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Mammalian empathy: behavioural

manifestations and neural basis
Frans B. M. de Waal1* and Stephanie D. Preston2*
Abstract | Recent research on empathy in humans and other mammals seeks to dissociate
emotional and cognitive empathy. These forms, however, remain interconnected in evolution,
across species and at the level of neural mechanisms. New data have facilitated the development
of empathy models such as the perception–action model (PAM) and mirror-neuron theories.
According to the PAM, the emotional states of others are understood through personal,
embodied representations that allow empathy and accuracy to increase based on the observer’s
past experiences. In this Review, we discuss the latest evidence from studies carried out across
a wide range of species, including studies on yawn contagion, consolation, aid-giving and
contagious physiological affect, and we summarize neuroscientific data on representations
related to another’s state.

Empathy In lay parlance as well as the scientific literature, the term This umbrella term includes obvious instances of
Any process that emerges empathy refers to both the sharing of emotions between affective resonance, such as when an observer feels con-
from the fact that observers individuals and the adopting of another’s point of view. tagiously distressed by the target’s distress or mimics their
understand others’ states by This capacity allows individuals to quickly relate to emotions. However, such outward signs are not required,
activating personal, neural and
mental representations of that
another’s state, which is essential in species that provide as shared neural representations do not need to produce
state, including the capacity to extensive parental care and work cooperatively towards downstream bodily responses7. This phenomenon exists
be affected by and share the common goals1. A mentalistic definition of empathy, for all states, but we focus on distress because of the pre-
emotional state of another; closer to theory-of-mind, is also common, and describes ponderance of relevant data and the clear application to
assess the reasons for the
how empathy allows one to access another’s mind by helping behaviour. Empathic accuracy exists on a con-
other’s state; and identify
with the other, adopting his simulating how one would feel in his or her shoes2. For tinuum that is dependent upon the observer’s attention,
or her perspective. example, Baron-Cohen3 describes empathy as a “leap of motivation to understand and relevant personal past expe-
imagination into someone else’s headspace”. Definitions riences. Empathy can but does not always lead to helping.
that favour cognition over emotion, however, exclude Conversely, helping can emerge from many routes aside
young children and most non-human species, which, from empathy and shared affect. As higher-level processes
nonetheless, are affected by the emotional states of such as simulation, theory-of-mind and cognitive empathy
others, and provide striking care and aid as a result. require observers to activate their own representations of
The notion that empathy is an affective fusion the target’s state from the top down, they are included
1
Psychology Department and
Living Links, Yerkes National with another individual’s state, rather than a cognitive under the umbrella term empathy, even if they require
Primate Research Center, deduction, had already been proposed in early 20th additional cognitive and executive processes.
Emory University, century philosophy 4. Lipps5, who gave us the concept of Arranging related yet distinguishable phenomena
36 Eagle Row, Atlanta, Einfühlung (German for ‘feeling into’), emphasized the into a single concept reflects the evolutionary view
Georgia 30322, USA.
2
Department of Psychology,
almost involuntary nature of this response, which he according to which complex organs and capacities arise
University of Michigan, regarded as possible without extensive learning, asso- incrementally. They evolve in layers, with each new layer
530 Church Street, ciation or reasoning. It took a century, however, for the being built on top of and dependent on older ones with-
Ann Arbor, Michigan 48109, quick spontaneous nature of human affective empathy out ever replacing them, as in the so-called Russian-doll
USA.
to be confirmed by empirical research. In this Review, model (FIG. 1). There exists a tendency to treat each aspect
*Both authors contributed
equally to this work. we propose a definition that balances the emotional separately and dwell on the distinctions, but in doing
Correspondence to
and cognitive sides, and use empathy as an ‘umbrella’ so we lose sight of the functionally integrated whole.
F.B.M.d.W. term for all processes that emerge from the fact that Accordingly, empathy is defined here as emotional and
dewaal@emory.edu observers understand others’ states by activating their mental sensitivity to another’s state, from being affected
doi:10.1038/nrn.2017.72 own personal, neural and mental representations of by and sharing in this state to assessing the reasons for it
Published online 29 Jun 2017 that state1,6. and adopting the other’s point of view.

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other requires and hand it to them15. Similarly, capuchin

