DecetyMeyer Empathy 2008

Development and Psychopathology 20 (2008), 1053–1080
Copyright # 2008 Cambridge University Press

Printed in the United States of America
doi:10.1017/S0954579408000503
From emotion resonance to empathic

understanding: A social developmental
neuroscience account
JEAN DECETYa AND MEGHAN MEYERb

a
University of Chicago; and b Stanford University School of Medicine
Abstract
The psychological construct of empathy refers to an intersubjective induction process by which positive and negative
emotions are shared, without losing sight of whose feelings belong to whom. Empathy can lead to personal distress or to
empathic concern (sympathy). The goal of this paper is to address the underlying cognitive processes and their neural
underpinnings that constitute empathy within a developmental neuroscience perspective. In addition, we focus on
how these processes go awry in developmental disorders marked by impairments in social cognition, such as autism
spectrum disorder, and conduct disorder. We argue that empathy involves both bottom-up and top-down information
processing, underpinned by specific and interacting neural systems. We discuss data from developmental psychology
as well as cognitive neuroscience in support of such a model, and highlight the impact of neural dysfunctions on social
cognitive developmental behavior. Altogether, bridging developmental science and cognitive neuroscience helps
approach a more complete understanding of social cognition. Synthesizing these two domains also contributes to a better
characterization of developmental psychopathologies that impacts the development of effective treatment strategies.
While enjoying a walk in the park with your son, teraction. For example, social psychologists re-
you suddenly notice a young woman with a sad gard empathy as a proximate factor motivating
expression on her face who is sitting on a bench prosocial behavior (Batson, 1991; Davis, 1994).
reading a letter. A wave of melancholy consumes Similarly, a large tradition in developmental sci-
you, and your son and you both express a wish to ence has been to study the onset and development
console the woman. This natural tendency to share of empathy, as some theorists suggest that empa-
and understand the emotions and feelings of oth- thy plays a crucial role in moral development,
ers in relation to oneself, whether one actually wit- motivating prosocial behavior and inhibiting ag-
nesses another person’s expression, perceived it gression toward others (e.g., Hoffman, 2001;
from a photograph, read about it in a fictive novel, Miller & Eisenberg, 1988). Indeed, empathy de-
or imagined it, refers to the phenomenological ex- velops from infancy, and by 2 years of age most
perience of empathy. children manifest prosocial helping responses’ to
Various domains of psychology suggest that others’ distress (Zahn-Waxler & Radke-Yarrow,
one function of empathy is to promote social in- 1990). In contrast, certain developmental disor-
ders, such as autism spectrum disorder (ASD)
and conduct disorder (CD) are marked by empa-
The writing of this manuscript was supported by NSF Grant thy deficits that likely influence their antisocial re-
BCS 0718480 (to J.D.). sponses to other’s distress, albeit with aloof apa-
Address correspondence and reprint requests to: Jean thy or active aggression, respectively.
Decety, Departments of Psychology and Psychiatry and
Center for Cognitive and Social Neuroscience, University
The link between empathy and social inter-
of Chicago, 5848 South University Avenue, Chicago, IL action likely derives from the relationship be-
60637; E-mail: decety@uchicago.edu. tween empathy and intersubjectivity. It has been
1053
1054 J. Decety and M. Meyer
postulated that empathy is a primary source of in- cess grounded in perception–action coupling
tersubjectivity, as the sense of shared experience and potentially underpinned by mirror neuron sys-
is a prerequisite for understanding what drives tems; (b) the ability to differentiate oneself from a
other people’s intentions, emotions, and motiva- perceived target, which relies on a sense of
tions (Gallagher, 2001; Meltzoff & Decety, agency, self-, and other awareness, and likely in-
2003; Trevarthen & Aitken, 2001). That is, inter- volves frontoparietal and prefrontal circuits; and
subjectivity, the ability to share the subjective (c) executive functions instantiated in the prefron-
states of others and resonate with their perspec- tal cortex (PFC), which operate as a top-down me-
tive, strongly relies on the ability to read (in the diator, helping to regulate emotions and yield
sense of reacting and understanding) others’ emo- mental flexibility (Figure 1). Taken together,
tions to determine their psychological state. In- drawing from these multiple sources of data help
deed, the absence of intersubjectivity deprives paint a more complete picture of the phenomeno-
individuals of the opportunity to develop proso- logical experience of empathy, as well as the re-
cial behaviors, empathy, and moral judgments spective mechanisms driving the phenomenon.
that are important byproducts of developing so-
cial cognition (Rochat & Striano, 1999).
A Clarification of Terms
In addition to intersubjectivity, empathy is also
phenomenologically tied to psychological con- Empathy is a loaded term, with various definitions
structs that may be partly innate in humans, offer- roaming the literature. Broadly construed, empa-
ing further evidence of the evolutionary basis of thy has been defined as an affective response
forming social bonds, and the role of empathy in stemming from the understanding of another’s
this process. Indeed, some of the basic building emotional state or condition similar to what the
blocks of empathy, such as emotion sharing and other person is feeling or would be expected to
an ecological sense of self, seem to be present feel in the given situation (Eisenberg, Shea, Carlo,
in the first days of life, suggesting a neurobio- & Knight, 1991). In line with this conception, em-
logically based predisposition for humans to be pathy can concede an interaction between two
connected to others (Rochat, 2002). These pro- individuals, with one experiencing and sharing
cesses prepare the individual for later empathic the feeling of the other (Feshbach, 1997). Other
connections through affective interaction with theorists more narrowly define empathy as one
others. Humans are indeed social animals, and vir- specific set of congruent emotions, those feelings
tually all of their actions are directed toward or are that are more other focused than self-focused (Bat-
produced in response to others (Batson, 1990). son, Fultz, & Schoenrade, 1987). Similarly, ac-
Humans rely on others for survival and are en- cording to Hoffman (2000), empathy refers to
dowed with a motivation to form and maintain the psychological processes that allow a person
strong interpersonal relationships, what Baumeis- to experience feelings more congruent with an-
ter and Leary (1995) have termed “the need to other’s situation than with his own situation.
belong.” Many developmental theories highlight the
Recent data from cognitive neuroscience also role of empathy in moral development, suggest-
offer new insights regarding the neural mecha- ing that when humans experience others’ emo-
nisms and brain areas that underpin empathy tions of distress they are motivated to respond
(Decety & Jackson, 2004, 2006; Decety & with prosocial help (Eisenberg, Spinrad, &
Lamm, 2006; Leiberg & Anders, 2006). The Sadovsky, 2006). However, whether experienc-
goal of this paper is to address the underlying cog- ing others’ emotional states entails prosocial re-
nitive–neural architecture that instantiates empa- sponding is unclear. During perspective-taking
thy and to highlight the dysfunction of these pro- tasks (using cognitive means to adopt another
cesses in developmental disorders marked by person’s point of view), social psychological re-
social–cognitive impairments. Based on empiri- search demonstrates that when individuals imag-
cal findings from cognitive neuroscience and de- ine how the other person would feel in a given
velopmental science, we argue that a number of situation versus how they would feel in the
components contribute to the experience of same situation, different emotions arise: the indi-
empathy: (a) affective sharing, a bottom-up pro- viduals are prone to feel sympathy for the other in
From emotion resonance to empathic understanding 1055
Figure 1. Schematic representation of bottom-up (i.e., direct matching between perception and action) and
top-down (i.e., regulation and control) information processes involved in empathy. These two levels of pro-
cessing are interrelated. The low level, which is automatically activated (unless inhibited) by perceptual in-
put, accounts for emotion sharing. Executive functions, implemented in the prefrontal cortex, serve to reg-
ulate both cognition and emotion, notably through selective attention and self-regulation. This metalevel is
continuously updated by bottom-up information, and in return controls the lower level by providing top-
down input. Thus, the top-down regulation, through executive functions modulates low levels and adds flex-
ibility, making the individual less dependent on external cues. The metacognitive feedback plays a crucial
role in taking into account one’s own mental competence in order to react (or not) to the affective states of
others.
the former, whereas the latter can lead to personal Here we will consider empathy as a kind of in-
distress, that is, a self-oriented aversive emotional duction process by which emotions, both positive
response such as anxiety or discomfort (Batson, and negative, are automatically shared. Empathy
Early, & Salvarani, 1997). Personal distress can be the source of an emotional response ema-
may lead an observer to relieve her own stress, nating from the self and directed to the other, a
and not necessarily help the other. Thus, it seems conceptualization congruent with many scholars
that the cognitive means used to assess an auto- (see Table 1). It is important that such a definition
matic shared affective state with another’s distress stresses the distinction between empathic concern
influences the likeliness to respond prosocially. and personal distress, both of which spring from
In the following sections, we review the affective empathy but have different goals and conse-
and cognitive components that give way to empa- quences. Furthermore, we will consider the con-
thy, reviewing first the automatic proclivity to struct of empathy within an overarching concep-
share emotions with others, and the cognitive tual framework. This framework suggests that
process of perspective taking and executive con- empathy involves parallel and distributed pro-
trol, which allow individuals to be aware of their cessing in a number of dissociable neurocompu-
intentions and feelings and keep separate self and tational mechanisms (Figure 1). Shared neural
other perspectives. circuits, self-awareness, mental flexibility, and
Table 1. Definitions of empathy provide a more comprehensive understanding

of empathy and related emotions, which also
† The ability to put oneself into the mental shoes of has the potential for generating new hypotheses
another person to understand her emotions and regarding social–cognitive disorders and thus
feelings (a form of simulation or inner imitation; contributes to better treatment and intervention
Goldman, 1993)
† A complex form of psychological inference in in developmental psychopathology.
which observation, memory, knowledge, and
reasoning are combined to yield insights into the
thoughts and feelings of others (Ickes, 1997) Emotion Sharing
† An affective response more appropriate to
someone else’s situation than to one’s own The automaticity of emotion sharing
(Hoffman, 1975)
† An other-oriented emotional response congruent Bodily expressions help humans and other ani-
with the other’s perceived welfare (Batson, Sager, mals communicate various types of information
et al., 1997) to members of their species. Specifically, emo-
† An affective response that stems from the tional expression and perception play pivotal
apprehension or comprehension of another’s
emotional state or condition and that is similar to roles in human social interaction (Schulkin,
what the other person is feeling or would be 2005). Emotions are short-lived psychological–
expected to feel in the given situation (Eisenberg, physiological phenomena that represent efficient
2000) modes of adaptation to changing environmental
demands. It has long been suggested that emo-
Note: These definitions point to an emotional experience
that is more congruent with another’s situation than with tion expression is an evolutionary adaptation
one’s own. Another important aspect of the construct of em- that facilitates survival (Darwin, 1872). Such a
pathy is that it must involve some sort of self–other differ- claim is supported by the observation that rules
entiation, which makes it distinct from related reactions
such as emotional contagion. govern emotional expressions, which can be
elicited by simple stimuli, as in the example of
disgust in the presence of bitter taste, as well as
emotion regulation constitute the basic macro- the speculation that detection of emotional ex-
components of empathy, which are mediated by pression offers clear adaptive advantages, par-
specific and interacting neural circuits, including ticularly in the formation and maintenance of so-
aspects of the PFC, insula, limbic system, and cial relationships.
