Empathy: Its ultimate and proximate bases

BEHAVIORAL AND BRAIN SCIENCES (2002) 25, 1–72
Printed in the United States of America
Empathy: Its ultimate and proximate
bases
Stephanie D. Prestona and Frans B. M. de Waalb
aUniversity of Iowa Hospital and Clinics, 2RCP – Neurology Clinic, Iowa City,
IA 52242; bLiving Links, Yerkes Primate Center and Psychology Department,
Emory University, Atlanta, GA 30322
stephanie-d-preston@uiowa.edu
dewaal@rmy.emory.edu
http://www.medicine.uiowa.edu/prestonresearch
http://www.emory.edu/LIVING_LINKS/
Abstract: There is disagreement in the literature about the exact nature of the phenomenon of empathy. There are emotional, cogni-
tive, and conditioning views, applying in varying degrees across species. An adequate description of the ultimate and proximate mecha-
nism can integrate these views. Proximately, the perception of an object’s state activates the subject’s corresponding representations,
which in turn activate somatic and autonomic responses. This mechanism supports basic behaviors (e.g., alarm, social facilitation, vicar-
iousness of emotions, mother-infant responsiveness, and the modeling of competitors and predators) that are crucial for the reproduc-
tive success of animals living in groups. The Perception-Action Model (PAM), together with an understanding of how representations
change with experience, can explain the major empirical effects in the literature (similarity, familiarity, past experience, explicit teach-
ing, and salience). It can also predict a variety of empathy disorders. The interaction between the PAM and prefrontal functioning can
also explain different levels of empathy across species and age groups. This view can advance our evolutionary understanding of empa-
thy beyond inclusive fitness and reciprocal altruism and can explain different levels of empathy across individuals, species, stages of de-
velopment, and situations.
Keywords: altruism; cognitive empathy; comparative; emotion; emotional contagion; empathy; evolution; human; perception-action;
perspective taking
1. Introduction
key in sight of the subject to be shocked. After the subjects
witnessed the shock of the conspecific, two-thirds pre-
The concept empathy has had a difficult history, marked by
ferred the nonshock chain even though it resulted in half as
disagreement and discrepancy. Although it has been stud-
many rewards. Of the remaining third, one stopped pulling
ied for hundreds of years, with contributions from philoso-
the chains altogether for 5 days and another for 12 days af-
phy, theology, developmental psychology, social and per-
ter witnessing the shock of the object. These monkeys were
sonality psychology, ethology, and neuroscience, the field
literally starving themselves to prevent the shock to the con-
suffers from a lack of consensus regarding the nature of the
specific. Starvation was induced more by visual than audi-
phenomenon. Despite this disagreement, the empirical
tory cues, was more likely in animals that had experienced
data on empathy are very consistent, across a wide range of
shock themselves, and was enhanced by familiarity with the
species. Consider the following examples:
shocked individual (Masserman et al. 1964).
An albino rat sees a distressed conspecific suspended in
Human infants orient to the distress of others, often re-
the air by a harness; he presses a bar to lower the rat back
sponding with their own distress cries from infancy to 14
to safe ground, staying close to and oriented toward him
months (e.g., Sagi & Hoffman 1976; Ungerer 1990; Zahn-
(Rice & Gainer 1962). Another rat sees a distressed con-
Waxler & Radke-Yarrow 1982). After the first year, children
specific receiving electric shocks and does not press the bar
start to show helping behaviors, even when they have be-
to terminate the shock, he instead “retreat[s] to the cor-
come distressed. They also imitate the distress behaviors of
ner . . . farthest from the distressed, squeaking, and danc-
the other, possibly “trying on” the expressions to better un-
ing animal and crouch[es] there, motionless” (Rice 1964,
derstand them (Zahn-Waxler et al. 1977, in Thompson
p. 167). The response of a rat to shock of a conspecific oc-
1987). With age, the level of personal distress decreases
curs without any prior experience with shock, is stronger af-
while appropriateness of helping behaviors increases (e.g.,
ter prior experience with shock, and strongest when prior
Zahn-Waxler et al. 1983).
shock occurred at the same time as to the conspecific
These examples, all from empirical reports, show that in-
(Church 1959).
dividuals of many species are distressed by the distress of a
In an experiment with rhesus monkeys, subjects were
conspecific and will act to terminate the object’s distress,
trained to pull two chains that delivered different amounts
even incurring risk to themselves. Humans and other ani-
of food. The experimenters then altered the situation so
mals exhibit the same robust effects of familiarity, past ex-
that pulling the chain with the larger reward caused a mon-
perience, and cue salience (Table 1), and parallels exist be-
© 2002 Cambridge University Press
0140-525X/02 $12.50
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Preston & de Waal: Empathy: Its ultimate and proximate bases
tween the development of empathy in young humans and
1.1. Terminology
the phylogenetic emergence of empathy (de Waal 1996;
Hoffman 1990, respectively). These facts suggest that em-
1.1.1. Proximate versus ultimate. Ernst Mayr first created
pathy is a phylogenetically continuous phenomenon, as
the distinction between proximate and ultimate causes of
suggested by Charles Darwin more than a century ago
behavior. According to Mayr, “proximate causes govern the
(1871/1982).
responses of the individual (and his organs) to immediate
The goal of this theoretical review is to present data
factors of the environment while ultimate causes are re-
across disciplines so that the continuity is apparent. More-
sponsible for the evolution of the particular DNA code of
over, this paper aims to show that consistencies exist be-
information with which every individual of every species is
cause all empathic processes rely on a general perception-
endowed” (Mayr 1961, p. 1503). Causes exist at each of
action design of the nervous system that has been postulated
these levels; therefore, theories that refer to different lev-
for over a century, is adaptive for myriad reasons, and exists
els are not in conflict. For example, when you help your dis-
across species. Recent advances in interdisciplinary re-
tressed neighbor, is it because you “feel their pain,” or be-
search and tools for understanding the brain provide strong
cause you will eventually need them to reciprocate? Given
support for the Perception-Action Model (PAM), warrant-
Mayr’s levels of causality, these hypotheses are not in con-
ing its application to emotional domains. This Perception-
flict; the former is a proximate explanation, the latter an ul-
Action Model also sheds light on the ultimate level de-
timate one.
scription, placing the emphasis on direct effects on
reproductive success from the general design of the ner-
1.1.2. Definitional distinctions. Much of the empathy lit-
vous system, rather than on indirect effects from helping
erature focuses on whether empathy is an emotional or cog-
behaviors. Thus, by fleshing out the phenomenon along
nitive process and distinguishes empathy from emotional
both proximate and ultimate levels, and by combining data
contagion, sympathy, and perspective taking (e.g., Eisen-
across fields, a unified story emerges.
berg 1986; Feshbach 1975; Hoffman 1978a; 1982a; Horn-
blow 1980; Omdahl 1995; Shantz 1975; Wispé 1986). These
distinctions are empirically based and help to categorize be-
havior (Batson et al. 1987; Doherty 1997; Eisenberg et al.