monkeys vary their food-sharing with what they know
Perspective- about their partner’s previous food consumption16. There
taking and is no a priori reason to exclude perspective-taking in
targeted helping smaller-brained species, and studies on rodent aid-giving
are indeed suggestive of related capacities (see below).
The shared vocabulary adopted here for expressions of
empathy in both humans and other animals reflects the
Darwinian assumption that if related species show sim-
Theory-of-mind
The ability to attribute mental ilar responses under similar circumstances, the underly-
states to others, such as ing proximate processes are probably homologous (that is,
Empathic
knowledge, intentions
concern and derived from a common ancestor) rather than analogous
and beliefs. consolation (that is, independently evolved).
Affective empathy
The first review of this framework was presented in
Also known as emotional 2002 (REF. 1) and was based on evidence available at the
empathy. Empathy that is time that came from across different species and levels
directly affected by the of analysis. According to the perception–action model
emotional state of another by
(PAM), individuals understand and have a sense of oth-
matching or ‘feeling with’ it, as
a result of perceiving this state. Perception–action Motor mimicry ers’ emotions because the nervous system evolved to map
mechanism and emotional others’ states onto their own individual representations
Cognitive empathy contagion for experiencing those states1. As such, when an observer
Empathy derived from attends to another’s state, he or she spontaneously
a top-down process in which
the observer imagines how the
accesses information about the other (the ‘target’), their
target feels, even if the target is feelings, the situation and other related concepts through
not present or their feelings a distributed associative process. The fact that observers
cannot be directly observed. understand others using their own individual representa-
Figure 1 | The Russian-doll Nature
model ofReviews | Neuroscience
the evolution of tions, which are developed through experience, explains
Empathic perspective-taking empathy. Various components of the empathic response,
The capacity to take another’s why empathy and accuracy increase with familiarity and
which have been added layer upon layer during evolution, similarity with the other and their situation. Extensive
affective perspective: for
remain functionally integrated. At its core is the
example, understanding their
perception–action mechanism, which induces a similar
empirical support for the PAM has accumulated since it
specific situation and needs, was first presented, and thus an update is warranted. In
separate from one’s own, emotional state in the observer as in the target. Its most
which still requires access to basic expressions are motor mimicry and emotional fact, so much research has been performed since 2002
personal representations of contagion. The doll’s outer layers, such as empathic that we cannot comprehensively review it here. We focus
the other’s state. concern and perspective-taking, build upon this core on summarizing the most robust and central findings
socio-affective basis while increasingly requiring emotion and debates, and often cite review articles to avoid selec-
False-belief task regulation, self–other distinction and cognition. Even tive citation. We place empathy within the Tinbergian
A crucial theory-of-mind task though the doll’s outer layers depend on prefrontal
that determines whether an framework according to which every behavioural phe-
functioning, they remain fundamentally linked to the core
observer knows what another nomenon can be investigated from different yet comple-
perception–action mechanism. Adapted with permission
knows, even if this knowledge
from: de Waal, F. B. M. in Feelings & Emotions: The mentary angles, such as ‘why’ these mechanisms were
is incongruent with the selected during evolution, and ‘how’ behavioural and
observer’s own.
Amsterdam Symposium (eds Manstead T., Frijda, N. &
Fischer A.) 379–399 (Cambridge Univ. Press, 2003). neural mechanisms regulate their expression17,18.
Targeted helping The existence of empathy outside of our own species
Assistance and care based on is hardly a novel idea. Even while avoiding the term itself,
a cognitive appreciation of the Thus defined, empathy is common in our species, early studies on altruistic behaviour often employed par-
other’s specific need or
starts early in life8, and shows neural and physiological adigms suggesting that the emotional contagion of pain or
circumstances.
correlates as well as inheritability 9. Whereas emotional distress is a motivating factor. Altruism is defined as an
Tinbergian framework responses to the emotions of others are commonplace act that benefits another individual at a cost to the self.
A series of ‘why’ questions that in many species10,11, the best evidence for empathic Having trained rats to obtain food by pressing a lever,
we may ask about any perspective-taking, which we have distinguished as cogni- Church19 found that if the same action delivers an elec-
observed behaviour, as
proposed by Niko Tinbergen.
tive empathy 12, comes from intensely social animals that tric shock to a visible second rat, the first rat will tem-
The questions concern have a high degree of encephalization, such as humans, porarily cease lever-pressing, thus foregoing its rewards.
different levels of causation: apes, elephants and dolphins. Some species show signs of Entitled “Emotional reactions of rats to the pain of oth-
for example, why did a theory-of-mind in a false-belief task13, while others per- ers”, Church’s 1959 paper inspired a flurry of research,
behaviour evolve (what are its
form targeted helping that demonstrates an appreciation which initially assumed a conditioning explanation.
benefits), why does the
behaviour occur (what caused of another’s specific predicament. For example, dolphins Later, it turned out that such behaviour did not require
it) and what is the behaviour’s may lift an incapacitated companion to the surface so prior experience with the protocol. For example, Rice and
phylogenetic origin? that they can breathe and chimpanzees may bring down Gainer 20 found that rats spontaneously help distressed
fruits from a tree to an elderly female who has lost her companions that have been hoisted off of the cage floor
Emotional contagion
Emotional state matching
climbing abilities14. Chimpanzees seem to understand the by lowering them back down. Monkeys tested in the
between a target and an needs and desires of others because after having judged same era showed even more dramatic responses, such
observer. another’s situation they will find the specific tool that the as macaques refusing to pull a chain that delivers food

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Consolation behaviour to themselves if doing so also shocks a visible conspe- the aversion was stronger to the former. None of these
Reassurance behaviour cific21. Subjects sometimes went more than a week with early results supported explanations based on learning
directed at a distressed party, only minimal food to avoid shocking another monkey, and conditioning, even though these processes do have a
such as a victim of aggression and this effect was augmented by prior shock experience role in empathy and altruism. The assumption of a basic
(also see the definition of
‘empathic concern’).
but did not require it 22. Such sacrifices relate to the tight empathy mechanism is in fact more parsimonious than is
social linkage among macaques and the fact that these any learning-based explanation, which would need to be
Empathic concern responses were more pronounced between familiar than rather demanding in its range of proposed contingencies.
Also known as sympathetic unfamiliar individuals22. With regards to our closest relatives, the apes, observa-
concern. Concern about
Early research stressed the untrained, spontaneous tions of empathic responses go back to early last century.
another’s state, and attempts
to ameliorate this state (also
nature of helping and its social bias in order to counter Yerkes24 reported “sympathetic behaviour” by a bon-
see the definition of explanations that were based on conditioning and associ- obo towards a sickly companion, and Ladygina-Kohts25
‘consolation behaviour’). ative learning. If the avoidance of aversive stimuli (such as described similar tendencies for her juvenile chimpanzee.
distress vocalizations) or the seeking of extrinsic rewards By the 1970s, these responses were defined as consolation
was the sole reason for altruistic behaviour, there would behaviour and were systematically documented in natural-
be no reason for a familiarity bias and effects should be istic settings26. The way in which apes comfort others in
similar between strangers, yet with few exceptions famil- distress (for example, embracing, touching and kissing)
iarity promotes altruism. In addition, when Miller et al.23 (FIG. 2) is morphologically similar to how young children
compared macaque responses to images of fearful con- express so-called empathic concern for family members
specifics versus negatively conditioned non-social stimuli, who have been instructed to feign pain or discomfort8,27.

Behaviour Definition Mechanisms Non-human species

a Mirroring Rapid face matching Motor mimicry • Chimpanzees
and movement mapping • Orangutans
• Gelada baboons
• Macaques

b Yawn contagion Yawning in response to Motor mimicry • Chimpanzees

another’s yawns • Macaques
• Canines
• Budgerigars

c State matching Sharing the emotional state Emotional contagion • Mice

of another • Voles
• Chickens

d Consolation Comforting a distressed party Empathic concern that is based • Chimpanzees

on emotional contagion and • Bonobos
requires self-regulation • Macaques
• Canines
• Elephants
• Voles
• Mice
• Rooks
e Learned helping Liberating another or relieving Aiding that is motivated by • Macaques
its pain emotional contagion, and requires • Rats
self-regulation and trial-and-
error learning

f Targeted helping Help adapted to the specific Aiding that is motivated by • Apes
need or situation of another emotional contagion, and requires • Capuchin monkeys
self-regulation and • Dolphins
perspective-taking • Elephants