frontoparietal networks. Consequently, this Emotional expression not only informs an in-
model assumes and predicts that dysfunction in dividual of another’s subjective (and physiologi-
each of these macrocomponents may lead to an cal) experience but also serves as a sort of social
alteration of the experience of empathy, and glue maintaining emotional reciprocity among
correspond with selective social cognitive disor- dyads and groups. Emotional contagion, defined
ders depending on which aspect is disrupted as the tendency to automatically mimic and
(Decety & Moriguchi, 2007). synchronize facial expressions, vocalizations,
In the following sections, we marshal sup- postures, and movements with those of another
port for this model by discussing first the be- person and, consequently, converge emotionally
havioral evidence and then the putative neural with the other (Hatfield, Cacioppo, & Rapson,
mechanisms that underpin them. We also sug- 1994) is a social phenomenon of shared emotional
gest that inadequacies in these mechanisms expression that given its automaticity occurs at a
may help account for various social–cognitive basic level outside of conscious awareness.
disorders. These sections are organized accord- From infancy, complex facial motor patterns
ing to each major aspect that contributes to permit infants to match facial emotion expres-
empathy: emotion sharing, self- or other aware- sions with others (e.g., Field, Woodson, Green-
ness, and executive control and emotion regula- berg, & Cohen, 1982; Haviland & Lelwica,
tion. We conclude by speculating on the conse- 1987). Very young infants are able to send emo-
quences of the experience of empathy in moral tional signals and to receive and detect the emo-
reasoning. We believe that combining develop- tional signals sent by others. Shortly after birth,
mental science with cognitive neuroscience can healthy infants convey facial expressions of
interest, sadness, and disgust (Field, 1989). Like- Table 2. Classification of three basic
wise, discrete facial expressions of emotion have categories of subjective experiences
been identified in newborns, including joy, inter-
est, disgust, and distress (Izard, 1982). These find- † Feelings correspond to the perception of private
ings suggest that subcomponents of full emo- experiences such as pain, hunger, or frustration.
tional expressions are present at birth (Table 2), This category of subjective experiences in general
terminates following particular actions such as
supporting the possibility that these processes feeding for hunger, comfort for pain, or fulfilling a
are hard wired in the brain. It has been suggested goal for frustration.
that infant arousal in response to feelings, affects, † Affects qualify the perception of a general mood
and emotions signaled by others serves as an or perceived private tone that exists as a
instrument for social learning, reinforcing the background to both feelings and emotions.
Affects are diffused and protracted in comparison
significance of the social exchange, which then to feelings. They fluctuate along a continuum
become associated with the infant’s own emo- from low to high tone.
tional experience (Nielsen, 2002). Consequently, † Emotions are the actual observable expressions of
infants would come to experience emotions as feelings and affections by invariant movement
shared states and learn to differentiate their own dynamics, postures, and facial display as in the
expressions of pain, joy, disgust, sadness,
states, in part, by witnessing the resonant re- surprise, and anger.
sponses they elicit in others. This automatic emo-
tional resonance between other and self provides Note: Rochat and Striano (1999) introduced a useful classi-
the basic mechanism on which social cognition in fication of three basic categories of subjective experiences
which are often confused in the literature, and which in-
general and empathy in particular later develops. clude feelings, affects and emotions.
Infant affective resonance manifests in infant
cry reactions to peer crying. One-day-old infants
selectively cry in response to the vocal character- tential result of empathy) may reflect activation of
istics of another infant’s cry, a finding that led to brain processes that mediate social attachments
the speculation that from birth infants are en- (Panksepp, 1986). By the first months of infant-
dowed with an innate precursor of empathic dis- hood, infants recognize and mimic the distinct
tress (Hoffman, 1975). Moreover, infants ex- emotions of their mothers, a behavior that ulti-
posed to newborn cries cry significantly more mately facilitates attachment (Haviland & Leli-
often than those exposed to silence and those ex- vica, 1987). This resonance or echoing of affect,
posed to a synthetic newborn cry of the same in- feelings, and emotions that takes place in the re-
tensity (Sagi & Hoffman, 1976). The finding ciprocal interaction between infants and their
demonstrates that infants’ auditory perception of caretakers is a necessary element for the develop-
another’s aversive affective state elicits the same ment of empathy and advanced social cognition
distressful emotional state in the self. Importantly, (Rochat & Striano, 1999).
this reaction exists before infants develop a sense The primary source of intersubjectivity im-
of others as physical entities distinct from the self pacts the quality of the infant’s affective state.
(Hastings, Zahn-Waxler, & McShane, 2006). For example, 3-month-old infants of depressed
This convergence between the self and other’s mothers are less inclined to match emotional states
aversive affective experience reflects the instan- with their mother than 3-month-old infants of
tiation of the initial building block that precedes nondepressed mothers. For instance, depressed
the experience of empathy: a behavior matching mothers and their infants synchronize negative ex-
response to other’s emotional states. pression states more frequently than nondepressed
Infants experience emotion contagion through mothers and their infants (Field, Healy, Goldstein,
interaction with their caretakers. Such a behavior & Guthertz, 1990). This seems to indicate that un-
scaffolds what Bowlby (1958) termed attach- der normal conditions, mothers stimulate and
ment, that is, the inclination to seek proximity to arouse their infant while modulating their infant’s
another person and feel secure in the presence behavior. Through this process, mother and in-
of that person. Attachment theory fits neatly fant’s emotional expression synchronize. Emo-
with evolutionary theory, which contends that tional unavailability and affective unresponsive-
kin-related altruism and reciprocal altruism (a po- ness may lead to the lack of such emotional
modulation among the depressed mother–infant show mixed success, and furthermore, research-
dyad. The greater matching of negative emotion ers of the reproduced studies interpret the infants’
among depressed mother–infant dyad likely re- interactive behaviors as nothing more than social
flects experienced emotion contagion of negative contingency outside of intersubjectivity (for a re-
affect. This interpretation is in line with findings view, see Rochat, 1999).
related to atypical autonomic arousal in anxiously In sum, the developmental data suggest that
attached children, a likely aftermath attachment the mechanism subserving emotion (as the
style of infants raised by depressed mothers. Au- observable expressions of feelings and affects)
tonomic arousal is associated with degree of facial sharing between infant and caretaker is immedi-
mimicry, with anxiously depressed children ately present from birth. Newborns are innately
showing increased arousal in response to negative and highly attuned to other people and motivated
facial expressions (Rogeness, Cepeda, Macedo, to socially interact with others. From the earliest
Fischer, & Harris, 1990). months of their lives, infants engage with other
Infants of healthy, nondepressed mothers people and with the actions and feelings ex-
show similar behaviors to the infants of depressed pressed through other people’s bodies (Hobson,
mothers in experiments using perturbation tests in 2002; Rochat & Striano, 2002). Such a mecha-
which researchers disrupted the flow of contin- nism is grounded in the automatic perception–ac-
gent expression modulation between healthy tion coupling of sensorimotor information, which
mothers and infants. In the still or blank face seems present at birth in some form. This mimicry
test (Tronick & Weinberg, 1997) a mother who between self and other is critical for many facets
previously established a protoconversational of social functioning. For instance, it facilitates at-
flow with her infant arrests her expression, and tachment and provides information about the oth-
looks to the infant without a response to the in- er’s emotional state. Mimicry also constitutes a
fant’s behavior. Infants show several petitions primary source of interpersonal engagement
for communication via smiling, vocalizing, and with others, what has been termed primary inter-
gesturing. When the mother continues to adopt subjectivity (Gallagher & Meltzoff, 1996; Galla-
a “still face,” the infants show eye contact avoid- gher, 2004). This mechanism provides the foun-
ance and distress, much like the infant’s reactions dation for understanding that others are “like
to depressed mother’s despondent affective state. me,” and underlie the development of theory of
Results from the still face perturbation test mind and empathy for others (Meltzoff & Decety,
have been replicated, however, using a double- 2003). In the following section, we discuss in de-
video DTV link so that infants who are a few tail the mechanism that drives emotional sharing
weeks old and mothers could communicate live and mimicry, the direct link between perception
(Weinberg & Tronick, 1996). After rhythmic and action.
communication stabilized, a 1-min recording of
the mother’s behavior was rewound and re-
Perception–action coupling mechanism
played. In this case, the mother’s behavior was
and the mirror neuron system
no longer contingent with the infant’s move-
ments. The infants intermittently tried to interact The automatic mapping between self and other is
with the taped behavior, and showed confusion supported by considerable empirical literature in
when the mother failed to respond with similar the domain of perception and action, which has
timing or appropriate expression, and eventually been marshaled under the prominent common-
showed prolonged distress and avoidance. It is of coding theory. This theory claims that somewhere
interest that replay of the infant’s behavior to the in the chain of operation that leads from percep-
mother caused the mother to feel uncomfortable, tion to action, the system generates certain deriva-
and verbal reports demonstrate that she worried tives of stimulation and certain antecedents of
that the infant was unable “to connect.” It should action that are commensurate in the sense that
be noted that many scholars remain skeptical of they share the same system of representational di-
such findings related to early infant intersubjec- mensions (Prinz, 1997). The core assumption of
tivity as measured by video dialogue between in- the common coding theory is that actions are
fant and mother. Attempt to replicate these results coded in terms of the perceivable effects (i.e.,
the distal perceptual events) they should generate. motor area, and the cerebellum. Recent neuro-
Performing a movement leaves behind a bidi- imaging experiments demonstrate that the mir-
rectional association between the motor pattern ror–neuron system is flexible, and that experi-
it was generated by and the sensory effects that ence and motivation modulate its functioning.