1994; 1998; Eisenberg & Okun 1996; Rice 1964; distinc-
tions summarized in Table 2), but they have been overem-
phasized to the point of distraction. This overemphasis on
definition reflects the deeper problem that empathy lacks
Stephanie Preston received her doctorate in Psy-
a proximate mechanism. Abstract and elusive definitions
chology in 2001 from the University of California,
like “putting oneself in the place of another” or “imagina-
Berkeley. Her dissertation investigated the effects of so-
tively projecting oneself into the situation of another” (All-
cial and metabolic stress on food-hoarding decisions in
port 1937; Buchheimer 1963; Demos 1984; Goldie 1999;
kangaroo rats. Her interdisciplinary research combines
Smith 1989) indicate an insufficient understanding of the
techniques and ideas across fields, and uses naturalistic
paradigms, in order to study how emotion and cognition
way the nervous system instantiates empathy. Thirty years
interact to produce behavior. She is currently a post-
ago G. W. Allport said it best when he concluded, “the
doctoral fellow at the University of Iowa with Antoine
process of empathy remains a riddle in social psychol-
Bechara, doing behavioral, psychophysiological, and
ogy . . . The nature of the mechanism is not yet understood”
brain imaging research on empathy, decision-making,
(Allport 1968, p. 30 from Wispé 1987, original emphasis).
and hoarding.
The original German word Einfühlung, of which the Eng-
Frans B. M. de Waal is a Dutch-born ethologist/
lish “empathy” is Titchener’s translation (1909; Wispé 1991,
zoologist renowned for his work on the social intelli-
p. 78), literally means “feeling into” (Wispé 1986). Einfüh-
gence of primates, such as chimpanzees, bonobos, ca-
lung was thought to result from a process where observers
puchin monkeys, and macaques. His first book, Chim-
project themselves into the objects they perceive (Lipps
panzee Politics (1982) compared the schmoozing and
1903; McDougall 1908/1923; Titchener 1909). Theodore
scheming of chimpanzees involved in power struggles at
Lipps first put forth a mechanistic account of Einfühlung,
the Arnhem Zoo with that of human politicians. Ever
where the perception of an emotional gesture in another di-
since, de Waal has drawn parallels between primate and
human behavior, from peacemaking and morality to cul-
rectly activates the same emotion in the perceiver, without
ture. His scientific work, conducted first in the Nether-
any intervening labeling, associative, or cognitive perspec-
lands and later at NIH-sponsored regional primate cen-
tive-taking processes (Lipps 1903). Two paths have since di-
ters in the USA, has been published in numerous
verged from the original Einfühlung.
technical articles in journals such as Science, Nature,
Some theories focused on the direct perception aspect,
Scientific American, and outlets specialized in animal
and on the basis of empathy in emotional contagion or im-
behavior and primatology. His award-winning popular
itation (e.g., Brothers 1990; Hatfield et al. 1993; Hume 1888/
books have been translated into more than a dozen dif-
1990; Levenson 1996; Levenson & Reuf 1992; Nietzsche
ferent languages. His latest work, The Ape and the Sushi
1895/1920; Smith 1759/1976; Wermlund 1949). McDou-
Master (Basic Books, 2001), tries to bridge the na-
gall observes in his Introduction to Social Psychology (1908/
ture/culture divide. Dr. de Waal is C. H. Candler Pro-
fessor in the Psychology Department of Emory Univer-
1923, p. 93) “that the behavior of one animal, upon the ex-
sity and Director of the Living Links Center at the
citement of an instinct, immediately evokes similar behav-
Yerkes Primate Center, Atlanta, Georgia. He is Corre-
ior in those of his fellows who perceive his expressions of
spondent Member of the Royal Dutch Academy of
excitement.” McDougall includes imitation of facial ex-
Sciences.
pressions from mother to infant, feelings of tenderness
evoked in observers of mother-infant interactions, and the
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Preston & de Waal: Empathy: Its ultimate and proximate bases
Table 1. Cross-species references for five main empathy literature findings. Empathy increases with Familiarity (subject’s previous
experience with object), Similarity (perceived overlap between subject and object, e.g., species, personality, age, gender), Learning
(explicit or implicit teaching), Past experience (with situation of distress), and Salience (strength of perceptual signal,
e.g., louder, closer, more realistic, etc.)
Past
Familiarity
Similarity
Learning
experience
Salience
Rats
Church 1959;
Lavery & Foley 1963;
Watanabe & Ono 1986
Rice & Gainer 1962
Monkeys
Aureli et al. 1989;
Miller et al. 1966;
de Waal 1996;
Masserman et al. 1964;
Miller et al. 1959a;
Aureli et al. 1997;
Miller et al. 1967;
de Waal et al. 1996
Miller et al. 1967
Miller & Deets 1976
Cords & Thurnheer
Miller et al. 1959a
1993; Demaria &
Thierry 2001;
Masserman et al.
1964; Miller et al.
1959a
Apes
O’Connell 1995
Yerkes & Yerkes 1929
Povinelli et al. 1992a
O’Connell, 1995
Human
Zahn-Waxler &
Martin & Clark
Capps & Sigman
Lamb & Zakhireh 1997;
infants
Radke-Yarrow
1982; Simner
1996; Thompson
Sagi & Hoffman
1982
1971
1987
1976; Simner 1971
Human
Zahn-Waxler
Feshbach &
Krebs 1970;
Murphy 1937
Eisenberg et al. 1990;
children
1982; Zahn-
Roe 1968;
Eisenberg et al.
Eisenberg et al. 1993
Waxler et al.
Rosekrans 1967;
1983; Radke-Yarrow
1984; Farver
Shantz 1975;
1983; Trivers 1974;
& Branstetter
Smith 1988
Ungerer 1990;
1994; Howes
Zahn-Waxler et al.
& Farver 1987
1979; Zahn-Waxler
1984
Human
Cialdini et al.
Batson et al.
