy for pain, as evidenced by clear demarcations in the time course, scalp distribution, and functional in aspects of time course, scalp distribution, and functional significance (Decety, 2007; Decety and Lamm, 2006; Decety and Meyer,…”

“Theoretically and conceptually, empathy has seen much attention in the philosophical, psychological, and more recently, cognitive neuroscience literature, with varying definitions and conceptualizations (Decety & Lamm, 2006).”

“However, subcortical systems do not lose their basic function, they may give up some of their autonomy in terms of the degree to which higher cortical systems can modulate their functions or regulate the emotional experience (adapted from [168–170]).”

“How we might do so requires consideration of the cognitive components of empathy, which may be said to be unique to humans and other primates (Decety & Lamm 2006, de Waal 2008).”

“We further predicted an enhanced self-other distinction in the expert group, represented neurally as additional activation of the right temporoparietal junction, an area known to play a crucial role in self-other distinction processes and theory of mind [2, 4].”

“aspects of empathy (Decety and Lamm 2006).”

“, 2016) and share emotions is automatic mimicry (Decety and Lamm, 2006; Schuler et al., 2016; Singer and Lamm, 2009).”

“…emotional and sensory experience of other individuals. n addition, appropriate social communications and behaviours eed vicarious experiencing of emotions congruent with those of thers while being aware of the distinction between the self and thers (Decety & Jackson, 2004; Decety & Lamm, 2006).”

“, [12,13,45]) emphasize the contribution of both automatic and controlled processes to the conscious experience of empathy.”

“Nevertheless, this result is consistent with developmental and neurological research findings that have suggested individuals must reach a certain level of neurological maturity before they can adequately understand and display empathy (Choudhury et al., 2006; Decety & Lamm, 2006).”

“It has previously been argued that forming such a cognitive representation is likely to serve to reduce empathic personal distress (Decety and Lamm, 2006), and therefore one might predict that not only would self-reported personal distress scores be higher than in typical controls, but also that…”

“…as a process of knowing is influenced by prior experiential knowledge of factors shaping the observation condition, previous interaction(s) with the target, and/ or exposure to texts, worlds, or spaces that in some way shape how the target is experiencing a circumstance (Decety & Lamm, 2006).”

“Emotional disconnection is considered to be a top-down process that has a regulatory function, in particular in terms of the inhibitory control exercised by the prefrontal and the cingulate cortex (Decety & Lamm, 2006; Singer & Lamm, 2009).”

“With respect to cognitive empathy, various functional neuroimaging studies have shown involvement of frontal brain areas in perspective taking, ToM, and empathic accuracy (Decety and Lamm, 2006; Frith and Frith, 2006; Gallese et al., 2004; Singer, 2006; Zaki et al., 2009).”

“As a two-component model distinguishing cognitive and affective aspects of empathy is proposed in the literature (e.g., Decety & Lamm, 2006), we ran a two-factor model in which fantasy items and perspective-taking items were assumed to measure the cognitive empathy factor, and personal distress…”

“, 2003) support the notion of a central involvement of anterior insular cortex in empathy (for overviews, see de Vignemont and Singer, 2006; Decety and Lamm, 2006; Gallese et al., 2004).”

“empathy, cultural differences, prosocial behavior, collectivism, personality, emotion Empathy is defined as the tendency to be psychologically in tune with others’ feelings and perspectives (Decety & Lamm, 2006).”

“Sharing the patient’s emotions (sympathy) can lead to empathic overarousal or personal distress (an aversive self-focused emotional reaction to the apprehension of another person’s emotional state) [22].”

“…model of empathy that involves a complex interaction between bottom–up (i.e., direct matching between perception and action) and top–down (i.e., regulation and control) information processes (Lamm, Porges, Cacioppo, & Decety, 2008; Decety & Lamm, 2006; Goubert et al., 2005; Decety & Jackson, 2004).”

“Here, we consider empathy as a construct accounting for a sense of similarity in feelings experienced by the self and the other, without confusion between the two individuals (Decety & Jackson, 2004; Decety & Lamm, 2006).”

“Empathy, the ability to experience and understand what other people feel without confusion between self and others, plays a fundamental role in social interaction and moral development (Decety and Jackson, 2004; Decety and Lamm, 2006; Decety and Moriguchi, 2007; Hodges and Wegner, 1997).”