it produces. Such an association can then be For instance, regions that belong to the mirror–
used backward to retrieve a movement by antici- neuron system showed greater hemodynamic re-
pating its effects (Hommel, Musseler, Aschersle- sponse when hungry participants were pre-
ben, & Prinz, 2001). These perception–action sented with videos of people grasping food. In
codes are also accessible during action observa- contrast, decreased activity was detected in these
tion, and perception activates action representa- regions when participants were in a satiated state
tions to the degree that the perceived and the rep- (Cheng, Meltzoff, & Decety, 2007). In addition,
resented actions are similar. Such a mechanism a number of neuroimaging studies have shown
has also been proposed to account for emotion that similar brain areas, pertaining to the same
sharing and its contribution to the experience of network are reliably activated during imagining
empathy (Decety, 2002; Decety & Jackson, one’s own action, imagining another’s action,
2004; Preston & de Waal, 2002). In the context and imitating actions performed by a model
of emotion processing, it is posited that percep- (Decety & Chaminade, 2003; Decety & Grèzes,
tion of emotion activates in the observer the 2006). For instance, a similar neural network is
neural mechanisms that are responsible for the engaged when individuals observe or imitate
generation of similar emotion. It should be noted emotional facial expressions (Carr, Iacoboni, Du-
that a similar mechanism was previously pro- beau, Mazziotta, & Lenzi, 2003). Within this net-
posed to account for emotion contagion. Indeed, work, there is greater activity during imitation,
Hatfield et al. (1994) argued that people catch the compared with observation of emotions, in pre-
emotions of others as a result of afferent feedback motor areas including the inferior frontal cortex,
generated by elementary motor mimicry of as well as in the superior temporal cortex, insula,
others’ expressive behavior, which produces a si- and amygdala. Such shared neural circuits reflect
multaneous matching emotional experience. an automatic transformation of other people’s be-
Neurophysiological evidence for this percep- havior (actions or emotions) into the neural repre-
tion–action coupling comes from electrophysio- sentation of one’s own behavior, and provides a
logical recordings in monkeys in which a unique functional bridge between first and third person
class of visuomotor neurons have been found in perspectives, culminating in empathic experi-
the ventral premotor and posterior parietal corti- ence (Decety & Sommerville, 2003; Sommer-
ces. These neurons, called mirror neurons, are ville & Decety, 2006).
active during a specific motor action and the The perception of other people in pain has re-
perception of the same action made by another in- vealed to be of particular importance for the in-
dividual (Rizzolatti, Fogassi, & Gallese, 2001). vestigation of the neural mechanisms underlying
Evidence for the existence of mirror neurons in empathy. Pain is a window through which one
humans is more indirect, and principally relies can obtain a detailed view of the cognitive and
on functional neuroimaging studies that indicate neurophysiological mechanism underlying the
that the neural circuits involved in action execu- experiences of empathy and sympathy. The per-
tion overlap with those activated when actions ception of pain in others thus constitutes an eco-
are observed (Blakemore & Decety, 2001; Dec- logically valid way to investigate the mecha-
ety & Grèzes, 2006), as well as transcranial nisms underpinning the experience of empathy
magnetic stimulation (TMS) and motor-evoked for two main reasons: first, most humans under-
potentials (MEP) studies that show changes in stand what is “pain”; it is a common and universal
the excitability of the observer’s brain regions experience; and understands what are its physical
that encode the execution of observed actions and psychological manifestations; second, we
(Fadiga & Craighero, 2004). This shared neural have good knowledge about the neurophysio-
network for action production and observation logical pathways that are involved in processing
includes the premotor cortex, the inferior frontal nociceptive information that include the somato-
gyrus, the parietal lobule, the supplementary sensory cortex, the supplementary motor area
(SMA), the anterior midcingulate cortex (aMCC), Mirror neuron dysfunction in ASD
the insula, the periaqueductal gray (PAG), and
thalamus. Numerous functional magnetic reso- Burgeoning research efforts suggest that an
nance imaging (fMRI) studies have shown that aberrant mirror neuron system may contribute to
when we perceive other people in pain, the motor and social problems experienced in ASD.
neural circuits underpinning the processing of Research with humans using TMS demonstrates
first-hand experience of pain are activated in selective changes in the amplitude of the MEPs
the observer (for a meta-analysis, see Jackson, (M1) during action observation (e.g., Fadiga, Fo-
Rainville, & Decety, 2006). In one recent study, gassi, Pavesi, & Rizzolati, 1995). To build on this
typically developing middle school-aged chil- finding, TMS was applied over the motor cortex
dren were scanned while observing dynamic vi- of adults with ASD and matched healthy controls.
sual stimuli depicting other people in pain (Dec- Compared to the controls, individuals with ASD
ety, Michalska, & Akitsuki, 2008). Results showed significantly less M1 amplitude change
show that neural circuits subserving the process- during the observation of transitive, meaningless
ing of nociceptive information are recruited by finger movements (Theoret et al., 2005). In con-
the sight of other people in pain (Figure 2). trast, observation of the finger movements in con-
Such a pattern of activation in children should trol subjects selectively modulated the excitability
not be surprising given the behavioral and phys- of the motor cortex in areas delivering signals to
iological data that document that affective shar- the muscles concerned with the observed action.
ing and vicarious emotional arousal, especially The weaker M1 modulation in individuals with
in response to others distress, is hard wired ASD suggests that the less mirror neuron activa-
and functional very early in life (e.g., Eisenberg tion in the motor cortex may be partly responsi-
& Eggum, 2008; Hoffman, 2000). This rudi- ble for a cascade of deficits in social cognition.
mentary capacity for resonating with the pain The fMRI experiments are in line with these
of others may trigger empathic distress in the ob- TMS findings, and indicate abnormal activation
server, and provides the affective and motiva- of mirror neuron systems during imitation in
tional base for moral development (Hoffman, adults with Asperger syndrome (Nishitani, Avi-
1982). kainen, & Hari, 2003) and reduced functional
It can be speculated that the perception– connectivity in mirror neuron system areas (Vil-
action coupling physiological mechanism is al- lalobos, Mizuno, Dahl, Kemmostsu, & Muller,
ready present at birth and develops gradually 2004). In attempt to examine a potential link be-
through experience and exposure to actions per- tween mirror neuron dysfunction and develop-
formed by self and others (Lepage & Theoret, mental delay of social cognitive skills, one
2007). This will account for neonate imitation fMRI study found a lack of activation in the
as demonstrated by the work of Meltzoff and inferior frontal gyrus (a key mirror neuron area)
Moore (1997). Recent empirical findings offer in children with ASD compared to controls dur-
evidence for a mirror neuron system encoding ing the observation and imitation of basic facial
perceived and executed human action in the emotion expression (Dapretto et al., 2006). How-
child’s developing brain. For instance, one ever, this finding was recently challenged by
study recorded electroencephalographic signals Bastiaanen, Thioux, and Keysers (2008, April),
via intracranial electrodes from a 36-month-old who scanned a group of 17 adults with ASD dur-
child with epilepsy while the infant observed an ing the observation of dynamic facial expres-
experimenter either drew with his right hand or sions, including disgust. The authors found that
kept his right hand still (Fecteau et al., 2004). ASD participants activate their mirror system
Cortical areas responding to the observation not less, but more strongly than controls when
of biological movements partially overlapped observing dynamic facial expressions.
with those that were active during the execution Structural neuroanatomical evidence also im-
of the same movements. An electrophysiologi- plicates aberrations in mirror neuron systems in
cal study demonstrated that the neural response ASD. One morphometric study reported locally
to the processing of biological motion was in diminished gray matter in adults with high-func-
place by 8 months (Hirai & Hiraki, 2005). tioning ASD in areas incorporated in the mirror
Figure 2. In this fMRI study, 17 typically developing children (9 + 1 years) were scanned while presented
with short dynamic (2.2-s duration) visual stimuli depicting painful and nonpainful situations (Decety et al.,
2008). These situations involved either (a) a person whose pain was caused by accident or (c) a person whose
pain was intentionally inflicted by another individual, as well as situations without any pain with one or two
agents for baseline. Consistent with previous fMRI studies of pain empathy with adults, the perception of
other people in pain in children was associated with increased neurohemodynamic activity in the neural cir-
cuits involved in the processing of first-hand experience of pain, including the insula, somatosensory cortex
(not shown), the aMCC, PAG, and SMA. (b) It was important that when children observed an individual
harming another, regions of the prefrontal cortex that are consistently involved in representing social inter-
action and moral behavior such as the temporoparietal junction (not shown), (d) the paracingulate cortex
(PCC), and orbitofrontal cortex (OFC) were also recruited. Of interest, children indicated in the postscan
debriefing that they thought that the situations in which pain was caused by another person were unfair,
and they asked about the reason that could explain this behavior.
neuron system compared to controls matched for problems engaging in intersubjective transactions
gender, age, intelligence quotient, and handed- and displays of empathic responding. It should be
ness (Hadjikhani, Joseph, Snyder, & Gager- noted, however, that in the tables included in the
Flushber, 2005). Cortical thinning of the mirror paper, not only mirror neuron cortical areas, but
system was correlated with the severity of ASD all areas of the brain, show a significant reduction
symptoms (as measured scores on the Autism Di- of gray matter. Thus, one needs to be cautious
agnostic Interview—Revised), and cortical thin- with these new findings, as cortical thinning
ning was also seen in areas engaged in emotion may not be specific to areas where mirror neurons
recognition and social cognition. Thus, irregular are located. In fact, an earlier study using magne-
thinning of cortical areas that implement mirror toecephalography failed to find any difference in
neurons and the broader network of cortical areas motor cortex activation between individuals with
subserving social cognition may contribute to the ASD and healthy controls while observing action
emotional deficits characteristic of autism, such as (Avikainen, Kulomaki, & Hari, 1999), a result
that is in contradiction with the study by Theoret tion of specific facial muscles in response to view-
and colleagues (2005). ing other people’s facial expressions. Facial mimi-
Perhaps more convincing evidence of anom- cry has been defined narrowly as the congruent
alies in the mirror neuron system in ASD derives facial reactions to the emotional facial displays
from EEG studies that examine mu rhythm in sen- of others, and is thus an expressive component
sorimotor areas. Robust evidence suggests that the (Hess & Blairy, 2001). More broadly construed,
magnitude of mu rhythm in sensorimotor areas is emotion contagion is an affective state that
strongly suppressed during the execution and ob- matches the other’s emotional display. Thus, fa-
servation of an action in adults (e.g., Muthuku- cial mimicry can be conceived of as a physical man-
maraswamy, Johnson, & McNair, 2003) and typi- ifestation of emotion contagion, and it occurs at an
cally developing children (Lepage & Theoret, automatic level in response to viewing others’ emo-
2006). In children and adults with high-function- tions (Bush, Barr, McHugo, & Lanzetta, 1989).