Aronfreed 1968;
Aronfreed 1965;
adults
1997; Sawyer
1981; Krebs
Gruen &
Eisenberg et al.
1966; Stinson
1975; Toi &
Mendelsohn
1991; Eisen-
& Ickes 1992
Batson 1982;
1986; Stinson
berg et al. 1994;
Gruen &
& Ickes 1992
Gouldner 1960
Mendelson
1986
contagious distress evoked in chimpanzees by the distress
US, and eventually responds to the distress of the other
of a conspecific.
with distress. Supporting this view, rats pre-trained with a
Other theories make use of Lipps’ projection, imitation,
shock paired to the shock of a conspecific significantly de-
and imagination, without the direct perception. This makes
crease bar pressing for the remainder of the experiment (in-
empathy a high-level, cognitive phenomenon, reserved for
terpreted as anxiety). However, as mentioned above, rats
humans (e.g., Allport 1961; Deutsch & Maddle 1975;
that experience an unpaired shock also decrease bar press-
Freud 1922/1945; Mead 1934; Titchener 1915). Even in
ing, just to a lesser degree. Even subjects that never ex-
comparative frameworks, empathy can be synonymous with
perienced shock decreased bar pressing, but the response
“perspective taking.” In one cooperation paradigm, animals
habituates quickly (Church 1959). These results were repli-
are considered to have empathy if they can perform the task
cated with pigeons (Watanabe & Ono 1986).
of their human partner after only having observed it during
Developmental research has incorporated different lev-
training. The transfer task is successfully done by apes but
els of empathy by tracking changes in the life span (e.g.,
not monkeys and is interpreted as evidence that only the
Eisenberg et al. 1983; Hoffman 1978; Ungerer 1990; Zahn-
former have empathy (Povinelli et al. 1992a; 1992c, respec-
Waxler & Radke-Yarrow 1982; Zahn-Waxler et al. 1992a).
tively). The task is not performed between conspecifics,
Hoffman (1982a; 2000) outlines a variety of emotional and
and does not include an emotional component.
cognitive processes that are involved in empathy, but a great
Still other theories reject both the direct perception ap-
deal of work needs to be done to clarify why these transi-
proach and the cognitive approach and suggest that empa-
tions take place, and how these levels interact.
thy is the result of conditioning (e.g., Allport 1924; Becker
These different views of empathy can be cohered into a
1931; Church 1959; Scheler 1923/1954). In the condition-
unified whole if a broad view of the perception-action
ing view, the distress of another is the Conditioned Stimu-
model is taken. The perception-action model is supported
lus (CS), and the distressor itself is the Unconditioned
when existing behavioral data on empathy is combined with
Stimulus (US). The subject learns that the CS predicts the
recent data from physiology and functional neuroanatomy.
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Preston & de Waal: Empathy: Its ultimate and proximate bases
Table 2. Usage of terminology by most current researchers divided into main variables of classification updated for a
perception-action view of the phenomena
Self-other
State
Term
Definition
distinction?
matching?
Helping?
Synonyms
Emotional
Subject’s state
No
Yes
None
personal distress,
contagion
results from the
vicarious emotion,
perception of object’s
emotional transfer
state
Sympathy
Subject feels “sorry for”
Yes
No
Depends
the object. Focused
more on object’s
situation than physical
state.
Empathy
Subject’s state results
Yes
At representation
Increasing with
from the attended
level, not
familiarity,
perception of the object’s
necessarily
similarity,
state.
visible.
salience.
Cognitive
Subject represents
Yes
No
Depends
true empathy,
empathy
state of object
perspective-
through top-down
taking
processes.
Prosocial
Actions taken to reduce
Usually
Not
Yes
helping, succorance
behaviors
the object’s distress.
necessarily
Applying the perception-action mechanism broadly re-
tonomic and somatic responses, unless inhibited (see Table
coheres the discrepant views into a unified whole, and
3 for clarification on the terms).
changes the ultimate model.
With the Perception-Action Model, whether or not a
subject perceives the state of the object depends crucially
1.1.3. An overview of the model. Throughout, the object is
referred to as the primary individual who experienced the
emotion or state. The subject is the individual that secon-
darily experienced or understood the emotion/state of the
object, through empathy. The authors view the term empa-
thy broadly, similar to Hoffman (2000), as: any process
where the attended perception of the object’s state generates
a state in the subject that is more applicable to the object’s
state or situation than to the subject’s own prior state or sit-
uation.
While Hoffman’s (2000) definition of empathy, and that
of many others focuses on the response of the subject, our
definition focuses on the process. A process model makes
empathy a superordinate category that includes all sub-
classes of phenomena that share the same mechanism. This
includes emotional contagion, sympathy, cognitive empa-
thy, helping behavior, and so on (Fig. 1). These phenomena
all share aspects of their underlying process and cannot be
totally disentangled (as also suggested by Thompson 1987).
All forms of empathy involve some level of emotional con-
tagion and personal distress (if only at the representational
level), and helping is never entirely for the sake of the ob-
ject (if only at the ultimate level). This process model also
links empathy to all facilitation behaviors that rely on per-
Figure 1. In order to unify the various perspectives, empathy
ception-action (e.g., ideomotor actions, imitation, the yawn
needs to be construed broadly to include all processes that rely on
reflex, automaticity, priming; see Fig. 1).
the perception-action mechanism. Thus, perception-action is a
superordinate class, which includes two basic level categories,
A Perception-Action Model of empathy specifically
motor behavior and emotional behavior. Both of these basic level
states that attended perception of the object’s state auto-
categories include subordinate categories of phenomena. Thus,
matically activates the subject’s representations of the state,
according to the model, various phenomena like emotional conta-
situation, and object, and that activation of these represen-
gion, cognitive empathy, guilt, and helping are similar in that they
tations automatically primes or generates the associated au-
rely on the perception-action mechanism.
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Preston & de Waal: Empathy: Its ultimate and proximate bases
Table 3. Clarification of terms from the summary of the model that are used throughout
Term
Meaning
Perception-
From the Perception-Action Hypothesis of motor behavior (Prinz 1987; 1992; 1997). Term “response” used in text
action
to refer to a more general class of phenomena.
Attended
Refers to the fact that strong empathic responses require that the subject is attending to the state of the object.
Differences in empathy across individuals, age groups, and situations are predictable from levels of attention.
Perception
Flexible definition that includes direct activation from the object in the external world, indirect activation from
associations with external events or objects, and indirect activation through imagination.