Figure 2 | Behavioural manifestations of animal empathy. The table ates atchi each othe s ph siolo ical st ess le el pa t c a e ile
summarizes behavioural patterns that are considered to be expressions bonobo wrapping her arms around another who has just lost a fight to
of empathy in non-human vertebrates, ranging from motor mirroring p o ide co solatio pa t d a at that has lea ed to li e ate a othe at
and yawn contagion to targeted helping. Most of these behaviours have that was trapped in a container (part e); and an adult chimpanzee
been characterized by experimental research, whereas others have been showing targeted helping by assisting a juvenile’s descent from a tree
documented observationally (see the references cited in the main text). pa t f). The images in parts a–f a e co tes o ie a cesco e a i
The mechanisms and the non-human species in which these behaviours i e sit o a a tal e esa o e o i e sit o i col
have been observed are shown. From top to bottom, the images show the ac oh so eo ia stit te o ech olo a a la
ollo i t o elada a oo e iles ith pla aces that is the a e ha i e sit a d al e i a tal i e sit o ali o ia
sho i apid acial i ic pa t a a a i ol pa t b p ai ie ole e ele

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Even infants younger than 1 year old exhibit significant Emotional contagion. Following the tradition of Church
attention and concern for a peer in distress28,29, which con- and Miller from the mid-20th century, researchers have
trasts with long-held stereotypes that human infants do recently confirmed the existence of contagious affect in
little more than cry contagiously when others cry. rodents. For example, the pain of one rodent may increase
the pain response of an observing conspecific, and this
Behavioural manifestations effect is highly influenced by familiarity with the suffering
Behavioural studies of empathy in mammals and other target47,48. Moreover, this effect is blocked by the presence
animals follow one of three approaches. The first focuses of strangers, who induce a glucocorticoid stress response
on motor mimicry, which is one of many behaviours that suppresses the natural motivating contagion of dis-
that reveal an underlying perception–action mechanism tress in rodents and humans49. Contagious emotional
(as described in the PAM). The second approach meas- responses are at least partially conveyed by the transfer of
ures resonating physiological and behavioural responses negative physiological states between the target and the
to the emotions of others, such as pain contagion. The observer. For example, both prairie voles50 and humans51
third is to focus on altruistic behaviour, such as con- match the hormonal stress response of a stressed target. In
solation behaviour and the helping of others in need, humans, this effect correlates with self-reported empathic
which are often motivated by shared affect between concern and perspective-taking in daily life51.
an observer and a target along with an evaluation of Contagious anxiety in observers probably follows an
the target’s situation. All three areas have seen recent inverted-U-shaped function, with moderate activation
progress, as summarized in FIG. 2. facilitating a response but high activation inhibiting it 52.
Emotion self-regulation may be key to keeping the activa-
Motor mirroring. Motor mimicry is a natural consequence tion at a moderate level. Thus, a bonobo’s ability to over-
of a neural system that maps another individual’s bodily come its own distress correlates with the frequency with
and facial expressions onto the observer’s own representa- which it offers consolation to others who are in distress53.
tions for action. This perception–action mechanism As emotion self-regulation is compromised in bono-
permits the adaptive synchronization of states between bos that are orphaned early in life53 — as also reported
targets and observers, such as in the rapid facial mimicry for human orphans54 — fully developed empathy may
described in humans30 and other primates31,32. Supporting require an affectionate upbringing.
a possible causal link with empathy, humans who report
being more emotionally empathic in daily life are the most Altruistic helping. It has been claimed that humans are
accurate mimics of others’ facial expressions33. A typical the only truly altruistic species, and that other animals
example of motor mimicry is yawn contagion, which can are self-interested and only care about return benefits
be studied with experimental protocols in which subjects (for examples, see REFS 55,56). This view erroneously
watch videos of yawning conspecifics or through natural- conflates evolution and motivation. Although the evo-
istic observations of the spreading of yawns across a group. lution of altruism is indeed explained by kin selection
Yawn contagion has been found in species as diverse as and reciprocal altruism — both of which emphasize the
humans, non-human primates, canines and birds34–37. As eventual return benefits from helping — this explana-
with empathy more broadly, yawn contagion is biased tion does not consider the role of motivation. Animals
towards socially close others, which cannot be explained do not know about genetic benefits such as inclusive
by attention as controlled studies report either similar or fitness. There is also not much evidence indicating that
greater attention to unfamiliar yawn stimuli34,38. they anticipate future return favours from their acts,
Even though monkeys are sometimes said to lack as in reciprocal altruism. One cannot be motivated by
true imitation39, they do mimic human facial and hand what one does not know. There is no conflict, therefore,
gestures40, and they socially prefer partners who mimic between the assumption that altruistic behaviour evolved
them41. In the wild, monkeys copy one another’s feeding for self-serving reasons and the suggestion that it reflects
techniques, resulting in ‘cultural’ behavioural variation42. a spontaneous motivational impulse that originates — at
In the laboratory, monkeys replicate the motor actions of least in humans and other mammals — from empathy
a group member in, for example, the way in which they with the recipient’s need, pain or distress6. Tinbergen18
open a box 43. Anthropoid apes show additional capaci- encouraged researchers to separate why a behaviour
ties in that they imitate with an understanding of cause evolved (the ultimate reason for its existence) from how
Perception–action
mechanism
and effect44. However, even in apes, motor mimicry and it is instantiated in the individual (its proximate causa-
Spontaneous activation of an shared representations probably provide the foundation tion). Theories regarding these issues are different yet
individual’s own personal for such behaviour: for example, when an observing ape compatible as they occupy separate levels of analysis.
representations for a target, spontaneously synchronizes his movements with those of The view that humans are uniquely altruistic is also
their state and their situation
a conspecific model demonstrating tool use45. Studies inconsistent with the increasing amount of evidence
when perceiving the target’s
state. of ape imitation indicate that it is not merely about indicating that even rodents are affected by the pain
emulating a beneficial outcome because ‘ghost’ demon- of familiar conspecifics and offer help. For example,
Emotion self-regulation strations of the correct outcome without an actual con- monogamous voles show a contagious stress response
Control over one’s own specific demonstrating the required actions are ignored. to familiar partners, and this is mediated by stress
emotions to promote adaptive
responding, including response
For imitation to occur, apes need to see a conspecific per- and anxiety induced in the observer; they also groom
delay, recovery from upsets form the action sequence46, which suggests the crucial stressed partners, and this seems to have a calming effect
and selective attention. role of bodily identification and motor mimicry. as it reduces anxiety-related behaviour 50. Rats learn by