ing ASD, however, mu rhythm suppression oc- Individuals with ASD are often reported to
curs when individuals observe their own action, lack automatic and spontaneous mimicry of facial
however it fails to suppress during the observation expressions. A recent study measured adolescents
of other persons’ action (Oberman et al., 2005), and adults with ASD and controls’ automatic and
suggesting dysfunction in mirror neuron systems. voluntary mimicry of emotional facial expres-
Moreover, this result did not significantly corre- sions via EMG recordings of the cheek and
late with age, implicating that this deficit mani- brow muscle regions while participants viewed
fests early and shows little improvement with still photographs of happy, angry, and neutral fa-
age. Bernier, Dawson, Webb, and Murias (2007) cial expressions (McIntosh, Reichmann-Decker,
extended these results to show that in individuals Winkelman, & Wilbarger, 2006). The cheek and
with high-functioning ASD, the degree of mu brow muscles of individuals with ASD failed to
wave suppression during action observation is as- activate in response to the videos, indicating that
sociated with behavioral assessments of imitation they did not automatically mimic the facial ex-
ability. That is, less mu suppression correlates pressions, whereas the muscles of the normally
with poorer imitation abilities, and is most robust developing controls showed activation. It is
for facial imitation skills. important that both groups showed evidence of
Together, these recent findings, which need successful voluntary mimicry. Difficulties in mi-
to be replicated, seem to suggest that dysfunc- micking other people’s emotional expression
tions of the mirror neuron system may hamper may thus prevent individuals with ASD from the
the normal development of self–other connect- afferent feedback that informs them of what others
edness, creating a cascade of deficient processes are feeling (Rogers, 1999). Indeed, in real-life sit-
that lead to social deficits, including empathy. uations, individuals with ASD are likely drawing
However, it is worth noting that this account is on distinct cognitive processing when gauging
still debated, and that the results from a recent others’ emotional states (Baron-Cohen, 2002).
fMRI study do not support a global failure of Other developmental disorders known for
the mirror neuron system in children with autism their motor deficits are less obviously tied to
(Hamilton, Brindley, & Frith, 2007). In the fol- problems with emotion sharing and empathy.
lowing section we consider the implications of For example, DCD is characterized by delayed
perception–action coupling deficits in a behav- motor development and weak motor skills, as
ior that is considered a manifestation of emotion well as poor social skills, including deficient
contagion, which is facial mimicry. empathy (Gillberg, 1992). It is plausible that
poor motor skills are the primary problem, be-
cause a child with motor deficits may be
Facial mimicry of emotions in children
shunned from social inclusion. Alternatively,
with ASD and developmental coordination
the child may purposefully engage him/herself
disorder (DCD)
in activities beyond the realm of physical activ-
An effective means to measure the role of percep- ity, for example, indulge in mathematics. Thus,
tion–action coupling in emotion sharing is via weak social skills may develop by default as
electromyography (EMG) recording of the activa- much of social interaction relies on motor
skills, especially in childhood. However, chil- tional state, this process only accounts for what
dren with DCD show information processing has been termed “motor empathy,” or “empathic
deficits, specifically in visual–spatial process- mimicry.” However, that the observation of an
ing (Wilson & McKenzi, 1998). Such a weak- emotion elicits the activation of analogous motor
ness would influence perception–action cou- representation in healthy observers, begs the
pling of emotional expression. Therefore, the question why there is not complete overlap be-
mechanism underlying their difficulty in coor- tween internally generated and externally engen-
dinating movements may also contribute to dered motor representations.
their inability empathize. In a complete empathic experience, observers
One study tried to tease out the nature of the must be able to separate themselves from others
relationship between motor skills and social and have some minimal mentalizing ability.
skills in children with DCD (Cummins, Piek, & This aspect is a landmark of mature empathic ex-
Dyck, 2005). In a sample of 39 children with perience (Eisenberg et al., 2006; Zahn-Waxler &
DCD and 39 normally developing children, chil- Radke-Yarrow, 1990). Affective sharing must be
dren with motor problems performed worse on modulated and monitored by the sense of whose
scales that measured the capacity to recognize feelings belong to whom (Decety & Jackson,
static and dynamic facial expressions of emotion. 2004). Thus, self-awareness generally and agency
What is more, when visuospatial processing was in particular are crucial aspects in promoting a
controlled, this difference remained; thus, the prosocial regard for the other rather than a desire
child’s motor ability was a significant predictor to escape aversive arousal. Phenomenologically
of social behavior. Children with DCD’s motor speaking, self-awareness pertains to the embod-
impairments may negatively influence their abil- ied, and contextually embedded first-person point
ity to calibrate sensorimotor information about of view in subjective experience. In a similar vein,
their own body, and thus hinder activation of research in the neurosciences and developmental
shared motor responses between self and other science use the term agency to describe the ability
during interactions of emotion expression. to recognize oneself as the agent of an action,
The shared neural representations account thought, or desire, which is crucial for attributing
suggests that problems with one’s own motor a behavior to its proper agent.
or body schematic system may undermine capac- Developmental work demonstrates that infants
ities for understanding others. Consequently, it is come into the world with an ecological sense of
possible that developmental problems involving self, that is, the self as perceived in relation to
sensory–motor processes may have an effect on the physical environment (Neisser, 1991). The
the capabilities that make up “primary intersub- ecologic sense of self is analogous to what phe-
jectivity,” or the ability to react contingently to nomenologists term, prereflective self-awareness,
others’ emotional expressions (Trevarthen & or the subjective, qualitative “feel” of entertaining
Aitken, 2001), and therefore the child’s ability experiences (Gallagher, 2000). An implicit, eco-
to resonate emotionally with others. It thus seems logic sense of self develops from birth, prior to
plausible that the defects in social and sensory– an explicit (conceptual) manifestation of self-
motor problems in ASD and DCD may, in part, knowledge by the second year, and this sense of
reflect a disturbed motor representation matching self is discriminated from the sense of others (Ro-
system at the neuronal level. This speculation not chat & Striano, 2000). By 2 months, infants be-
only helps explain problems in primary inter- come incrementally systematic and deliberate in
subjectivity, but also the other sensory–motor the exploration of their own body and the percep-
symptoms of autism: oversensitivity to stimuli, tual consequences of self-produced action. For ex-
repetitious and odd movements, and possibly, ample, infants delineate between perceptual
echolalia (Gallagher, 2004). events that are self-generated or not self-gener-
ated. In one study, Rochat and Hespos (1997a)
tested whether newborn infants within 24 hr of
Self- and Other Awareness
birth discriminate between double touch
Although emotion contagion provides the obser- stimulation specifying themselves and external
ver with direct information of the other’s emo- (one way) tactile stimulation indicating nonself
objects via the robust rooting response manifest fants represent the other as “like me” (e.g., similar
by healthy infants from birth. Recording the to the self in some respect; Meltzoff & Brooks,
frequency of the rooting in response to external 2001). Further evidence suggests that infants
or self tactile stimulation indicated that newborns may productively use information from their
are inclined to manifest rooting responses almost own action capacities to understand the actions
three times more often in response to external of others (Woodward, Sommerville, & Guajardo,
compared to self-stimulation. The finding sug- 2001). Affective sharing among infants (reviewed
gests that from birth, infants discriminate be- above) also highlights the automatic overlap be-
tween intermodal invariants that specify self- tween other and self in infancy, which provides
compared to external stimulation. Thus, infants the basis for the development of intersubjectivity
develop an understanding of their own body as and social cognition.
a differentiated entity, situate, and agent in the A sense of agency can also be traced to in-
environment. fancy. From birth, infants learn to be effective
The study by Martin and Clark (1982) is also in relation to objects and events. Within hours
of special interest; they tested 1-day-old babies following birth, neonates can learn to suck in cer-
reactions to audiotapes of neonatal crying, the tain ways and apply specific pressures on a
crying of an 11-month-old, and the newborn’s dummy pacifier to hear their mother’s voice or
own crying. They not only replicated Simmer’s see their mother’s face (Decasper & Fifer,
results that infants cry in response to other in- 1980; Walton, Bower, & Bower, 1992). The find-
fant cries but also showed the more interesting ing suggests that infants manifest a sense of
trait that newborns did not respond to the sound themselves as agentive in the environment. Fur-
of their own cries. Another investigation, con- thermore, by 2 months of age, infants also
ducted by Dondi, Simion, and Caltran (1999), show positive affect, such as smiling and plea-
also demonstrated that newborns are able to sure expression, when they accomplish causing
discriminate their own and other infants’ cries. an auditory and visual event (by activating a mu-
These results suggest that there is some self- sic box by pulling a cord attached to a limb).
other distinction already functioning from birth. When the cord is then furtively disconnected
By 3 months of age infants become aware of from the box, hindering infants’ effectiveness,
their own body as a dynamic and organized entity they switch expressions from pleasure to anger
with specific featural characteristics. In another (Rochat & Striano, 2000).
series of studies, infants faced two on-line video In sum, the studies reviewed indicate that in
images presented on a split screen. Infants viewed addition to the early roots of perception–action
a split videotape screen showing contingent coupling leading to emotional expression, a
movements of the body from the waist down sense of self, agency, and other distinction
(Morgan & Rochat, 1997). One view showed in- emerge early in infancy. An ecologic sense of
fant’s their own legs as they would be specified via self develops immediately via proprioceptive
direct visual proprioceptive feedback, whereas the calibration of sensory–motor experiences. Both
other showed experimentally modified on-line this resonance mechanism and an ecological
view of their own legs. From 3 months of age, in- sense of self situate the individual in the social
fants look significantly longer at the unfamiliar environment and account for the duality of hu-
view of the legs that violates visual proprioceptive man beings who are strongly motivated to be
feedback. Thus, by this age infants experience an connected to others as well as to retain indepen-
intermodal calibration of the body, developing an dence and autonomy. In the following section,
intermodal body schema that serves as a percep- we will highlight that primacy of the self-experi-
tual based “protorepresentation” of the body. ence permeates throughout development, and
Although the above data highlights that infant can be seen in findings from cognitive neu-
representations of self and other actions are dis- roscience studies showing immediate activation
tinct, research also suggests that infants form of self-produced actions prior to other-produced
shared representations of their own and others’ ac- actions. In addition, we provide neurophysiolog-
tions. Neonates imitate the actions of others in a ical evidence for a cerebral mechanism specifi-
flexible and goal-directed way, suggesting that in- cally devoted to self–other distinction.