Automatically
As a matter of course, unless controlled or inhibited. Does not require conscious and effortful processing.
Representation
Parallel distributed patterns of activation that reliably fire in response to a given stimulus. Formed by the combina-
tion of developmental tuning biases and connectivity of neurons as well as alterations due to experience.
Unless
Imitative actions are inhibited during observation of action, centrally (from prefrontal inhibition), peripherally
inhibited
(with spinal cord inhibition blocking the motorneurons that execute the action), or both.
on their interdependence or interrelationship. Interdepen-
can be decreased by distracting or re-orienting attention,
dence can be temporary and superficial, like when the sub-
distress returns to almost equal levels when the distraction
ject and object must cooperate for a local goal or when the
stimulus is removed, and the hormonal stress response may
object’s distress blocks the goal of the subject. Interdepen-
remain throughout (Gunnar et al. 1984; Harman 1994; re-
dence can also be long lasting and deep, like the interde-
viewed in Rothbart et al. 1994). This internal “distress
pendence of family members or spouses that must cooper-
keeper” (Rothbart et al. 1994) may be the mechanism for
ate for long-term goals spanning a lifetime. The more
negative feelings like guilt and remorse that pervade even
interrelated the subject and object, the more the subject
when attention is shifted. As evidence, trait sympathy is cor-
will attend to the event, the more their similar representa-
related with the probability for entering situations of dis-
tions will be activated, and the more likely a response. The
tress and the susceptibility for guilt and shame after refus-
more similar the representations of the subject and object,
ing to help (reviewed by Smith 1992).
the easier it is to process the state of the object and gener-
These processes do not require conscious awareness, but
ate an appropriate response.
they can be augmented by cognitive capacities in evolution
There are broadly two types of response: response with
and development so that empathy is possible in the absence
the object (matching responses as with distress to distress
of the object of distress, from imagination or effortful pro-
or joy to joy), and response to the object (instrumental re-
cessing. For example, if a subject witnesses the distressed
sponses as with consolation to distress or fear to anger). Ex-
state of an object that has been robbed, the subject may feel
emplifying responses with the object, human and nonhu-
distressed, and may think about the object, robbery, and
man subjects that correctly identify the emotion of an
feelings of vulnerability and fear. Alternatively, the subject
object have a physiological response that is correlated with
may think of the object or hear of the object’s loss, which in
the object’s state (Levenson & Ruef 1992; Miller et al. 1967,
turn activates associated thoughts related to the object –
respectively). Exemplifying responses to the object, human
robbery and vulnerability – and produces feelings of dis-
subjects that are empathically concerned show a decelera-
tress.
tory heart-rate response to the object of distress (Eisenberg
The arguments for adaptation and evolution of percep-
et al. 1990; 1991; 1994) and rhesus macaque subjects show
tion-action processes are presented in the next section “The
increased heart rate to the approach of a dominant animal
ultimate bases of empathy.” The proximate model follows,
(controlling for posture and activity) (Aureli et al. 1999).
with a review of the literature on perception-action in mo-
Since imitation emerges much earlier than prosocial re-
tor behavior, and in emotional behavior (including adult hu-
sponse, and people learn to inhibit and control emotional
mans, nonhuman animals, human children, and individuals
contagion and imitation, responses with the object should
with empathy disorders). Finally, there is a detailed de-
emerge earlier, and with less learning. But, data in the ulti-
scription of the role that representation plays in a percep-
mate section attest to the need for experience to fine-tune
tion-action model, explaining the pervasive effects of learn-
the circuits for responding with the object as well; thus, a
ing and experience on empathic processes. Cognitive
strict division along “nature versus nurture” is not war-
empathy is addressed in the final section as a phenomenon
ranted.
based on the perception-action mechanism, but requiring
The automaticity of overt responses with the object de-
additional cognitive capacities that develop with the pre-
crease with age and experience, due to many factors, dis-
frontal cortex.
cussed below. These include increased prefrontal function-
ing, increased segregation of self and other representations,
and learned display rules – all of which inhibit the auto-
2.The ultimate bases of empathy
matic response. In addition, attention can be preemptively
allocated when an automatic response is undesirable (de-
Ultimate accounts are notorious for being cursory and spec-
termined by current goals and the ability to help). However,
ulative. Moreover, previous evolutionary models of empa-
covert responses may still occur, even outside of awareness.
thy did not reference important empirical research avail-
In orienting studies with infants, even though overt distress
able in animals and humans, and dealt only with one aspect
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Preston & de Waal: Empathy: Its ultimate and proximate bases
or one level of the phenomenon. For example, many have
of a complex cost/benefit analysis on the perceived effec-
proposed that emotional contagion exists to facilitate the
tiveness of helping and the effect of helping on short and
mother-infant bond (Darwin 1998/1872; McDougall 1908/
long-term goals. If the cost is greater than the benefit, at-
1923; Plutchik 1987). Because emotional contagion is con-
tention can be directed away from the distress to control or
sidered related to empathy, the mother-infant bond is tran-
subvert empathic processing altogether, making the desire
sitively used as an evolutionary explanation for empathy.
to help less likely.
While the mother-infant bond is surely important for de-
According to a perception-action model, the evolution of
veloping empathy, this does not allow automatic forms of
a perception-action organization of the nervous system was
empathy to be linked with cognitive forms, or explain why
the precursor to empathy; this organization is adaptive for
we experience empathy for nonoffspring.
much more basic reasons than helping behavior. This orga-
Many have proposed that inclusive fitness and reciprocal
nization adaptively generates responses from perception,
altruism explain altruism (Axelrod 1984; Hamilton 1964;
using the same representations to code objects and their as-
Maynard Smith 1964; Trivers 1971). Because altruism and
sociated actions. This is computationally more efficient in
empathy are considered related, inclusive fitness and recip-
terms of the way the information is processed and the stor-
rocal altruism are expected to explain empathy. However,
age space it requires. It also facilitates appropriate re-
inclusive fitness and reciprocal altruism were developed to
sponses to the environment (like ducking away from a pro-
explain how behaviors that appear “altruistic” could have
jectile or attacker). Such behavioral tendencies are the
evolved (like taking care of someone else’s offspring or
keystone of reproductive success.
alerting your neighbors to the presence of a predator).