“…links in our brains enable us to understand other peoples motor action has been expanded to include the ability to share not only motor actions but also feelings and sensations with others (Preston & de Waal 2002; Gallese 2003; Decety & Jackson 2004; Decety & Lamm 2006; de Vignemont & Singer 2006).”

“Theoretical conceptualizations of empathy (Decety & Jackson, 2004; Decety & Lamm, 2006; de Vignemont & Singer, 2006; Gallese, 2003; Preston & de Waal, 2002) suggest that we understand other people’s affective states via activation of neural networks usually involved in processing our own affective states.”

“…neuroscientists have argued for a definition that requires at least a partial, isomorphic sharing of the feeling(s) of another person to be classified as empathy (e.g. Bernhardt and Singer, 2012; Decety and Lamm, 2006; Decety et al., 2012; Gonzalez-Liencres et al., 2013; Singer and Lamm, 2009).”

“The brain can distinguish at the cortical level whether the self or another individual is experiencing an emotion or pain or peripheral arousal; yet, at some core level, it is difficult to distinguish personal from socially relevant cues (Decety & Lamm, 2006).”

“Based on a model of empathy for pain consisting of early emotional sharing and late cognitive evaluation (Decety and Lamm, 2006; De Vignemont and Singer, 2006; Fan and Han, in press; Preston and de Waal, 2002), the ERP results reported in this paper indicate that the early neural activity…”

“Without self-regulation, information processing would lose flexibility and would become primarily bound to external stimulations” (Decety & Lamm, 2006, p. 1160).”

“appraisal, and mechanisms of control (Decety and Sommerville, 2003; Decety and Jackson, 2004; Decety and Lamm, 2006).”

“…since there is strong empirical evidence that individuals tend to be empathic toward others’ pain, suffering, and distress (Decety & Jackson, 2006; Decety & Lamm, 2006; Preston & de Waal, 2002); (2) the perceived verisimilitude of the message, since it is a precedent of state empathy (Campbell…”

“A growing body of empirical neuroscientific evidence suggests that perception and/or empathy for pain is not an all-or-none phenomenon but it is strongly influenced by interpersonal, intrapersonal and situational factors (Decety and Jackson, 2004; Decety and Lamm, 2006).”

“The evaluation of another person's emotion can be achieved in more than one way, i.e. via autonomic perception ( " emotional empathy " ), and/or intellectual reasoning of the other's mental state ( " cognitive empathy " ; Decety & Lamm, 2006; Preston & de Waal, 2002; Davis, 1983).”

“On the contrary, they are sophisticated cognitive skills and as such can be learned, increased, perhaps even “mastered” (Decety & Lamm, 2006).”

“While this conclusion may seem trivial, it actually brakes new grounds in the context of empathy research: most current models of empathy for pain or distress in human neuroscience used prerecorded stimuli [2,4,9,10,11,72,73,74] or used live interactions but prevented participants from viewing the reactions of their p…”

“, the affective link between the empath and the person in pain) processes shape the cognitive, affective and behavioral responses accompanying this phenomenon (Goubert et al., 2005; Decety and Lamm, 2006).”

“The observing person catches and shares the pleasant affect, while still knowing that the original source of the affect lies in the other person and not within the self (Decety & Jackson, 2004; Decety & Lamm, 2006), that is, positive empathy is triggered (Sallquist et al., 2009).”

“For instance, empathy does not only require individuals to share others’ emotional state but also to control these emotions to provide a complementary empathic response (Bird & Viding, 2014; Decety & Lamm, 2006).”

“Such processes are characteristic of nonconscious mimicry of facial expressions, posture, gestures, and mannerisms observed in self and others when we interact with them.”

“For example, the anterior insula appears to activate more so with vicarious experiences of pain (Jackson et al., 2006), while for first-hand experiences of pain the posterior insula is implemented (Decety & Lamm, 2006).”

“Decety and colleagues (Decety & Jackson, 2004; Decety & Lamm, 2006; Decety & Moriguchi, 2007) combined cumulative, qualitative descriptions of empathy from the social sciences with the new findings in social cognitive neuroscience, which led to a conceptualization of empathy as the dynamic…”

“…in its “functional architecture” which encompasses several major components – affect sharing, self-other awareness, regulatory processes, and mental flexibility to adopt the subjective perspective of another, with constant interplay between these mechanisms (Decety & Lamm, 2006; Decety, 2007).”