Cognitive neuroscience of self–other poral lobes. Because of these anatomical charac-

awareness and agency teristics, this region is a key neural locus for self-
processing that is involved in multisensory body-
One role that cognitive neuroscience can contrib- related information processing, as well as in the
ute to the study of the self and other is to ground in processing of phenomenological and cognitive
physiological mechanisms the distinct dimen- aspects of the self (Blanke & Arzy, 2005). Its le-
sions, aspects, and characteristics of the self and sion can produce a variety of disorders associated
other to help address the potential separability or with body knowledge and self-awareness such as
relatedness of each component part of self-pro- anosognosia, asomatognosia, or somatoparaphre-
cessing. It has been proposed that nonoverlapping nia (Berluchi & Aglioti, 1997). For instance,
parts of the neural circuit mediating shared repre- Blanke, Ortigue, Landis, and Seeck (2002) dem-
sentations (i.e., the areas that are activated for self- onstrated that out-of-body experiences (i.e., the
processing and not for other processing) generates experience of dissociation of self from body)
a specific signal for each form of representation can be induced by electrical stimulation of the
(Jeannerod, 1999). This set of signals involved right TPJ. Of interest, one study found aberrant
in the comparison between self-generated actions white matter adjacent to the TPJ, as well as in
and actions observed from others ultimately allow the ventromedial prefrontal cortices and anterior
the attribution of agency (comparison between ef- cingulate gyri (Barnea-Goraly et al., 2003) in
ferent motor signals and afferent sensory signals). children with ASD. Thus, deficits in self-other
It has also been suggested that the dynamics of processing in individuals with HFA may be due
neural activation with the shared cortical network to, in part, structural differences in pertinent brain
is an important aspect to distinguish one’s own ac- areas or in abnormal connectivity between these
tions from the actions of others, and that the la- areas.
tency difference between the changes in activity In addition, a number of functional imaging
elicited by the perception of self versus others’ ac- studies point out the involvement of the right
tions reflects the calibration process of shared TPJ in the process of agency (i.e., the awareness
representations (Decety & Jackson, 2004; Jackson of oneself as an agent who is the initiator of ac-
& Decety, 2004). Furthermore, the fact that the tions, desires, thoughts, and feelings). In one
onset of the hemodynamic signal is earlier for fMRI study, participants were instructed to open
the self than for the others (Jackson, Brunet, and close their hand slowly and continuously
Meltzoff, & Decety, 2006; Grèzes, Frith, & Pas- (0.5 Hz), whereas this movement was filmed
singham, 2004) may be considered as a neural sig- and projected to them online onto a screen (Leube
nature of the privileged and readily accessible self- et al., 2003). The authors reported a positive cor-
perspective. relation between the extent of temporal delay be-
Accumulating evidence from neuroimaging tween hand movement and its visual feedback
studies in both healthy people and psychiatric and the hemodynamic increase in the right TPJ.
populations, as well as lesion studies in neurolog- In another fMRI study, Farrer and Frith (2002) in-
ical patients, indicates that the right inferior parie- structed participants to use a joystick to drive a cir-
tal cortex, at the temporoparietal junction (TPJ) cle along a T-shaped path. They were told that the
with the posterior temporal cortex, plays a critical circle would be driven either by themselves or by
role in the distinction between self-produced ac- the experimenter. In the former case, subjects
tions and actions generated by others (Blakemore were requested to drive the circle, to be aware
& Frith, 2003; Jackson & Decety, 2004). In addi- that they drove the circle, and thus to mentally
tion, some recent data suggest that this region is attribute the action seen on the screen to them-
specifically involved in theory of mind (Apperly, selves. In the latter case, they were also requested
Samson, Chiavarino, & Humphreys, 2004; Saxe to perform the task, but they were aware that the
& Wexler, 2005). The TPJ is a heteromodal asso- experimenter drove action seen on the screen.
ciation cortex, which integrates input from the lat- The results showed that being aware of causing
eral and posterior thalamus, as well as visual, an action was associated with activation in the an-
auditory, somesthetic, and limbic areas. It has re- terior insula, whereas being aware of not causing
ciprocal connections to the PFC and to the tem- the action and attributing it to another person was
associated with activation in the right TPJ. It is in- from someone else’s perspective but not from
teresting that individuals experiencing incorrect their own (Ruby & Decety, 2001). Similarly,
agency judgments, as it can be the case in schizo- this region was specifically involved when partic-
phrenia, feel that some outside force is creating ipants imagined how another person would feel in
their own actions. One neuroimaging study found everyday life situations that elicit social emotions
hyperactivity in the right TPJ when patients with (Ruby & Decety, 2004) or painful experiences
schizophrenia experienced alien control during a (Jackson et al., 2006; Lamm, Batson, & Decety,
movement selection task compared with healthy 2007) but not when they imagined these situations
controls (Spence et al., 1997). Such delusions of for themselves. Such findings point to the similar-
control may arise due to a disconnection between ity of the neural mechanisms that account for the
frontal brain regions, where actions are initiated, correct attribution of actions, emotions, pain,
and parietal regions where the current and pre- and thoughts to their respective agents when one
dicted states of limbs are represented. mentally simulates actions for oneself or for an-
Another study used a device that allowed mod- other individual. Further, they support a crucial
ifying the participant’s degree of control of the role for the right TPJ, not only in mental state pro-
movements of a virtual hand presented on a screen cessing, but also in lower level processing, includ-
(Farrer, Franck, Georgieff, Frith, Decety, & Jean- ing reorienting attention to salient stimuli (Decety
nerod, 2003). Experimental conditions varied to & Lamm, 2007).
the degree of distortion of the visual feedback pro- Other areas implicated in self-processing, such
vided to the participants about their own move- as the medial PFC, posterior cingulate cortex, and
ments. Results demonstrated a graded hemody- precuneus, have been shown to be active when
namic activity of the right TPJ that parallels the individuals are at rest and deactivate during cogni-
degree of mismatch between the executed move- tively demanding tasks (Raichle et al., 2001). It
ments and the visual reafference. Strikingly, such has been hypothesized that this “resting state” net-
a pattern of neural response was not detected in work contribtes to self-reflective thought, social
schizophrenic patients who were scanned under perceptions, and theory of mind (Gusnard, Akbu-
the same procedure (Farrer et al., 2004). Instead, dak, Shulman, & Raichle, 2001). It is of interest
an aberrant relationship between the subject’s de- that in line with the social deficits observed in
gree of control of the movements and the hemo- ASD, individuals with ASD demonstrate atypical
dymamic activity was found in the right TPJ resting state activation in these networks (Ken-
and no modulation in the insular cortex. Addi- nedy, Redcay, & Courchesne, 2006). However,
tional evidence for the contribution of the right further research is needed to understand the nature
TPJ in self-awareness and the sense of agency de- of the relationship between self-experience, the
rives from studies on imitation that document the resting state networks, and social behavior in typi-
selective involvement of this region during recip- cally developing children, and those with ASD.
rocal imitation, in which it may be difficult to
keep track of agency, that is, who is imitating
Self, other, agency, and intersubjective
whom (Chaminade & Decety, 2002; Decety,
exchange in ASD
Chaminade, Grèzes, & Meltzoff, 2002). Results
from these studies provide strong support for the A mature sense of self-, agency, and other
implication of the right TPJ in the process of awareness are crucial for full-blown empathy,
self-agency by demonstrating a clear dissociation as they allow the observer to move beyond
between the left and the right TPJ. When partici- shared representations and accurately gauge
pants imitated the other, the left TPJ was strongly the other’s emotional state in relation to oneself,
engaged, whereas greater activation was detected in other words engage in intersubjective ex-
in the right TPJ when they were being imitated. changes. According to clinical descriptions, au-
Only this later condition involved discrepancies tistic children show problems in thinking, relat-
between predicted outcomes of the action per- ing, and communicating to the world as well as
formed by the participants and those perceived. moving through alternative perspectives that
The right TPJ is also selectively activated when others entertain (Hobson & Meyer, 2006), all
participants are asked to mentally simulate actions of which we suggest draw from more than basic
level motor resonance, as they include an agen- it is unclear whether observed differences reflect
tive stance over one’s actions and an ability to unique responding in children with ASD or
interpret others as agentive actors as well. unique responding in children with develop-
Empirical evidence supports the suggestion mental, cognitive delay.
that children with ASD fail to effectively discrim- Further evidence of weak self–other differen-
inate the actions of the self and other. A recent tiation among children with ASD derives from a
study examined self–other orientation (identifica- study utilizing a visual perspective taking task
tion) among 16 older children with autism, and 16 (Lee, Hobson, & Chiat, 1994). During such a
comparison, developmentally delayed children task autistic children were significantly less prone
matched for age and IQ (Meyer & Hobson, to use the pronoun “me” to answer whether they
2004). Participants performed four object-ori- were the subject in a photograph. Moreover, autis-
ented tasks such as rolling a wheel and stacking tic subjects were less likely than controls to em-
objects. Lines on the floor segregated the child’s ploy the pronoun “you” to refer to the experi-
and experimenter’s “personal space,” and tasks menter. The experimenters suggest that these
were either directed toward the child’s “personal results do not reflect vocabulary or semantic prob-
space” or toward the adult’s “personal space.” lems, as the children with ASD showed high ver-
After the model, children were encouraged to imi- bal ability, which was measured by the British
tate actions with a toy. In comparison to control Picture Vocabulary Scale. Instead, it was sug-
participants, children with autism performed sig- gested that failures to use pronouns reflect deficits
nificantly fewer responses that modeled the self– in perspective taking. Person pronoun use is
other orientation to the object. Instead, a signifi- among the few trademarks signifying self-con-
cant portion of the children with ASD showed sciousness, others including self-recognition in
“geometric repetition.” That is, they accurately mirrors and demonstration of self-conscious emo-
imitated the experimenter’s actions (i.e., rolling tions such as shame (Zelazo, 2004). By age 2,
the wheel); however, they did so without either executive function allows individuals to control
a “self”-orientation or an “other” norientation. aspects of conscious awareness, including con-
For example, children with ASD would roll a scious control of emotion, thought, and action.
wheel horizontally in the center of the testing Thus, executive functions may allow individuals
space, disregarding the experimenters’ wheel to regulate their egocentric bias, and engage in ac-
rolling either toward themselves or the child. curate perspective taking. In the case of ASD,
These findings suggest that it is not motor mim- problems seem to reflect not a bias in one’s own
icry that is problematic in autism per se, but in- perspective per se, but a weakness in adopting a
stead, specific impairments in intersubjective imi- conscious perspective albeit personal or other
tation. Children in the control group did not show oriented. Thus, it is likely that empathy deficits
this pattern of responding, which was interesting. in autism reflect problems at each or several of
Instead, they fell into one of two categories of re- the components integral to empathy. In the fol-
sponding: either consistently adopting appropri- lowing section, we discuss the crucial role of ex-
ate self- or other orientation, or showing a mix a ecutive function in mature empathy.