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trial-and-error how to free a trapped conspecific by since it has the property of transforming another per-
opening a door 57,58, and this is again mediated by shared son’s misfortune into one’s own feeling of distress”. This
anxiety but impeded by excessive stress in the observer 57. is the beauty of the empathy mechanism and makes its
The transfer of negative affect from a target to an operation similar to most activities that are required
observer is also thought to motivate another important for mammalian survival (for example, eating, breeding
prosocial behaviour in primates: consolation. Defined as and nursing), which are all inherently rewarding. If the
comforting body contact aimed at distressed others, con- same intrinsic rewards apply to helping behaviour, this
solation was first described in the great apes26,53,59,60, but has is no reason to denigrate the response or to refuse to call
since also been found in some macaque species61, canines62, it ‘altruistic’. Evolutionary biology already assumes that
elephants63, rodents50 and corvids64. In primates, responses altruistic tendencies yield long-term net benefits.
such as placing an arm around another or grooming a Altruistic behaviour is far from limited to mammals,
victim of aggression have been shown to reduce behav- yet it remains unclear whether the same mechanism
ioural indicators of anxiety, such as self-scratching and underlies helping in non-mammals. This is quite pos-
self-grooming 60,65, while also reducing heart rate66. sible in other vertebrates (see below), but it is less likely
In line with the PAM1, these studies support the crucial that homologous, neural perception–action mechanisms
role of caught distress and arousal in prosocial behaviour, underpin the well-documented altruism of invertebrates
which nonetheless must be kept within limits to facilitate such as social insects. Through convergent evolution,
a prosocial response. The same mechanism probably genetically distant species often arrive at functionally
underlies rescue attempts by rodents, dogs, elephants, pri- similar, analogous behaviours while using different
mates and humans, given that all of these species possess mechanisms. However, even if the sophisticated rescue
mammalian brains that have highly conserved character- of trapped conspecifics by ants is not based on emo-
istics. Although many acts that are defined by biologists as tional or cognitive empathy 75,76, it has been suggested
altruistic (for example, alarm calls and defence of the hive) that contagious ant alarm and digging is induced in
do not require emotional empathy, there is a category of nearby conspecifics by the release of a volatile chemical
directed altruism in mammals that does seem to depend on from the mandible of a trapped ant 77. If true, the mech-
an affective sensitivity to another’s state and situation6,14. anism in ants may not be as different from the PAM as
There is little support for the main alternative hypoth- one might think, as their helping response is still trig-
esis, which is that helping behaviour is driven by tangible gered by the transfer of a physiological state from target
rewards. For example, rats prefer to release a trapped cage to observer, and thus represents a pheromonal analogy
mate over accessing attractive food for themselves57,58,67. to the perception–action mechanism of mammals.
They share any available rewards after the rescue and per-
form helping responses even if a subsequent reunion with The evolution of empathy. Offspring care most likely
the target (which could be rewarding) is blocked57. Both strengthened the evolution of empathy because of the
human children and chimpanzees spontaneously assist selection pressure to develop a rapid, motivating emo-
a human experimenter, but children given an extrinsic tional connection between helpless neonates and their
reward for helping actually help less than do those who caregivers8,12,78. Signalling their state through smiling and
are merely praised or not rewarded at all68,69. Thus, aid can
be given in direct response to another’s need or distress in
a manner that is independent of extrinsic rewards.
Taken together, altruistic and consoling responses Target 1 Observer
Emotion
seem to arise from the transfer of emotion from the tar- transfer
get to the observer, which in turn motivates the observer Shared
Distress
a ect
to approach and console the target, thus reducing the 2
Consolation Self-regulation
negative state of both parties (FIG. 3). The central role of and/or aid
affect transfer in helping behaviour was demonstrated
in rats in the above helping paradigm, in an experiment 3
that showed that the administration of the anxiolytic Emotion
transfer
midazolam reduced rats’ helping responses without 4
ed ced
impairing the instrumental act required to obtain food67. Relief Self-reward
distress
Affect transfer provides a built-in reward to helping
because it gives the observer a stake in another’s well- Figure 3 | From affect transfer to altruism. As shown in
Nature Reviews | Neuroscience
Directed altruism being, producing both shared pain and vicarious relief multiple animal studies, empathy may promote aid-giving
Helping or comforting or joy when the pain is ameliorated; this is accompanied behaviour between conspecifics6,57,58. First, the target’s
behaviour directed at an
by the “warm glow” that humans feel after doing a good distress induces stress or distress in the observer through
individual in need, pain or e otio al t a s e step he o se e eeds to
distress. deed70 or the vicarious rewards that monkeys seem to
downregulate its own distress in order to effectively attend
gain from prosocial behaviour 6,71,72.
to the target, such as through helping or consolation
Convergent evolution Blurring the line between the self and the other at step he es lti ed ctio o the ta et s dist ess as
A process in which unrelated the proximate level undermines the usefulness of a
species independently evolve a result of being helped is then transferred back to the
similar traits or capacities in
dichotomy between selfish and altruistic motives6,73. As observer, ameliorating the observer’s caught distress
response to similar expressed by Hoffman74, “empathy may be uniquely well step this ed ctio co stit tes a i t i sic e a d o
environmental pressures. suited for bridging the gap between egoism and altruism, pe o ed alt is step