The general benefit of a response-oriented nervous sys-
Inclusive fitness, reciprocal altruism, and group esteem
tem laid the groundwork for a perception-action organiza-
are all complementary factors that additively increase the
tion. This organization was further refined in group-living
likelihood of helping behaviors. Indeed, empathy, helping,
animals, because social animals have as much a need to re-
and degree of closeness are correlated with decreasing ten-
spond with another individual with a matching response as
dencies from kin to close friends, acquaintances, and
they do to respond to another individual with an instru-
strangers (Cialdini et al. 1997), and altruistic behavior in
mental response. This change to the perception-action or-
experimental situations is directed at friends more than
ganization made possible all phenomena that rely on state-
neutral individuals (Sawyer 1966). But with our model, in-
matching or social facilitation, including empathy. Thus,
clusive fitness and reciprocal altruism did not drive the se-
affective resonance, state matching, emotional or affective
lection for empathy; they are additional benefits to a highly
empathy all rely on this transition. Basic information pro-
adaptive nervous system organization.
cessing components of empathy (such as effects of famil-
Perception-action mechanisms emphasize that percep-
iarity, similarity, and experience) were possible as long as
tion selects elements in the environment that require or
there were networks of neurons that changed from experi-
suggest a response by the subject. In group-living species,
ence. But later increases to the prefrontal cortex also aug-
objects that require a response are those that the subject re-
mented these processes to allow empathy to take place in a
lies upon to attain personal goals; these are usually friends
top-down manner, with more control, and in a broader
and relatives. Thus, nervous systems that respond automat-
range of situations. Subsequent sections examine the extent
ically with empathy to situations where they must respond,
to which perception-action processes exist across species
create the appearance of reciprocity, and maximize inclu-
and why these processes are adaptive.
sive fitness. Evidence for the effect of interdependence on
empathy, human children are more motivated to help in ex-
periments when there is a responsibility for the object’s dis-
2.1. Perception-action processes facilitate group living
tress (Chapman et al. 1987). In the primate literature, rec-
McDougall noted that empathy appears to exist in group-
onciliations between former opponents are much more
living animals, or those with the “gregariousness instinct,”
likely between kin and friends (de Waal & Yoshihara 1983;
because these animals are innately affected by the emotions
reviewed by Kappeler 1992). Species with cooperative kin
of others (McDougall 1908/1923). According to McDou-
relationships show higher levels of reconciliation between
gall’s theory, sympathy “is the cement that binds all animal
related individuals than nonrelated individuals (Aureli et al.
societies together, renders the actions of all members of a
1989; 1997; Demaria & Thierry 2001). In chimpanzees,
group harmonious, and allows them to reap some of the
where male alliances are very important for intra and inter-
prime advantages of social life” (McDougall 1908/1923,
group conflicts, reconciliation is higher among males than
p. 93).
females (de Waal 1986a; Goodall 1986b; but see Baker &
If one group member sees something dangerous, usually
Smuts 1994). In an experimental situation, macaque pairs
a predator, an alarm call is given and in most cases the group
trained to cooperate for food dramatically increase their
moves away from the source of danger en masse. Thus, the
conciliatory tendency (Cords & Thurnheer 1993).
alarm of one individual alarms others. This phenomenon is
The literature suggests that empathy and helping are de-
empirically documented for many species, including ground
termined by the subject’s ability to help. Human subjects
squirrels (e.g., Sherman 1977), birds (e.g., Powell 1974), and
are more likely to help when the level of need or potential
monkeys (e.g., Cheney & Seyfarth 1985). Given this behav-
benefit to the object is higher (Aronfreed 1968; note that
ior, danger is more likely to be detected even though each
this is also when the probability of reciprocation by the ob-
individual spends less time on vigilance (Kenward 1978;
ject is highest, Gouldner 1960). Adult human subjects that
Powell 1974). The “more eyes” phenomenon allows indi-
are trait sympathetic volunteer to help a distressed object
viduals to spend more time on other activities that promote
when they expect to have control over the procedure or ex-
reproductive success such as feeding and finding mates. The
pect to be able to help the object (Smith 1992). Thus, it may
evolutionary importance of detecting and responding to
be more accurate to consider helping behavior as the result
danger is evident in the general design of the nervous sys-
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Preston & de Waal: Empathy: Its ultimate and proximate bases
nate releasing stimuli, or rule-based behavior would not be
related to empathy, while those that share the perception-
action mechanism would. For example, fish schools could
rely on a general rule where each individual maintains an
equal distance to all neighboring individuals. If one indi-
vidual detects a predator and tries to move quickly away, it
would create mass violations to the rule and adjustments.
This would have the overall appearance of group alarm, but
would not be an example of empathic processing. This ex-
emplifies the need to understand mechanism in order to
categorize behavior.
Should we expect the mechanisms to be the same? In-
formation processing, brain structure, and brain design are
greatly conserved across species (Finlay & Darlington
1995; Krubitzer 1995). Moreover, there is direct behavioral,
physiological, and neurological evidence for perception-ac-
tion processes in monkeys, chimpanzees, and humans (re-
Figure 2. Social facilitation of drinking in captive hyenas (adapted
viewed in sect. 3). Finally, although there are surely differ-
from Glickman et al. 1997).
ences in the cognitive capabilities across species (discussed
in sect. 3), or in the phenomenology of empathy, percep-
tion-action processes are not generally accessible to con-
scious awareness. Therefore, the basic structures, mecha-
tem. Response circuits dedicated to the perception of neg-
nism, and application to social behavior are likely to be
ative emotions, especially fear, have been easy to locate rel-
shared at least across group-living mammals.
ative to positive ones (e.g., Adolphs et al. 1994; 1995; Ekman
et al. 1983; Miller et al. 1966; Scott et al. 1997).
The social facilitation of behavior also relies on the per-
2.2. Perception-action processes facilitate the mother-
ception-action mechanism, and is evident across group-liv-
offspring bond
ing animals. For example, hyenas live in tightly bound
The parent-child relationship both relies upon and is nec-
groups that live, forage, eat, and move together. In social fa-
essary to develop the ability of individuals to be affected by
cilitation experiments with hyenas in captivity, when one in-
the emotional state of others (as noted by others, including
dividual drinks, the probability that an observing individual
Darwin 1998/1872; McDougall 1908/1923; Plutchik 1987).
will drink in the next few minutes is 70%. Even a subject
Infants are emotionally affected by the state of their moth-
that was not actively attending is 20% more likely to drink
ers and mothers are emotionally affected by the state of
than in baseline conditions (Glickman et al. 1997, Fig. 2).
their offspring.