strategies, including not imitating at all. The au-
thors speculated that the findings reflect the fail-
Mental Flexibility and Self-Regulation
ure of identification in autism, highlighting corre-
spondence between performance on this task and Given the sharedness of the representations of
the capacity to comprehend others’ perspectives one’s own emotional states and others, as well
and to mentally shift from one perspective to an- as similarities in brain circuits involved during
other. The finding is in line with other data sug- first- and third-person perspective taking, it
gesting an autism-specific difficulty in accurately would seem difficult not to experience emotional
imitating the orientation of an action in relation to distress while viewing another’s distressed state
the model’s body (e.g., Ohta, 1987; Smith & Bry- and personal distress does not contribute to the
son, 1998). However, future research should empathic concern and prosocial behavior (Bat-
replicate these findings with an additional con- son et al., 2003; Decety & Lamm, 2008). Indeed,
trol group of typically developing children, as distress in the self can hinder one’s inclination to
soothe the other’s distress. However, it would not studies by Posner and Rothbart (2000) strongly
be adaptive if this automatic sharing mechanism suggest that executive regulation undergoes
between self and other was not modulated by dramatic change during the third year of life.
cognitive control and metacognition. It is neces- The PFC develops slowly compared to other
sary that executive functions work in a top-down regions during ontogeny, and reaches its matura-
fashion to regulate our proclivity to be biased in tion only late in adolescence (Bunge, Dudukovic,
our self-perspective while gauging another per- Thomason, Validya, & Gabrieli, 2002). Evidence
sons’ emotional state, and promoting a sympa- for this delayed maturation is provided by mea-
thetic regard for the other rather than a desire to sures of myelination, gray matter reduction, syn-
escape aversive arousal (Decety, 2005). Ventral aptogenesis, and resting metabolism (Huttenlo-
and dorsal regions of the PFC have been associ- cher & Dabholkar, 1997). Imaging studies
ated with response inhibition and self-control, indicate that prefrontal areas do not attain full ma-
which are key components of emotion regulation turations prior to adolescence (Paus et al., 1999;
(i.e., adjustments in type, magnitude, and dura- Sowell, Thompson, Holmes, Jernigan, & Toga,
tion of emotional responses that are made to 1999). Childhood cognitive development relates
meet personal, situational and interpersonal de- to maturation of the middorsolateral frontal cortex
mands; Ochsner & Gross, 2005). Support for as well as the ACC, which are critical for the de-
this hypothesis in the domain of pain empathy velopment of executive functions, especially the
comes from a recent fMRI study in which physi- dramatic increase in children’ ability to suppress
cians who practice acupuncture were compared external influences (Paus et al., 1999). Specifi-
to naı̈ve participants while observing animated cally, changes in cerebral blood flow, which re-
visual stimuli depicting needles being inserted flects synaptic activity, in the PFC, almost doubles
into different body parts including the mouth re- from age 0 to 2 years (Chiron et al., 1992). Further,
gion, hands, and feet. Results indicate that the an- the frontal association cortex is the last area to in-
terior insula, periaqueducal gray, and anterior crease blood flow from infancy to childhood, and
cingulate cortex (ACC; i.e., neural regions that reaches adult values only by adolescence (Taka-
belong to the pain matrix) were significantly ac- hashi, Shirane, Sato, & Yoshimoto, 1999). Direct
tivated in the control group, but not in the physi- support for age-related changes in brain activity
cian group, who instead showed activation of the associated with metacognition is provided by a
dorsal and ventral medial regions of the PFC, as neuroimaging investigation of theory of mind in
well as the right TPJ, involved in emotion regu- participants whose age ranged between 9 and 16
lation and metacognition (Cheng et al., 2007). years (Moriguchi, Ohnishi, Mori, Matsuda, &
It is of interest that the development of self Komaki, 2007). Both children and adolescents
and other mental state understanding is func- demonstrated significant activation in the neural
tionally linked to that of executive functions, circuits associated with mentalizing tasks,
that is, the processes that serve to monitor and including the TPJ, the temporal poles, and the
control thought and actions, including self- medial PFC. Furthermore, the authors found a
regulation, planning, cognitive flexibility, re- positive correlation between age and the degree
sponse inhibition, and resistance to interference of activation in the dorsal part of the medial
(Russell, 1996). There is increasingly clear evi- PFC. Impairment of the medial/cingulate PFC is
dence of a specific developmental link between commonly associated with deficits in social inter-
the development of mentalizing (i.e., the pro- action and self-conscious emotions (Sturm, Ro-
cess of making sense of mental states in oneself sen, Allison, Miller, & Levenson, 2006). Such pa-
and other persons) and improved self-control at tients may become apathetic, disinterested in the
around the age of four (e.g., Carlson & Moses, environment, and unable to concentrate their at-
2001). Improvement in inhibitory control corre- tention on behavioral and cognitive tasks. It has
sponds with increasing metacognitive abilities also been suggested that frontal damage hinders
(Zelazo, Craik, & Booth, 2004), as well as perspective taking ability (Price, Daffner, Stowe,
with maturation of brain regions that underlie & Mesulam, 1990). The current understanding
working memory and inhibitory control of the role of the PFC in executive functioning
(Tamm, Menon, & Reiss, 2002). A series of fits well with developmental research, which
indicates that empathic concern is strongly related Sager, et al., 1997, but see Cialdini, Brown,
to effortful control and self-regulation, with chil- Lewis, Luce, & Neuberg, 1997, for a different
dren high in effortful control expressing greater account of empathy and self-other merging).
sympathy and less personal distress (Rothbart, A recent study by Lamm et al. (2007) investi-
Ahadi, & Hershey, 1994). Effortful control may gated the distinction between empathic concern
support empathy and prosocial behavior by allow- and personal distress combining a number of
ing the child to attend to the thoughts and feelings behavioral measures and event-related fMRI.
of another without becoming overwhelmed by Participants were asked to watch a series of video-
their own distress (Posner & Rothbart, 2000). clips featuring patients (their face only) undergo-
Adopting another’s perspective is integral to ing painful medical treatment either with the in-
human empathy and is linked to the development struction to put themselves explicitly in the
of moral reasoning (Kohlberg, 1976), altruism shoes of the patient (“imagine self”), or, in
(Batson, 1991) and a decreased likelihood of in- another condition, to focus their attention on the
terpersonal aggression (Eisenberg et al., 2006). feelings and reactions of the patient (“imagine
Of special interest are findings from social psy- other”). Behavioral measures confirmed previous
chology that document the distinction between social psychology findings that projecting oneself
imagine the other and imagine oneself (Batson, into an aversive situation leads to higher personal
Sager, et al., 1997). These studies show that the distress and lower empathic concern while focus-
former may evoke empathic concern (defined ing on the emotional and behavioral reactions of
as an other-oriented response congruent with another’s plight is accompanied by higher em-
the perceived distress of the person in need), pathic concern and lower personal distress (e.g.,
whereas the latter induces both empathic concern Batson et al., 2003). Neuroimaging data were con-
and personal distress. This observation may help sistent with such findings. Both the self and other’
explain why empathy, or sharing someone else’s perspectives were associated with hemodynamic
emotion, need not yield prosocial behavior. If signal increase in the neural regions that belong
perceiving another person in an emotionally or to the pain matrix including the insula and ACC.
physically painful circumstance elicits personal However, the self-perspective evoked stronger
distress, then the observer may tend not to fully hemodynamic responses in brain regions in-
attend to the other’s experience and as a result volved in coding the motivational– affective di-
lack sympathetic behaviors. mensions of pain, including bilateral insular
The effect of perspective taking to generate cortices and aMCC. In addition, the self-per-
empathic concern was documented in a study con- spective led to stronger activation in the amyg-
ducted by Stotland (1969). In his experiment, par- dala, a limbic structure that plays a critical role
ticipants viewed an individual whose hand was in fear-related behaviors, such as the evaluation
strapped in a machine that participants were told of actual or potential threats. It is of interest that
generated painful heat. One group of subjects the amygdala receives nociceptive information
were instructed to watch the target person care- from the spinoparabrachial pain system and
fully, another group of participants were instructed the insula, and its activity appears closely tied
to imagine the way the target felt, and the third to the context and level of aversiveness of the
group was instructed to image themselves in the perceived stimuli (Zald, 2003). Imagining one-
target’s situation. Physiological (palm sweating self to be in a painful and potentially dangerous
and vasoconstriction) and verbal assessments of situation thus triggers a stronger fearful and/
empathy demonstrated that the deliberate acts of or aversive response than imagining someone
imagination yielded a greater response than pas- else to be in the same situation. Alternatively
sive viewing. Empathy specifically seems to be and less specifically, the stronger involvement
sensitive to perspective taking, as demonstrated of the amygdala might also reflect a general in-
by a series of studies demonstrate the effectiveness crease of arousal evoked by imagining oneself
of perspective-taking instructions in inducing em- to be in a painful situation. Regarding the insular
pathy (Batson, Sager, et al., 1997) and that empa- activation, it is worth noting that it was located
thy-inducing conditions do not compromise the in the middorsal section of this area. This part
distinction between the self and other (Batson, of the insula plays a role in coding the
sensory–motor aspects of painful stimulation, the second year of life. At this age children man-
and it has strong connections with the basal ifest a self-concept and self-conscious emotions,
ganglia, in which activity was also higher and children’s reparative behaviors after they
when adopting the self-perspective. Taken to- cause distress in the other emerge (Zahn-Waxler
gether, activity in this aspect of the insula possi- & Radke-Yarrow, 1990). A longitudinal study of
bly reflects the simulation of the sensory aspects young children’s development of concern for
of the painful experience. Such a simulation others’ distress showed that prosocial behaviors,
might both lead to the mobilization of motor such as hugs and pats, emerge around the begin-
areas (including the SMA) to prepare defensive ning of the second year of life, increasing in in-
or withdrawal behaviors, and to interoceptive tensity throughout this year and sometimes pro-
monitoring associated with autonomic changes vide self-comfort. However, by the end of the
evoked by this simulation process. second year, prosocial behaviors appear to be
Various domains of research suggest that more appropriate to the victims needs, are not
mental flexibility to adopt another person’s necessarily self-serving, and children’s emotions
point of view is an effortful and controlled appear to be better regulated (Radke-Yarrow &
process. Moreover, the capacity to take the con- Zahn-Waxler, 1984).