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Ideomotor action crying, human infants prompt caregivers into action. demands on it (for an example, see REF. 84). The fact that
An action that is covertly Equivalent signals operate in other animals in which mammals retain distress vocalizations into adulthood
mimicked when another’s reproduction requires feeding, cleaning and warm- hints at the continued survival value of care-inducing
action or movement of an ing of the young. Parents that paid close attention to signals, such as those that prompt primates to carefully
object is being observed, such
as moving your arm when you
the emotional signals from their offspring probably lick and clean the wounds of unrelated conspecifics85.
watch someone bowl or tilting out-reproduced the indifferent ones, and this selective Despite the fact that the spread of emotion from
your head in synchrony with advantage applies at least to mammals and birds. The one individual to another occurs spontaneously, empa-
a pendulum swing. signals of the young are not just responded to but induce thy is still subject to appraisals, filters and inhibitions86
an agitated state in observers, suggesting that parents that prevent it from being expressed when it would be
Motor imitation
Re-enactment by the observer
become distressed at the perception of offspring distress79. maladaptive. For example, chimpanzees are capable
of a target’s motor movements Transferred negative affect provides a natural motivation of brutally killing each other 87,88, as are humans. Social
or facial expressions. to act1,12. In addition, neuropeptide systems that subserve species must be able to suppress their empathic response
offspring care are homologous across mammals and facil- to another’s pain when, for example, it is better for the
Affordances
Motor or action properties of
itate altruism in humans (for a review, see REF. 78). Given observer to flee, keep a safe distance or confront a poten-
objects that are activated by this origin, the capacity to be motivated to help distressed tial adversary. Conflicting individual goals will prevent
their percepts, which are and vulnerable targets should occur in a wide variety of the activation of shared representations from proceeding
intrinsic to the mental vertebrates that show social attachment and parental care, to compassion, concern or altruistic action, but they are
representation of the object.
including rodents80, birds81 and possibly reptiles82. Given still needed to at least initially decode the target’s state.
Simon effect the highly conserved nature of neuropeptide systems, Conversely, in humans and other species, the empathic
A behavioural effect in which an even older origin of empathy could be envisioned, response is increased by similarity, familiarity and social
motor actions are facilitated particularly in species that show social attachments83. closeness (for examples, see REFS 1,47,89), and this is
when they are consistent with Once the neural underpinnings of an empathic ‘off- consistent with where evolutionary theory expects it to
the spatial location of the
stimulus, and slowed when
spring care system’ existed, they could serve outside of the occur: that is, in close interdependent social relationships
they are inconsistent or rearing context and have a role in the wider social fabric. that involve either genetic relatedness or reciprocation.
opposing the location. They could be activated by the perception of a distressed Thus, the empathy mechanism is biased in precisely the
adult conspecific, such as in rodent consolation behav- way that is predicted by the current evolutionary models
iour 50. For every species, the reach of empathy varies with of cooperation6.
its social organization, creating differences across solitary,
pair-bonded, cooperatively hunting or group-living ani- Neural basis
mals, not because the empathy mechanism works differ- The PAM1 offers a proximate explanation for how we
ently, but because species and their ecology place different can ‘feel into’ others’ states. The PAM derives from
a perception–action theory of motor behaviour that
reveals overlapping representations for performing and
observing actions, as exemplified in phenomena such as
Box 1 | Mirror neurons as part of the ‘bigger picture’
ideomotor action, motor imitation, affordances and the Simon
The extension of mirror neurons to social-cognitive phenomena135,136 has received both effect90. Applied to emotional phenomena, attending to
attention and criticism. Mirror cells cannot fully explain empathy, but their relevance another’s distress is assumed to activate observers’ own
should not be dismissed. Mirror neurons per se only represent a small subset of monkey distributed representations for the target and their state
F5 inferior premotor cells91 and, thus, must be part of a larger coding scheme. Yet, even
and situation — including related feelings, memories and
these single cells represent motor plans and goals, which are bidirectionally connected
associations — in a connectionist manner.
to the resulting sensations90, allowing primates to infer goals from simple observed acts.
Extended to emotional phenomena, observing an affective posture or expression can A few key early studies offered the first notable neuro-
feed back from peripheral motor representations to activate associated emotional scientific evidence for the PAM. First, mirror neurons were
states. After the discovery of mirror neurons in macaques91, their existence was recorded in macaque monkeys that responded similarly
confirmed in human patients137. Given that mirror cells were found in humans outside of to performed and observed actions, and these recordings
traditional ‘mirror regions’, mirroring may be a generalized neural coding strategy. In provided cellular-level evidence for perception–action
addition, some human cells are activated during execution but are inhibited during coding in the brain91 (BOX 1). Extending this to humans,
observation, which may assist in self–other distinction138. a subsequent imaging study found premotor activity in
Brain areas that constitute the wider ‘mirror system’ — namely, the inferior frontal the brains of participants who simply observed pictures of
gyrus (IFG; also known as Brodmann area 44) and rostral posterior parietal cortex (rPPC)
tools (for example, hammers) or silently named the use
— clearly participate in the imitation of motor acts, expressions and empathy. These
of the tool in their mind92. Finally, emotional evidence for
human mirror regions are homologous with the macaque mirror regions F5, and PF and
PFG (which are subdivisions of the rostral inferior parietal lobule). These human regions using personal representations to perceive another’s affect
are also interconnected with the insula and show activation in functional MRI (fMRI) came from a brain-lesion study in which patients were
studies of empathy and imitation136,139. The role of the IFG is supported by a meta-analysis most impaired at decoding another’s facial expressions of
that found consistent activation of the IFG and adjacent anterior insula during empathic emotion when they had somatosensory damage93. Since
pain118. The ventromedial prefrontal cortex can integrate such affective signals to guide these results were summarized in the original theoretical
emotional decisions134. Both mirror theories and the perception–action model (PAM) review paper 1, many studies have further tested this view
presume that motor acts and affective states can transfer from a target to an observer in through a variety of methods, including positron emission
a bottom-up, goal-relevant manner through shared representations for perception and tomography, functional neuroimaging (functional MRI
action. However, the PAM explains a wider range of phenomena and empathic
(fMRI)), psychophysiology, electromyography, transcra-
biases through its focus on distributed, person-specific representations that are
nial magnetic stimulation and electroencephalography
formed through experience7.
(for reviews, see REFS 94–96).