Similarly, hyena subjects successfully conditioned to avoid
a food resume eating it when placed with other group mem-
2.2.1. Effects of the mother on the infant. Continuous and
bers that eat the food (Yoerg 1991). The perception-action
coordinated emotional and physical contact between the
mechanism explains such examples of social facilitation.
mother and infant are thought to organize the emotion reg-
The vicariousness of activity, often seen in group-living
ulation abilities of the infant, which determine the emo-
animals, is also symptomatic of the innate response to emo-
tional competence of the individual (e.g., Brazelton et al.
tion in others. Anecdotally, wild dogs are described as nos-
1974; Deboer & Boxer 1979; Gable & Isabella 1992; Levine
ing, licking, squeaking, and jumping at each other before
1990; Stern 1974; 1977).
the onset of a hunting expedition (van Lawick-Goodall &
On a neurophysiological level, maternally-separated rat
van Lawick-Goodall 1971). Similarly, anecdotal accounts of
pups show reduced levels of growth hormone (GH) and a
rhesus macaques report that a severely distressed infant will
peripheral biochemical block between GH and the enzy-
often cause other infants to approach, embrace, mount, or
matic activity required for cell protein synthesis. This can
even pile on top of the victim; the distress seems to spread
be reversed with appropriate stimulation. After 24 hours of
to the other infants who then seek contact to soothe their
separation, the sleep of these rat pups is also disturbed, due
own arousal (de Waal 1996). This type of emotional conta-
to the lack of entraining interactions with the mother
gion is also the first stage of empathic responding in hu-
(Hofer 1995; 1999). Separation causes arousal and the re-
mans, exemplified in experiments where infants in a nurs-
lease of stress hormones in attached primate infants and
ery cry in response to other infants’ cries (Sagi & Hoffman
mothers (Levine 1990). Rhesus macaques raised without
1976; Simner 1971) and year-old children seek comfort af-
their mother lack the normal, adaptive relationship be-
ter witnessing the injury of another (Hoffman 1990; Zahn-
tween behavior and neurochemistry in response to stress
Waxler et al. 1992a).
(Kraemer & Clarke 1996). In humans, infants of depressed
There are a few main reasons not to reject the continuity
mothers have reduced left hemisphere activation (Jones et
of these phenomena. First, the behavioral repertoires of
al. 1998) and lack the normal increase in vagal tone between
mammals are superficially very similar. However, behaviors
3 and 6 months that is correlated with vocalizations and op-
of different species may appear similar, or achieve the same
timal neurological functioning (Field et al. 1995).
function, but may not share the same mechanism (“anal-
Behavioral development has also been shown to rely on
ogy” in evolutionary biology). This is especially likely for
the mother-infant relationship. Isolate monkeys are im-
species that diverged hundreds of millions of years ago,
paired at sending and receiving emotional expressions to
such as vertebrates and invertebrates. Cases that rely on in-
typically-developing conspecifics (Miller et al. 1967), a task
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Preston & de Waal: Empathy: Its ultimate and proximate bases
easily done by normally-developing individuals (Miller et
negative affect after referencing a mother with a fearful ex-
al. 1962; 1963). The expressive impairments of the isolate
pression (Klinnert et al. 1983; Sorce et al. 1985). The
animals has been compared to that of humans with autism,
mother’s emotion is adaptively perceived and incorporated
who are also impaired at the communication of affect (e.g.,
into the offspring’s actions without necessitating the same
Bemporad 1987; Harlow & Harlow 1966; Miller et al.
level of response (as in alarm) or direct experience (as re-
1967). Infants of depressed mothers are impaired at match-
quired by conditioning). Social referencing studies have
ing happy facial and vocal expressions (Lundy et al. 1997)
found negative emotions to affect the behavior of infants
and show less orientation and fewer facial expressions in re-
much more than positive ones. This is in accordance with
sponse to modeled happy and surprise expressions (Lundy
findings from other fields, and with the importance of alarm
et al. 1996).
and distress contagion on reproductive success.
We argue that the PAM subserves the ability of infants to
perceive and learn from the expressions of the caregiver.
2.2.2. Effects of the infant on the mother. It is also adap-
The actions and expressions of the mother are mapped onto
tive for the parent to be affected by the emotional state of
existing representations of the infant and generate actions
the infant. In the ethological literature, Eibl-Eibesfeldt
and expressions in response. This facilitates not only the in-
(1971/1974) postulates that the evolution of parental care
fant’s ability to understand the behavior of the mother, but
in birds and mammals created not only actions by the par-
also facilitates coordinated activity in the dyad, necessary
ent to care for offspring, but also concurrent actions by the
for the development of emotion regulation.
offspring to request care. Interactional views of develop-
Infants and their caretakers are thought to use their emo-
ment similarly postulate that the infant directs the mother’s
tional expressions to reinforce positive affect, transform
behavior as much as the mother directs the infant’s (Bell
negative affect, and provide breaks when arousal becomes
1968; 1971; Brazelton et al. 1974; Osofsky 1971; Wiesen-
too high (Malatesta & Haviland 1982; Tronick 1989). Such
feld & Klorman 1978; Yarrow et al. 1971). Smiling and cry-
responsiveness is thought to organize behavior (Campos et
ing by the infant are thought to modify the affective and be-
al. 1983) and create a sense of security and efficacy (e.g.,
havioral responses of their caregivers. Such behaviors signal
Bell & Ainsworth 1972). The coordinated activity between
the infant’s state, providing the impetus for attention and
caregiver and infant seems required for emotional regula-
action (Acebo & Thoman 1995; Bowlby 1958; 1969). Illus-
tion and control (Field 1994), which are in turn required for
trating the importance of infant-to-mother communication,
empathic competence throughout life (Ungerer 1990). A
a deaf female chimpanzee at a zoo lost a succession of in-
lack of coordinated activity may contribute to behavioral
fants despite intense positive interest because she did not
problems associated with an inability to assess and control
correct positional problems (such as sitting on the infant, or
emotions, such as tantrums, poor impulse control, and risk-
holding it the wrong way) in response to soft distress calls
taking (Tronick 1989).