“…states; second, cognitive empathy requires more conscious deliberation, enables understanding of people's emotions and putting these into perspective, and may support strategic social interactions and communication (Decety & Jackson, 2004; Decety & Lamm, 2006; Hakansson & Montgomery, 2003).”

“…suggest that the flow of information from the shared representational system is not unidimensional, but rather that the aFMC may control shared representations, by enhancing or inhibiting the automatically evoked activations of this system [see also Decety and Lamm, 2006; Olsson and Ochsner, 2008].”

“According to their definition, affective representations in the brain are automatically activated by perceptual input, whereas cognitive control is mediated by cortical structures, mainly the prefrontal cortex (Decety and Lamm, 2006).”

“These findings support the two-level (early bottom-up and late top-down processing) theory of Decety and Lamm (2006)3.”

“Empathy is generally considered to be the ability to experience and understand what others feel [10].”

“This sharing stems from the perception–action coupling (supported by the MNS), which automatically induces the observer to resonate with the emotional state of another individual, with the observer emulating the motor representations and associated automatic and somatic responses that stem from the observed target [22…”

“In any case, it is clear that observing—or even merely anticipating—someone else in pain elicits an empathic response (Decety and Lamm, 2006; Bernhardt and Singer, 2012; Lamm et al., 2017).”

“These results were consistent across three independent analyses aimed at testing the same hypothesis and shed new light on the existence and nature of shared neural representations of affective states (Decety and Lamm, 2006; Singer and Lamm, 2009).”

“The present study supports theoretical concepts defining empathy as a complex interplay of bottom-up and top-down processes (e.g., Decety and Lamm, 2006; Goubert et al., 2005).”

“Obviously, this is a complex social phenomenon that, until recently, has received much attention from philosophers and psychologists rather than neuroscientists (Decety and Lamm 2006).”

“…one contrasts internally represented imitated states with the perceived emotional state of another while keeping a separation of the self from the other person; this allows for an overall assessment of imitated and perceived emotional states (Decety and Lamm, 2006; Preston and de Waal, 2002).”

“Decety and Lamm (2006) pointed out that distractive strategies may be important for humans if the cost of empathizing is excessive.”

“For example, Decety and Lamm (2006) proposed that empathy involves both emotion sharing (bottom-up information processing) and executive control, which modulates the shared affective experience (top-down information processing).”

“Most recently, the insula has also been associated with different aspects of the self [5,6,16], reward [14,15] and empathy [66].”

“Decety and Lamm (2006) claim that altruistic empathy is a striking quality that runs contrary to the Darwinian tradition of natural selection, and is evident in life beyond humanity.”

“…recognition (perception) and affective empathy (feeling and action) is also supported by both psychophysiological and cognitive neuroscience research, which has suggested that the link stems from an automatic perception–action mechanism leading to emotional contagion (Decety and Lamm, 2006).”

“Although several of the advice PE (e2) activations reported in this paper have previously been associated with ‘theory of mind’ processes (Decety and Lamm, 2006; Lamm et al., 2009; Carrington and Bailey, 2009; Chang et al., 2011; Frith and Frith, 2012), these activations may not be specific to social learning tasks.”

“…M anuscript A uthor M anuscript Empathy, the ability to understand and experience what others feel without confusion between oneself and others (Decety & Lamm, 2006), is a multidimensional construct encompassing (1) a cognitive component, the ability to understand another’s perspective and…”

“Without self–other distinction and the regulation of emotions, an affective response to another person’s emotional state could be aversive causing distress or excessive emotional stimulation in the observer: this is particularly important in the context of modern life where we may experience the emotional states of ot…”

“This is likely related to the mirror neuron system (Gallese, 2004; Rizzolatti, 2005, Singer & Lamm) and occurs in a bottom-up, automatic way (Decety & Lamm, 2006; Singer & Lamm).”

“…suggest dissociable roles of dorsal anterior cingulate and anterior insula in empathic processing, though this has not yet been demonstrated (only anterior–posterior distinctions within each region representing observed and experienced pain, respectively; see Decety and Lamm, 2006, for a review).”