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Bottom-up Research has confirmed the existence of overlapping expression and empathy (BOX 1). There are more studies in
Describes a neural and mental neural signatures for experiencing and observing affective this rich field than can be described here, but we summa-
process that is stimulus-driven states, including happiness, anger, fear, disgust, sadness97–99 rize the main findings and controversies below, focusing
on the basis of directly and — most often — pain (for a review, see REF. 100). The on the implications for the PAM.
observed information without
requiring explicit cognitive
data are largely consistent, logical and supportive of the
processes or capacities. PAM. However, there is controversy in the field that orig- Levels of empathy in the brain. Even though the PAM
Empathy arises from inates from divergent views of what ‘overlap’ between rep- emphasizes the spontaneous activation of the observer’s
bottom-up processes that are resentations means (for example, it might be mistaken for representations for the target’s state7, it is not limited
shared across species such as
signatures that are ‘identical’ or ‘without distinct proper- to reflexive processes such as mimicry and emotional
motor mimicry, emotional
contagion and state matching.
ties’). In addition, controversy persists regarding the role contagion, but also addresses complex forms of empa-
of mirror neurons or mirror systems in empathy. Mirror thy, including the effects of attention, regulation, expe-
theories are similar to the PAM in that both rely on shared rience and culture. Perception–action processes are
representations for perception and action. However, the indeed more noticeable during contagion and mimicry.
PAM focuses more on distributed representations that However, the PAM is a proximate-level theory that pre-
include relevant feelings, memories and associations sumes a shared, distributed, neural representation for
that are related to the target, and to the target’s state and the self and other that is engaged whenever the state
situation. Even if mirror theories are sometimes maligned of another individual is decoded, even if the shared
because of popularized media accounts about them, they property is not always obvious to or felt by the observer.
should not be dismissed, but rather understood in con- If observers attend to another’s state, this produces
junction with information about neural coding strate- empathy and accuracy in a highly graded fashion that
gies and the function of the inferior frontal gyrus (IFG) increases with personal and contextual factors, and
in the perception and production of language, gesture, can be inhibited in many different ways (for example,
avoiding attention, focusing on the response and motor
inhibition at multiple levels of the system). As representa-
Target Observer
tions are person-specific and developed through experi-
ence, they are fundamentally sensitive to the observer’s
Cognitive unique history, which explains why empathy and accu-
racy increase with the relevance of the target’s state to
the observer’s own past experiences, and to their simi-
ecti e larity and familiarity; these effects occur across species
(as discussed above). As a result of this graded quality,
In cognitive empathy, top-down one cannot make binary statements about experiences
imagination activates the
a ecti e ep ese tatio s that that are ‘the same’ or ‘different’, or in which empathy or
a e also i ol ed i otto p accuracy either does or does not exist7,101.
a ecti e e path a d this Observers must process the target’s state using what-
p o ides the i a i atio
ith i o atio e a di ever relevant representations they possess — at least
the e otio al states o othe s initially — as part of the process of basic information
decoding. Degrees of ‘understanding’ that result from
this process range from a rudimentary sense that the
other feels ‘bad’ to a highly tailored, accurate under-
ist i ted associated ep ese tatio s that standing of that specific state and its entailments98,102.
a e i ol ed i a ecti e a d co iti e e path There is also information about the target in the observ-
• h siolo ical states • acial e p essio s er’s activated representation, which makes it possible
i ect pe ceptio leads to • Semantic concepts • od post es
otto p a ecti e e path • ssociated e o ies
for the observer to understand dissimilar others on the
basis of specific knowledge about them. Finally, shared
representations do not always lead to felt resonance,
i e | Both cognitive and affective empathy access distributed, person-specific compassion or help, particularly when the observer’s
affective representations. Bottom-up, affective empathy (red box) occurs when an
goals conflict with those of the target; this explains the
observer directly perceives the emotional state (such as a sad facial expression) of the
target. This naturally activates distributed, personal representations of the target’s state
importance of interdependence for prosocial outcomes.
in the observer (purple box). These representations have developed over time with Whereas neuroscience has shown that there are dis-
experience in the observer’s life and include associated memories, semantic concepts, tinct brain correlates for emotional and cognitive empathy
and bodily states and expressions. When empathy proceeds in a top-down, cognitive (for examples, see REFS 103–106), and clinicians observe
manner (blue box), the neural regions that support working memory, executive distinct emotional or cognitive empathy impairments in
function, emotion regulation and visuospatial processes instead access the affective clinical disorders107,108, these distinctions do not under-
empathy representations from the top-down (indicated by the arrows). Thus, although mine the shared-representations model. It is sometimes
the stimulation emerges from inside the mind rather than from the outside world, the useful to bifurcate empathy into affective and cognitive
affective regions and the associated representations are shared between cognitive
and affective processes. Thus, subtractions of affective from cognitive forms of
components, but this does not deny shared processes.
empathy reveal greater brain activity in the blue regions than in the red regions. Shared processing is required for both bottom-up and top-
However, the cognitive process must still access the affective regions and their shared down forms of empathy because it is the distributed affective
associated representations (purple) to provide the imagination or simulation with representation that imbues the percept with content and
content and meaning. meaning, and this is needed for all forms of empathy (FIG. 4).

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Top-down This initial decoding phase of processing is mostly brief during theory-of-mind tasks is more medial when the
Describes a neural and mental and not subjectively experienced, except in rare cases task is more affective (for example, involving the orbito-
process that requires of sustained resonance. Moreover, their shared proper- frontal cortex and/or VMPFC) and more lateral when
a conscious, cognitive ties cannot be demonstrated using procedures designed it is more cognitive (involving the DLPFC) (for exam-
evaluation to take into account
information that is not directly
to emphasize differences, such as the fMRI subtraction ples, see REFS 103–106). ‘Mentalizing’ per se — that is,
observable, such as taking method or even multi-voxel pattern analysis. By analogy, thinking about what the other thinks or believes, or tak-
another’s perspective or our concept of a chair includes the affordance of sitting in ing their perspective — is particularly associated with
reasoning about their state on a chair, which can be associated with motor activity when activation of the STG and TPJ106,109,110. The amygdala is
the basis of conceptual
viewing chairs. However, it does not follow from this that not always implicated in empathy because it habituates
knowledge. These processes
participate in more advanced
our neural correlates for viewing chairs and tree stumps quickly to repeated stimuli, but it is engaged by tasks that
forms of empathy that are are indistinguishable, or that either will always be accom- involve salient states such as fear and distress, or learning
more sophisticated in humans panied by subjectively felt pressure on our backsides. associations between these states and outcomes111–113.
and with age, but they are not When human subjects are presented with differ- However, just because neural regions are engaged to
required to simply understand
how someone feels.
ent tasks, concepts, instructions or stimuli, we obvi- different extents, or are engaged more reliably in one task
ously expect differences in brain activity. For example, than in another, does not mean that they are completely
emotional empathy tasks engage brain regions that ‘separate’ and do not share properties. Researchers need
are associated with affective and motor-motivational to focus on the inherent relationship between the task,
processes to a greater extent (for example, the insula, instructions and analysis strategy and their resulting
anterior cingulate cortex (ACC), thalamus, amygdala, neural correlates. Even if we argue against oversim-
fusiform gyrus, somatosensory and motor cortices, and plified claims about neural distinctiveness or overlap,
ventromedial prefrontal cortex (VMPFC)). Cognitive it is true that we need to study the precise way in which rep-
empathy and perspective-taking tasks engage exec- resentations overlap versus the precise way in which they
utive, working memory and visuospatial processes are distinct, particularly at the scale of neurons and their
to a greater extent (for example, the dorsolateral PFC distributed interconnections.
(DLPFC), dorsomedial PFC (DMPFC), superior tempo-
ral gyrus (STG), temporoparietal junction (TPJ), supe- Empathic pain. Owing to its ease of study, physical pain
rior parietal lobule (SPL) and inferior parietal lobule is the most common context for testing shared rep-
(IPL)) (FIG. 5). In addition, the frontal activity observed resentations between the self and the other. Typically,