ceptual perspective of the other is thought to be The ability to regulate emotions may be sub-
a necessary component in the fully developed, ject to individual differences, and may interact
mature theory of mind. Developmental research with the degree to which individuals experience
indicates that perspective taking develops pro- emotions. Eisenberg and her colleagues (1994)
gressively. In the affective domain, children proposed a model suggesting an interaction be-
demonstrate emerging awareness of the subjec- tween the intensity at which emotions are experi-
tivity of other people’s emotions around enced and the extent to which individuals can reg-
18 months. By this age, infants understand ulate their emotions. In line with her model,
that they should provide an experimenter with multimethod regression analysis of empathy-re-
a piece of food that the experimenter reacts to lated responses combining self-report measures
with apparent happiness (e.g., broccoli) rather and facial muscle activity in response to empa-
than one that the experimenter previously re- thy-inducing videos (of impoverished chil-
acted to with disgust (fish crackers), even if the dren), suggest that increased emotional in-
infant prefers the latter food (Repacholi & Gop- tensity and decreased regulation on standard
nik, 1997). In contrast, 14-month-olds fail to self-report measures predict personal distress
demonstrate this understanding. This is the first in response to viewing the video vignettes.
empirical evidence that infants of this age have These interactions are first seen in infancy, as
at least a limited ability to reason nonegocentri- findings from infant development demonstrate
cally about people’s desires (Flavell, 1999). that 4-month-olds low in self-regulation are
Executive functions not only facilitate per- prone to personal distress at 12 months of age
spective taking, but also control attention and (Ungerer et al., 1990). In childhood, individuals
metacognitive capacities, both of which facili- with increased levels of emotional intensity
tate prosocial responding in reaction to another’s (based on self-report, teacher–parent report,
distress. Attention to others and the environment and autonomic measurements) and weak regu-
occurs when individuals are able to attend to ex- lation are prone to personal distress in response
ternal stimuli and disregard to some extent their to another’s predicament, as they become over-
self-experience. Metacognitive capacities allow whelmed due to their vicariously induced
for recursive thinking about the self’s actions, negative emotions (Miller & Eisenberg, 1988).
and are thus linked to emotions such as shame
or guilt which emerge as a result of causing an-
Mental flexibility deficits in developmental
other’s distress. Children first demonstrate re-
disorders of empathy
sponses to the distress of others with other-
focused behaviors like concern, attention to the Children with empathy deficits likewise show def-
distress of the other, cognitive exploration of icits in executive function and children with ASD
the event, and prosocial interventions around specifically show deficits in mental flexibility
(Bennetto, Pennington, & Rogers, 1996; Min- It is noteworthy that violent offenders, and
shew, Meyer, & Goldstein, 2002; Ozonoff & children with aggressive behavior problems, ex-
McEvoy, 1994; Ozonoff, Pennington, & Rogers, perience deficits in empathy and empathic con-
1991). A series of studies found that when an ex- cern, although the result of the lack of empathy
perimenter feigns distress in a room where chil- manifests in behavior differently than that seen
dren were playing, children with ASD looked to in ASD or DCD. The former responds aggres-
the experimenter much less than healthy and men- sively to others’ distress (Arsenio & Lemerise,
tally retarded children (Corona, Dissanayake, Ar- 2001), whereas the later simply lack prosocial be-
belle, Wellington, & Sigman, 1998; Dissanayake havior. The distinction can be understood as the
& Sigma, & Kasari, 1996; Sigman, Kasari, Kwon, difference between apathy and hostility, both of
& Yirmiya, 1992). However, when Blair (1999) which are categorized as unempathetic in the tra-
replicated such studies, but controlled for executive ditional sense, although one is “passive,” and the
function demands of attention, children with ASD other is “active.” Individuals with ASD seem to
performed similar to healthy children. That is, lack either an interest or capacity to resonate emo-
when experimenters’ feigned distress was unam- tionally with others, or engage in intersubjective
biguous and took place under conditions of low transactions (Gallagher, 2001). In contrast, chil-
distractibility, children with ASD showed auto- dren with developmental aggression disorders
nomic responses similar to controls. In studies react aggressively to the observation of others’
measuring facial mimicry, when given ample distress.
time, individuals with ASD do show affective CD is a mental disorder of childhood and ado-
compensatory tactics to accomplish emotion read- lescence that is characterized by a longstanding
ing; and in emotion recognition tasks, they show pattern of violations of rules and laws. Symptoms
activation in brain areas related to intentional atten- of CD include aggression, frequent lying, running
tional provision and categorization (Hall, Szecht- away from home overnight, and destruction of
man, & Nahmias, 2003). These data indicate that property. CD is important partly because it is the
alongside bottom-up information processing defi- major childhood precursor to antisocial personal-
cits (e.g., affective mimicry), top-down executive ity disorder in adulthood (Lahey, Loeber, Burke,
control is also impaired in individuals with ASD. & Applegate, 2005). Children with aggressive be-
Empathy deficits in Asperger syndrome also havior problems show deficits in regulating emo-
seem to reflect poor executive function. A case tions, which may result in harmful patterns of in-
study of two adolescents with Asperger syndrome terpersonal behavior. Lewis, Granic, and Lamm
with severe inabilities for emotional and cognitive (2006) reviewed several of their recent studies in-
aspects of empathy suggests that these weaknesses vestigating individual and developmental differ-
do not reflect significantly worse emotion recog- ences in cortical mechanisms of emotion regula-
nition or cognitive perspective taking per se, but tion, corresponding with different patterns of
instead, reveal poor integration of the cognitive interpersonal behavior. Their methods include
and affective components of empathy (Shamay- event-related potentials and cortical source mod-
Tsoory, Tomer, Yaniv, & Aharon-Peretz, 2002). eling, using dense-array EEG, as well as video-
Indeed, these executive function deficits in taped observations of parent–child interactions,
ASD have been documented by fMRI experi- with both normal and aggressive children. By re-
ments using cognitive tasks. Aberrant activity lating patterns of brain activation to observed be-
in prefrontal, frontal, as well as atypical fronto- havioral differences, the authors found (a) a steady
parietal interactions, have all been documented decrease in cortical activation subserving self-reg-
in fMRI experiments probing executive func- ulation across childhood and adolescence, (b) dif-
tion in ASD (Kana, Keller, Minshew, & Just, ferent cortical activation patterns as well as behav-
2007; Silk et al., 2006). It is likely that deficits ioral constellations distinguishing subtypes of
in mental flexibility are grounded in atypical aggressive children, and (c) robust correlations be-
structure and function in prefrontal, frontal, tween the activation of cortical mediators of emo-
and parietal lobes and contribute to perspec- tion regulation and flexibility in parent–child
tive-taking difficulties observed in individuals emotional communication in children referred
with ASD. for aggressive behavior problems.
Emotion is normally regulated in the human which is associated with aggressive behavior,
brain by a complex circuit that includes several re- contributes to these antisocial reactions.
gions of the PFC (dorsal and ventral), the amyg- One way to determine whether CD is associ-
dala, hypothalamus, ACC, insula, and ventral ated with low arousal or poor regulation is to
striatum. Descending pathways from orbitofron- investigate patterns and changes in autonomic
tal and medial prefrontal cortices, which are nervous system. Sympathetic activation or para-
also linked with the amygdala, provide the means sympathetic inhibition leads to changes in cardiac
for speedy influence of the PFC on the autonomic functioning, which can be interpreted as bodily
system, in processes underlying appreciation and cues of discomfort or distress and a need for ac-
expression of emotions (Barbas, Saha, Rempel- tion. Porges (1996) has found that parasympa-
Clover, & Ghashghael, 2003). It is of interest thetic nervous system functioning, as reflected in
that key areas found to be functionally or struc- heart rate variability (heart rate [HR] variability
turally impaired in antisocial populations include measures the variability in HR associated with
dorsal and ventral regions of the PFC, amygdala, breathing and indexes an individual’s competency
hippocampus, TPJ, and ACC (Raine & Yang, to physiologically and behaviorally reacts to exter-
2006). Raine has hypothesized that the rule- nal stimuli) influenced by the vagal system, is re-
breaking behavior common to antisocial, violent, lated to the control of attention, emotion and be-
and psychopathic individuals may in part be at- havior. Porges suggests that the tonus of the
tributable to impairments in some of the struc- vagus nerve provides a theoretical basis for the
tures (dorsal and ventral PFC, amygdala, and child’s ability to focus attentional processes, in-
TPJ) or dysfunction in amygdala–orbitofrontal hibit irrelevant activity, regulate emotion, and ap-
cortex (OFC) structural connectivity, normally propriately engage with the environment (Porges,
subserving moral cognition and emotion. 1995).
In contrast, impulsive aggression may be the In the domain of empathy, the work of Eisen-
product of failed emotion regulation. Impulsive berg and Fabes (1994) suggests that deceleration
aggression is associated with a low threshold of HR may be associated with attention to others
for activating negative affect and with failure to that characterizes empathic concern, and HR de-
respond appropriately to the anticipated negative celeration is also associated with an increase in de-
consequences of behaving aggressively. David- sire to help and comforting. A number of studies
son, Jackson, and Kalin (2000) have proposed indicate that antisocial behavior, and CD are asso-
that the mechanism underlying suppression of ciated with, and predictable from, low resting HR
negative emotion is via an inhibitory connection in children, adolescents, and adults (e.g., Lahey,
from regions of the PFC to the amygdala. Hart, Pliszka, Applegate, & McBurrett, 1993;
In addition to functional brain abnormalities Raine, Venables, & Sarnoff, 1997). Because
corresponding with emotion dysregulation and low resting HR is associated with greater aggres-
empathy deficits in CD, impulsive aggression sion, and aggression and concern for others are in-
in CD is associated with decreased noradrener- versely related, it has been predicted that high HR
gic (NA) function, which also correlates with should predict greater concern for others. One
poor empathic ability in this population (Raine, study found that HR was positively correlated
1996). In fact, a low resting heart rate, a partly with concerned responses toward adults who
heritable trait reflecting fearlessness and were simulating injuries (Zahn-Waxler, Cole,
stimulation seeking, at 3 years of age predicted Welsh, & Fox, 1995). However, Calkins and Ded-
aggressive behavior at 11 years of age (Raine, mond (2000) reported that aggressive children
Venables, Mednick, & Sarnoff, 1997). Children displayed no physiological indicators of under-
with clinical levels of behavior problems, often arousal, as indexed by resting HR. The authors
a precursor to the development of CD, show in- did find, however, that these children displayed
creased disregard for others, for example, anger, poor behavioral and physiological regulation, as
avoidance, and/or amusement by another’s dis- indexed by a lack of HRV during challenging sit-
tress, a negatively toned response pattern that uations. This latter finding supports the idea of a
differs significantly from normal children’s re- failure of self-regulation in relation to empathy
sponses. It is likely that decreased NA function, and aggression. Cardiac vagal regulation was
found to differentiate among children at risk for many neuroscience findings pertain to adult par-
behavior problems (Calkins, Graziano & Keane, ticipants, not children. Future studies should aim
2007). In that study (a sample of 335 children), to incorporate children in the investigation of the
there was a trend for the children at risk for exter- neural basis of empathy, especially because con-
nalizing problems to display less vagal withdrawal tradictions surround the few neuroscience stud-
than the control group. Future research should ul- ies that examine emotion sharing in children.