(de Waal 1982). What is the mechanism for such interper-
In humans, fear and personal distress lead to self-
sonal communication?
directed efforts and, thus, are prohibitive of empathy, sym-
Crying and smiling can induce autonomic arousal in the
pathy, and perspective taking (Eisenberg et al. 1994). Emo-
caregiver that simultaneously acts as an unconditioned
tion regulation problems are correlated with personal
stimulus to motivate a response and as the precursor stim-
distress and a lack of helping in preschoolers, older chil-
ulation for the response (Wiesenfeld & Klorman 1978).
dren, college undergraduates, and the elderly (Doherty
When rat pups are separated, they produce ultrasonic vo-
1997; Eisenberg et al. 1994; 1996; Eisenberg & Okun 1996,
calizations that instigate the mother to search for, retrieve,
respectively). Similarly, although albino rats press a bar to
and return the pups to the nest (Smotherman et al. 1978).
eliminate the distress of a hoisted animal, they do not press
Crying in human infants elicits high levels of maternal at-
a bar to eliminate the distress of a conspecific being
tention in postnatal weeks with high, continued levels of
shocked. The latter situation is interpreted as being too
maternal stimulation (Acebo & Thoman 1992). High levels
stressful for the subjects, precluding an empathic response
of crying associated with colic cause distress in parents (e.g.,
(Rice 1964). Thus, without emotional linkage, or the inter-
Liebman 1981; Meyer & Thaler 1971; Rowell 1978). Moth-
actions necessary to develop its capacities, infants cannot
ers are physiologically aroused when witnessing their own
learn to regulate their emotions and the development of
infant crying; they show an increase in heart rate and large
more advanced forms of empathy are compromised.
skin conductance responses. The crying of a strange infant
Emotional linkage can also teach offspring about their
elicits the standard orienting response (Wiesenfeld & Klor-
environment. If an infant is aroused by the display of emo-
man 1978).
tion in the parent (especially fear or distress), then the in-
Emotional contagion proximately guides the parent-off-
fant can use the mother’s reaction as an unconditioned stim-
spring relationship, increasing the success of both individ-
ulus to learn about danger. For example, if an infant
uals. If a similar emotion is elicited in the subject as in the
monkey is aroused by the arousal of a parent in the pres-
object, then tailored care is much more likely. Proper care
ence of a snake, it can learn to fear snakes without the need
increases viability of the offspring and, thus, the reproduc-
for a more costly direct experience (Mineka & Cook 1988;
tive success of the parent. Fulfilling the needs of the off-
1993; Mineka et al. 1984). Typically-developing 12-month-
spring also assuages the arousal of the caregiver and offsets
old children socially reference the mother in the face of am-
the unwanted attention from group members and preda-
biguity (Feinman 1982; Klinnert et al. 1983). When pre-
tors caused by an individual displaying distress.
sented with a loud toy in the lab, children this age approach
Although emotional displays can coordinate, regulate,
the toy if the mother smiles but approach the mother if she
and guide the parent-child relationship, care is often pro-
expresses fear. When infants approach a visual cliff, social
vided in the absence of such releasers. What is the mecha-
referencing to the mother determines whether or not the
nism for these acts of helping? The association between a
infant will cross (Sorce et al. 1985). These infants display
context and its outcome is facilitated by emotional arousal
8
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Preston & de Waal: Empathy: Its ultimate and proximate bases
(e.g., Corodimas & LeDoux 1995). Therefore, contagious
uli can be used to elicit empathy and help from nonoff-
distress from offspring to parent can act as an uncondi-
spring. A distressed chimpanzee, for example, who has just
tioned stimulus, motivating the parent to act before a stress-
lost a major battle will “pout, whimper, yelp, beg with out-
ful display erupts. For example, captive and wild ungulate
stretched hand, or impatiently shake both hands” in order
species approach their calves for nursing before a request
to solicit the consolatory contact of others (de Waal & Au-
is emitted (Murdock et al. 1983). Through empathy, the
reli 1996). Eibl-Eibesfeldt (1971/1974) argues that the in-
parent can also provide care when conditioned associations
fantile releasers of caregiving are used throughout adult
to personal experience dictate it necessary. The parents (in-
life, such as the use of a high-pitched voice or “baby names”
directly) and the offspring (directly) benefit because the
between lovers.
offspring’s needs are satisfied without the cost of unwanted
Why is it beneficial to extend innate releasing mecha-
attention and a stressful display.
nisms and care-giving beyond the parent-child relation-
Emotional displays can continue to indicate the needs of
ship? Because releasers elicit distress in the receiver
altricial offspring into adolescence. Distress vocalizations
through the PAM, they can initiate the actions of potential
that include sounds of crying and whining may signal ap-
allies and terminate the actions of predators and conspecific
peasement and recruit help. Temper tantrums, an extreme
attackers. It is mistaken to argue whether help is given for
example, are used by offspring to direct the behavior of the
the benefit of the object or to terminate the object’s aver-
caregiver after their needs diverge (Einon & Potegal 1994;
sive distress signal or the subject’s personal distress. Aver-
Trivers 1974). Tantrums that include “screaming, crouch-
sive signals evolved because, by definition, others want
ing, hurling self on ground, running and occasionally at-
them terminated. The comparative evidence below attests
tacking the mother” are common in young humans and
to the success of these signals in soliciting help from con-
chimpanzees (Einon & Potegal 1994). The temper tantrum
specifics (for a detailed review of the comparative data, see
endangers reproductive success by causing respiratory dis-
Preston & de Waal 2002).
tress, damage to the vocal folds, and involving self-inflicted
Given a perception-action view of empathy, these pro-
injury (Einon & Potegal 1994; Potegal & Davidson 1997),
cesses extend to the prediction and response to allies as well
but it can be a successful technique because the parent is
as competitors. The PAM can produce appropriate helping
averse to the loud display of anger (Potegal & Davidson
behaviors, as well as effective punishments. In both cases,
1997).
the subject accesses the object’s state and generates an ap-
The preceding evidence suggests that the emotional link-
propriate response. Associated representations of the ob-
age between parent and offspring has a profound effect on
ject and situation will determine whether the desired out-
reproductive success. It provides an unconditioned access
come is to produce or alleviate distress. The generation of
to the infant’s emotional state, and thus the need as well as
the state in the subject can be bottom-up or top-down. And
the motivation to help. It conditions offspring to know
both could occur simply with learned, conditioned re-
when and how to request care and conditions parents to
sponses that prove effective in producing the desired out-
know when and how to provide care. Thus, the direct emo-
come. However, there is a difference between the normal
tional link between individuals is highly adaptive for group-
phenomenon where the subject creates distress in the ob-
living individuals, especially those that provide extended
ject for self-defense, or to secure resources (like Machiavel-
care. This direct link also provides the basis for empathy
lian intelligence; Byrne & Whiten 1988), and the abnormal
and helping outside of these contexts.
phenomenon where the subject seeks to produce or witness
Phenomena that increase the reproductive success of rel-
high levels of distress in noninterrelated objects (like psy-
atives are the purview of inclusive fitness. However, in-
chopathy). The latter case is an impairment in the percep-
clusive fitness models would argue that the PAM evolved to
tion-action circuit for emotional states, addressed in section
indirectly increase the reproductive success of mothers
3.4.5, “Evidence from disorders of empathy.”
through offspring. According to our model, the PAM evolved
In summary, combining an ultimate and a proximate de-
because it is adaptive for basic responses to the environ-
scription of empathy greatly changes the argument for
ment, and for group living. Subsequently, the mechanism
adaptation, allows one to link different levels of empathy,
was exapted in altricial species to improve care of offspring,
and exhibits the inherent relationship among these levels.
and to develop emotion regulation and synchrony; which in
Data is presented in the following section to support the
turn are necessary for the proper development of empathy,
proximate model.
cognitive empathy, and helping behavior.