aMCC, SMA DLPFC M1 S1

ACC and CMA Thalamus
S2
IPL

TPJ

VMPFC PI
AI and
IFG
Amygdala TP
Thalamus FG
STG Hypothalamus FG

Regions emphasized by Regions emphasized by e io s sha ed et ee co iti e

a ecti e empathy tasks co iti e e path tas s a d a ecti e tas s

Nature Reviews | Neuroscience

Figure 5 | Neural regions that participate in human empathy. The figure shows a medial sagittal view (far left), a left
lateral side view (centre) and a coronal view (far right) of the human brain, and indicates the relative locations and roles of
brain areas that are involved in human empathy. Affective representations are required to imagine how another person
feels. Depending on the task, however, the observed neural activity will emphasize bottom-up, affective brain areas or
top-down, cognitive ones. Regions that are more associated with affective empathy tasks — such as direct perception of
the emotion or pain of another person — are shown in red: the anterior cingulate cortex (ACC) including perigenual and
subgenual regions of the ACC, amygdala, thalamus, hypothalamus, primary motor cortex (M1), premotor cortex, the
p i a a d seco da so atose so co tices a d a d the te po al pole ai e io s that a e o e
associated with higher-level, top-down forms of empathy — such as imagining how you would feel in the place of another
o ta i thei pe specti e a e sho i l e the do solate al p e o tal co te i e io pa ietal lo le
te po opa ietal ctio s pe io te po al s a d si o s o e io s that a e co o l
activated in both affective and cognitive tasks are shown in green: the anterior insula (AI) and the anterior middle
ci late co te a hich e te ds do sall i to the s pple e ta oto a ea a d ci late oto a ea
e al locatio s a e app o i ated so that the e io s ca e ie ed i st th ee i a es o e a ple the is
normally too medial to be seen in the lateral image, the amygdala is shown in the medial view as emerging from behind the
isi le idli e slice i i ht te po al co te a d di e e ces i late alit e io a d tas a e ot ep ese ted
inferior frontal gyrus; PI, posterior insula; VMPFC, ventromedial PFC.

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participants view images of injury to another (for exam- effects are influenced by personal experience, patients
ple, a hand closed in a door or cut with a knife) or sym- with congenital insensitivity to pain (CIP) — who do
bols that are associated with the application of a noxious not experience peripheral pain — are also impaired
stimulus to another (for example, an electrical shock or at detecting others’ pain and can feel indifferent to it,
a hand submerged in ice-cold water). In other phases of although their performance can be improved by trait
the experiment, the same participants receive a noxious concern for others122 (BOX 2).
stimulus to their own body. Neural activity is operation- The precise meaning of the ‘empathic pain’ network
alized as ‘empathic pain’ when the same brain region is is debated (see REFS 118,123–126). Generally, researchers
activated during pain to the self and pain to the other. assume that the anterior insula and aMCC do not repre-
Data from these studies strongly support the PAM in sent the sensation of physical pain, such as the feeling of
that pain representations are shared but not identical, a prick on your arm or a burn on your fingertip. Instead,
and are widely distributed and highly specific to the these regions are thought to encode something about
state, task and the observer’s prior experiences. Almost the salient, aversive or arousing properties that pain
all studies find that both experiencing pain (‘self pain’) shares with other experiences. Even the earliest reports
and perceiving another’s pain (‘other pain’ or ‘empathic of empathic pain suggested that it represents affective
pain’) activate the anterior insula and cingulate cortex rather than sensory components114. Similarly, a recent
(from the posterior ACC (pACC) to the anterior middle meta-analysis found that the bilateral anterior insula and
cingulate cortex (aMCC))114–117. A meta-analysis has con- the dorsal ACC (dACC)–aMCC–supplementary motor
firmed early empirical reports, and found that viewing area (SMA) were reliably activated during empathy for
either pain or symbols of pain to the other consistently pain and for basic emotions125. Moreover, self and other
activate the bilateral anterior insula (merging into the experiences activate the left anterior insula and mACC
IFG), and the pACC or aMCC118. for three distinct negative experiences (pain, disgust
There is also pharmacological evidence that one’s and economic unfairness)126. In addition, patients with
own pain influences how one processes the pain of oth- CIP still show anterior insula and aMCC activity when
ers. Acetaminophen decreases self pain and empathic observing others’ pain, which suggests that the activation
pain for physical and social forms of distress 119. does not derive from peripheral sensations127 (BOX 2).
Analgesia reduces self pain and empathic pain, and this Of course, introspection alone is sufficient to tell us
is accompanied by reduced pain ratings and alterations that empathic pain does not usually make people feel
in the pain related P2 type event-related potential120. the precise peripheral sensation that they witness being
Even placebo analgesia reduces empathic pain and experienced by another. People do not look at their own
associated activity in the anterior insula and aMCC, hand when they see someone touch a hot stove or say
and this effect can be blocked by the opioid antago- “Ouch!”. They are more likely to feel an aversive sicken-
nist naltrexone121. Moreover, demonstrating that pain ing feeling in their stomach and wrinkle their nose in
disgust while turning away and exclaiming “Ooh!” or
“Ugh!”. Their experiences differ from those of the other.
Box 2 | The mysterious case of empathic pain in patients who do not feel any
As such, they must also differ at the level of the brain
while sharing affective properties as well.
Functional MRI (fMRI) has shown that the anterior insula and anterior middle cingulate Although the representations in the anterior insula
cortex (aMCC) are activated in patients with congenital insensitivity to pain (CIP) are unlikely to be specific or exclusive to felt pain (at
during empathic pain122,127. Does this mean that empathy does not require a similar least in this anterior region), they probably represent
experience or access to personal representations of pain? The data tell a different story.
feeling states that are more like the internal ‘gut’ feelings
Patients with CIP are actually impaired at perceiving others’ pain and empathizing
with them, and this impairment scales with their pain insensitivity. In one study,
that are experienced in a wide variety of intense states,
patients with CIP “frequently suspected other people of exaggerating their pain and including disgust, pain, dread, anxiety, stomach aches
often considered others — including their friends or spouse — as ‘sissies’” (REF. 122). and even desire. The anterior insula is known to repre-
Some patients showed no reaction to others’ pain at all, in experiments or real life122. sent interoceptive states across species128, and patients
Patients with CIP also rate others’ pain as less aversive, they have a less intense with CIP who have spared anterior insula activation in
empathic pain response in the left anterior insula and inferior frontal gyrus, and the response to empathic pain do experience internal sen-
aMCC, and they lack the aMCC response to others’ facial pain. In short, patients with sations such as headaches and stomach aches127. The
CIP are impaired at empathizing with others’ pain. aMCC is assumed to respond to any unexpected out-
Patients with CIP also do not have a deficit for all types of pain, only peripheral pain, come that requires a fast or reissued response, including
and some somatic pain (for example, headaches and migraines) remains intact122.
pain, non-pain negative states, cognitive-motor errors
These intact representations allow them to relate to the noxious, aversive, motivating
properties of pain that are represented in the anterior insula and aMCC. Patients with
and even unexpected rewards (see REFS 71,129–131).
CIP also learn how to interpret pain cues, allowing them to pass easy behavioural tests This motor-motivational view of the aMCC is consist-
such as rating facial pain on a three-point scale122. ent with other proposals71,125,131 and with the caregiving
Therefore, data from patients with CIP support the perception–action model by model of altruism78. These interpretations are consist-
showing that it is harder to feel concerned about another’s state in the absence of ent with the core principle of the PAM that the brain
a highly relevant, elaborate representation of the same state from personal integrates sensation and action more than linguistic and
experience. It also supports the view that the brain uses whatever representations disciplinary categories tend to.
are available to understand others, in a way that scales with the relevance of the Even if the anterior insula and aMCC are not spe-
observer’s experiences7. Experience with one’s own pain thus influences one’s ability cific to felt pain, one should not conversely infer that
to empathize with another’s.
empathy ‘never’ includes bodily sensations or peripheral