timately clarify the relationship between struc- Finally, the model reviewed here offers inter-
tural/functional differences in patterns of brain ac- esting insights for debates surrounding the natur-
tivation with NA function in individuals with CD. alization of normative ethics. Empathy has been
The maturation of executive functions, includ- associated with the propensity to respond to an-
ing emotion regulation (subserved by the dorsal other’s predicament in a prosocial, or “moral”
and ventral PFC and their connections with the way. Yet, an understanding of what motivates
amygdala) by 2 years of age contributes to the de- us to feel empathy in the sense of caring for the
velopment of prosocial behaviors. Conversely, if other (Batson et al., 2003) and then help them
executive functioning is not intact, self and other is unclear. In fact, humans fail to consistently re-
perspectives may not be regulated and individuals spond to others’ negative situations prosocially
may over- or underidentify with an observed tar- across contexts. Further research in child develop-
get. In the case of childhood aggression and CD, ment and cognitive neuroscience may help eluci-
it is likely that poor executive control and dysfunc- date these interrelationships and hopefully offer a
tion of emotion regulation contributes to empathy better understanding of emotional resonance, em-
deficits, although other factors (NA function) also pathy, and their relationship with prosocial, moral
contribute to reactionary behaviors. reasoning (and the lack thereof). The results of a
recent fMRI study on empathy and theory of
mind with children seem to indicate that there is
Conclusions
little overlap in the brain circuits associated with
We have argued that empathy depends upon both empathy for pain and moral reasoning, although
bottom-up processes, which are driven by emo- this does not mean that these circuits do not com-
tion expressions, and top-down processes, includ- municate (Decety et al., 2008). In this study, chil-
ing self-regulation and executive control. These dren watched situations involving either a person
different aspects are underpinned by distinct whose pain was caused accidentally or a person
neural systems that develop at different stages. whose pain was intentionally inflicted by another
Notably, emotion sharing relies on the percep- individual, as well as situations without any pain
tion–action coupling mechanism, which seems with one or two agents. It is important that when
functional very early in development, and allows children observed an individual intentionally
the newborn to implicitly share subjective bodily harming another, regions of the PFC that are con-
experiences with others. Controlled processes, sistently involved in representing social interac-
subserved by the PFC, develop later and play a tion and moral behavior such as the temporopa-
major role in metacognition, including taking rietal junction, the paracingulate cortex (PCC),
into account a cognitive representation of one’s and OFC were recruited (see Figure 2). It is of in-
own mind and other’s mind, aspects that are terest that children indicated in the postscan de-
necessary for social emotions which require briefing that they thought that the situations in
self-monitoring (see Figure 1). We have also which pain was caused by another person were
shown that developmental disorders related to unfair, and were asking about the reason that
empathy reflect dysfunction of these different as- could explain this behavior. Evidence from moral
pects. It is noteworthy that the current knowl- neuroscience suggests a critical role of a cortico-
edge in social cognitive neuroscience is at a pre- limbic network subserving moral judgment. This
liminary stage, and many findings need to be network includes the medial OFC, the TPJ, the
reproduced. In relation to the goal of this paper, amygdala, and anterior PCC (Moll, de Oliveria-
ties drawn between developmental and neuro- Souze, & Eslinger, 2003). Furthermore, the mon-
scientific evidence in emotion sharing and em- itoring of outcomes that relate to punishments and
pathy can only be loosely strung together, as rewards is linked to activity in the OFC
(Kringelbach & Rolls, 2004). It is worth empha- should be done with caution. It is difficult to derive
sizing that the regions selectively associated with the computational function of an area without tak-
the perception of an agent harming the other being into account its extrinsic and intrinsic connec-
long to the neural systems underlying moral tivity, the distribution of receptor types, and the in-
thinking. formation processing of the intrinsic neurons. Such
We have argued that genuine empathy goes information is generally lacking. In addition, a set
beyond emotion sharing and a simple resonance of cortical areas may be active in a wide range of
of affect between the self and other. It depends functions from action perception to empathy and
crucially on self–other awareness and on the abil- theory of mind, but across those functions the net-
ity to regulate one’s own emotional state, allow- works in which they participate may be quite dif-
ing proper identification of the other’s condition ferent (see Cacioppo et al., 2003). More empirical
and freeing up resources for coping with an- data from both developmental science and cog-
other’s distress in prosocial ways. Successful nitive neuroscience in the future will contribute
emotion regulation in infancy is essential for the to a fuller understanding of the mechanisms in-
development of the ability to control one’s own volved in empathy and their developmental time
arousal and, with the sense of agency, be able course. Furthermore, brain imaging investigations
to tag the aroused state as indicative of the state of emotional processes often draw from limited
of the other. Children as well as adults who be- methodologies that may overlook flaws in the op-
come overaroused by another’s distress, due to erational definitions of the emotional phenomena
lack of emotion regulation and/or self–other dis- studied. For example, many fMRI experiments re-
tinction, may use up too many cognitive require participants to identify the emotion in static
sources dealing with their own emotion and fail faces or short animations, implicitly considering
to act in a prosocial fashion (Nielsen, 2002). that emotion recognition can be equated with emo-
tional experience. Clinical investigations with neu-
rological patients, however, indicate that these pro-
Limitations of the scope
cesses (emotion recognition and experience)
It is important to note several limitations of our involve quite different neural substrates (Leven-
review. The first limitation pertains to the extent son, 2007). Future neuroimaging studies of emo-
to which conclusions can be drawn from the re- tion in general, and empathy in particular, should
lationship between the development of empathy base stimuli on the discrete emotional experience
in healthy children and the manifestation of em- examined. Meeting this goal would be facilitated
pathy deficits that occur in developmental disor- by the further collaboration between cognitive neu-
ders. We covered findings from infant develop- roscientists and developmental psychologists.
ment to address the innateness of the interacting Third, and finally, empathy is a complex con-
components of empathy; however, most of the struct and the above model does not account for
findings reviewed from developmental disorders all that empathy entails. The phenomenological
pertain to observations from early childhood. experience of empathy and its role in initiating
This limitation in part reflects the difficulty to ob- prosocial, empathic reactions likely draws on
tain infant data across developmental disorders as several interacting factors (and complicated
they are often not diagnosed until childhood. distributed brain networks) not mentioned in
Some analysis of infant behavior of children di- our review. For example, motivation likely in-
agnosed with developmental disorders comes fluences empathic accuracy: people who are
from home video analysis (see Baranek, 1999), motivated to produce empathically accurate re-
although such studies are sparse, and findings sponses to another’s predicament are less sus-
are ambiguous due to weak scientific control. ceptible to social inference biases such as the
Second, the relationship between neural evi- fundamental attribution error (Fletcher, Reeder, &
dence and behavioral data is indirect, and thus Bull, 1990; Tetlock, 1985). In addition, the type
speculations may be far reaching. Neuroimaging of rapport between observer and target influences
data help to answer fundamental questions about the intensity of emotion contagion between mem-
the mechanisms subserving imitation. However, bers of a dyad, with patients and therapists, mothers
their interpretation in relating structure to function and infants, and spouses, and even individuals who
perceive others as similar to themselves ranking tasks than children living in individualistic cul-
high in autonomic synchrony (Levenson & Ruef, tures (Eisenberg, Bridget, & Shepard, 1997).
1997). Social psychologists emphasize the role of
Another important area of interest regarding the situational context as opposed to personality in
contribution of empathy to the development of in- the experience of empathy (or the absence of it),
tersubjectivity is its relation to the so-called attach- although many recognize the combination of sit-
ment system described by Bowlby (1958), that is, uation and personality as the best predictor of so-
an innate psychobiological system that motivates cial behavior (Fiske, 2004). Although situational
infants to seek proximity to people who will protect context is important, creating ecologically valid
them. One can argue that the mechanisms that un- situations in a laboratory setting or in an MRI
derpin the development of empathy, especially scanner poses a challenge. Theoretically, assess-
through interaction with caregivers who are re- ing personality traits and correlating them with
sponsive, partly overlaps, and are functionally task performance and biological markers should
linked with promoting optimal functioning of the pose no great challenge. These constructs, how-
attachment system. The consequences of this link ever, are rarely stable and they are dependent on
between empathy and attachment are paramount. many variables. Thus, designing ecologically
Indeed, Mikulineer and Shaver (2005) have docu- valid experiments remains a challenging process,
mented the idea that people who have the benefits especially with children.
of secure social attachments find it easier to per- A current aim in cognitive neuroscience is to
ceive and respond to other people suffering, com- study the interaction between affect and cogni-
pared to those who have insecure attachments. tion. Empathy, a valuable social phenomenon,
Personality traits, temperaments, and cultural exemplifies this complex relationship because
norms of emotional display also contribute to the it draws on aspects such as emotion sharing
degree to which empathy may be experienced in and self-regulation. In addition, affective and
the observer (Eisenberg & Fabes, 1994; Posner social cognitive developmental neuroscience of-
& Rothbart, 2000). Likewise, children from cul- fers promising insights for both our understand-
tures that promote reciprocal relations and coop- ing of typical and psychopathological social
eration tend to be better at perspective-taking behavior.
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DecetyMeyer Empathy 2008

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Development and Psychopathology 20 (2008), 1053–1080

Copyright # 2008 Cambridge University Press

From emotion resonance to empathic

JEAN DECETYa AND MEGHAN MEYERb

Table 1. Definitions of empathy provide a more comprehensive understanding

Cognitive neuroscience of self–other poral lobes. Because of these anatomical charac-

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