3. The proximate bases of empathy
2.3. Perception-action effects outside the mother-
offspring bond
The fact was overlooked that, in order to express it, the body
must in the last analysis become the thought or intention that it
Empathy may have a phylogenetic and ontogenetic basis in
signifies for us.
the emotional linkage between parent and offspring, but
Merleau-Ponty, Phenomenology of Perception (1962/1970,
empathy is exercised across the lifespan in many mammals.
p. 197).
How is empathy extended from these rudimentary forms of
emotional linkage?
The “Perception-Action Hypothesis” (a term from motor
Empathy in alarm and parent-offspring situations was
behavior) is grounded in the theoretical idea, adopted by
described as resulting from innate releasing stimuli. High
many fields over time, that perception and action share a
pitched sounds that resemble alarm calls or screams induce
common code of representation in the brain (reviewed by
fast action in situations of immediate physical danger, while
Allport 1987; Prinz 1987; 1992; 1997; Rizzolatti & Arbib
sounds that resemble crying induce action for less immedi-
1998). According to the perception-action hypothesis, per-
ate needs like food, comfort, and warmth. These same stim-
ception of a behavior in another automatically activates
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Preston & de Waal: Empathy: Its ultimate and proximate bases
one’s own representations for the behavior, and output from
mental and emotional state of the object by simulating the
this shared representation automatically proceeds to motor
object’s state internally (Carruthers & Smith 1996; Davies
areas of the brain where responses are prepared and exe-
& Stone 1995a; 1995b). Generally, the perception-action
cuted. This organization makes sense if perceptual systems
mechanism and simulation theory are not in conflict. Some
evolved to provide accurate information about the environ-
descriptions of the simulation process seem more explicit
ment to appropriately plan and guide movements (Prinz
and cognitive than a perception-action model would sug-
1992). These common codes are not restricted to physical
gest, but most postulate implicit as well as explicit processes.
movements, they include abstract, symbolic representa-
In the literature, simulation theory stands in contradis-
tions (Decety et al. 1997; Jeannerod 1994; Prinz 1997).
tinction to the theory-theory, which postulates that individ-
uals understand the world through theories that they de-
velop (Gopnik 1993; Gopnik & Wellman 1992). With the
3.1. Existing theories
PAM, the two theories are compatible; simulation theory is
Previous theoretical accounts of empathy have implicated
a description at a level between metaphor and mechanism
a perception-action model to varying degrees (Adolphs
that is interested in how the state of the object is imparted
1999; Boodin 1921; Brothers 1990; Levenson & Reuf 1992;
to the subject while theory-theory is a description at the
Lipps 1903; McDougall 1908/1923; Meltzoff & Moore
level of metaphor that is interested in the ways that these
1997). Lipps’ (1903) theory was an early proponent of
perceptions change during development (see Schulkin
the perception-action model in motor behavior and he ex-
2000, for a comparison of the two theories with respect to
plicitly applied the theory to empathic processes. Similarly,
mirror neurons).
McDougall stated, “sympathy is founded upon a special
The discovery of mirror neurons (di Pelligrino et al.
adaptation of the receptive side of each of the principal in-
1992) prompted a series of papers extending the possible
stinctive dispositions, an adaptation that renders each in-
function of these cells from the coding of simple motor acts,
stinct capable of being excited on the perception of the bod-
to the coding of other’s mental states and these cells were
ily expressions of the excitement of the same instinct in
suggested to provide evidence for the simulation theory of
other persons” (1908/1923, p. 95).
empathy (Adolphs 1999; Adolphs et al. 2000; Gallese &
In more recent history, Brothers (1990) suggested that
Goldman 1998; Iacoboni et al. 1999; Ruby & Decety 2001;
understanding the emotion of others entails to some degree
Williams et al., 2001; Wolf et al. 2001; literature reviewed
experiencing the emotion observed. This hypothesis was
by Motluck 2001). While mirror neurons alone cannot pro-
certainly correct, though it was not linked to the experi-
duce empathy at any level, they do provide concrete cellu-
mental empathy literature, and at the time had little back-
lar evidence for the shared representations of perception
ing from physiological and neurological evidence. Gallup
and action that were postulated by Lipps (1903) and Mer-
also suggested that information about the self is used to
leau-Ponty (1962/1970) and behaviorally demonstrated by
model the states of others. His “introspective” model seems
Prinz and colleagues (Prinz 1997).
implicitly more cognitive than the PAM since he did not see
Given the history of a perception-action theory of empa-
the object’s state as being mapped automatically onto the
thy that extends back at least to the beginning of the last
subject’s representations, and reserved the process for the
century, with small upsurgences along the way, the model
few species that exhibit theory of mind (Gallup 1998b).
seems to have had intuitive appeal to researchers looking
Less directly implicating perception-action processes, Lev-
for simple, mechanistic ways to instantiate empathy. The
enson and Reuf (1992) suggested that the heart-rate con-
theory has not yet enjoyed mass acceptance, however, for
cordance between subjects in affect communication para-
many reasons. The behaviorist and cognitive revolutions di-
digms could be the basis for empathy. This agrees with the
rected theory away from the level of mechanism. In addi-
PAM since similar states are induced in the subject and ob-
tion, folk psychology generally regards empathy as a phe-
ject, but does not include central nervous system compo-
nomenon reserved for humans. Given a lack of knowledge
nents.
of the mechanism, these approaches are appropriate. Now,
Based on extensive research, Meltzoff and colleagues
data in humans, nonhuman primates, and rodents support
propose the Active Intermodal Mapping