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stimulation. Ideomotor actions and spontaneous mim- Research supports an evolutionary, perception–action
icry demonstrate the effector-specific, peripheral effects view in which observers spontaneously imitate, mimic
of the underlying neural perception–action process90. In and ‘feel into’ the states of those they attend to through
the emotional domain, the somatosensory cortices are a neural process by which the targets’ states are mapped
activated during a variety of empathy tasks — includ- onto the observers’ distributed learned and personal
ing those involving pain104, facial emotion recognition93 representations for the target, state and situation. This
and emotional empathy 105 — thus indicating a role for shared component of self and other representations
sensation in observing emotions, particularly when the explains the strong biases for similarity, familiarity and
task emphasizes sensation. The anterior insula — which past experience that are found across species.
is consistently activated during empathic pain (see All species may not possess complex capacities to
above) — is also active during observed and imitated put themselves into another’s ‘shoes’ in the same goal-
facial emotion132, felt and observed disgust 97,133, and the directed manner as is seen in humans, but most car-
feeling of ‘butterflies in the stomach’ while anticipating egiving mammals that live in interdependent social
risk134. Thus, there are times when sensations have a groups are affected by the pain and distress of familiar
more prominent role in empathic emotion perception, others in ways that may propel them to act on their
particularly when the sensation is made salient by the behalf. For some species, there is experimental evi-
stimuli and task instructions. For example, rating pain dence of well-developed empathic perspective-taking
intensity on the target’s limb activates more sensory and targeted helping. Shared representations of affec-
areas than does rating pain aversiveness or viewing tive states are activated from the top down in more
facial pain expressions without knowing the cause124. cognitive forms of empathy, which recruit additional
Tasks that focus attention on the location of the injury executive and visuospatial processes. However, the lit-
activate more sensory activity (for example, in S1, S2 erature overestimates distinctions between emotional
and the SMA), whereas tasks that ask subjects to ‘place and cognitive empathy, following traditional practices
themselves into the shoes of the other’ recruit more to dichotomize in science and philosophy. Despite each
visuospatial, executive and working-memory processes having unique features, affective and cognitive empa-
(mentalizing; for example, the STG, TPJ, IPL, DMPFC thy both require access to the shared representations of
and VMPFC)100,118,124. By carefully linking neural regions emotion that provide simulations with content and an
to the focus of the task and the experience of the subject, embodied meaning.
the many seemingly puzzling results from different stud- Future research must examine empathy and its mech-
ies begin to make sense. anisms in a wider variety of species, even beyond the
mammals, to better understand the underlying mech-
Conclusion anisms and how empathy shifts with social ecology. In
Our scientific understanding of empathy has greatly addition, neuroscience must move beyond oversimplified
improved within the past two decades owing to a huge claims of ‘same’ or ‘different’ processes, and apply a more
amount of research into how this capacity evolved, exists phenomenological approach that contextualizes results
across species, and is instantiated in the body and brain. within the tasks, instructions and analyses employed.

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Affect. Neurosci. 11, 1345–1353 (2016). affect, pain and cognitive control in the cingulate The authors declare no competing interests.
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opioidergic regulation suggest that empathy for pain 131. Morrison, I., Peelen, M. V. & Downing, P. E. The sight of Publisher’s note
is grounded in self pain. Proc. Natl Acad. Sci. USA others’ pain modulates motor processing in human Springer Nature remains neutral with regard to jurisdictional
112, E5638–E5646 (2015). cingulate cortex. Cereb. Cortex 17, 2214–2222 (2007). claims in published maps and institutional affiliations.

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