The Evolution of Human Emotion

4.
28 The Evolution of Human Emotion

L A Parr, Emory University, Atlanta, GA, USA
B Waller, University of Portsmouth, Portsmouth, UK
2007 Elsevier Inc. All rights reserved.
4.28.1 Introduction: Emotion Is Necessary for Survival

4.28.1.1 Directions for Understanding the Evolution of Emotion
4.28.1.2 Emotion Underlies Adaptive Behavior
4.28.1.3 The Innate Expression of Internal Arousal Systems
4.28.2 Assessing Emotion through Facial Movement
4.28.2.1 Are Primate Facial Expressions Homologous?
4.28.2.2 Assessing Similarity in Human Facial Expressions
4.28.3 The Evolution of Social Emotions
4.28.3.1 Building Blocks for Complex Emotions
4.28.3.2 Social Emotions
4.28.3.3 Brain Systems Involved in Social Emotions
4.28.3.4 Precursors in the Evolution of Human Emotion: A Final Word
Glossary
homology
social emotions
theory of mind
A trait or behavior in two related species that is attributable to a common

ancestry.
Emotions such as shame, embarrassment, guilt, and pride that require selfconsciousness and an understanding of
social rules and their transgressions.
The ability to understand the mental
states of others.
4.28.1 Introduction: Emotion

Is Necessary for Survival
Human emotions, rooted though they are in our animal
nature, are nevertheless run through, as mere animal emotions
are not, with thought and belief, wish and want, fantasy and
imagination, as should be expected of language-using, conceptexercising creatures (Bennett and Hacker, 2005, p. 31).
Emotion has long been viewed as an important

phenomenon underlying animal behavior. Emotion
helps individuals attend to and extract relevant
information from the environment and organize
physiological, motivational, and cognitive action
patterns that facilitate adaptive responses to aid
the survival of the organism. As such, emotion can
be thought of as a process that facilitates appropriate responses to a wide range of both internal and
environmental situations. Emotional reactions are
critical in avoiding predation, finding mates, nurturing young, caring for the elderly, and engaging
in behavior that is consistent with social and
cultural rules. Some researchers refer to these as
drives, innate reflexes, or unconditioned responses.
447
448
448
450
453
453
455
458
458
462
464
466
No matter the term, each of these phenomena

involves emotion.
Emotion is not only an elusive concept by definition, but the investigation of emotion is fraught with
difficulty. One of the main reasons is that emotion
influences, and is influenced by, so many facets of
the mind and biology. Emotions involve cellular
and hormonal processes that in turn affect physiological and neural systems. These collectively affect
behavior, the interactions between individuals and
other species, and ultimately the integration of the
individual within its society. In part because of
its interdisciplinary nature, it is becoming a more
common practice for researchers to examine emotion as a multidimensional construct, incorporating
multiple levels of analysis that cross basic evolutionary, biological, behavioral, social, and cultural
boundaries (Cacioppo and Gardner, 1999; Frijda,
1986; Kappas, 2002; Keltner and Haidt, 1999).
Whereas this componential approach has a progressive structure, ranging from basic biological to social
processes, it has been argued clearly by others that
this progression is anything but linear or hierarchical
(Cacioppo and Berntson, 1992). In fact, social factors
can influence biological factors and vice versa, with
no one level of analysis having any greater role than
another for understanding emotion. Many have
argued that the only way to fully understand emotion
is to examine each level, not restricting the analyses
to any single component (Kappas, 2002; Leventhal,
1991). Only through the collective integration of
ideas and findings across disciplines will researchers
begin to identify the quantitative and qualitative features leading to the expression of emotion in animals
and ultimately to identify and understand what is

unique about human emotion.
4.28.1.1 Directions for Understanding
the Evolution of Emotion
This article will focus on three broad developments in

the emotional behavior of animals with reference to
human behavior. The first is that emotion involves
innate, reflexive, and adaptive behavior that shares
commonalities in its underlying mechanisms of production in all animals. Studies from both nonhuman
primates and human neonates suggest, for example,
that some facial expressions are produced from birth
with little or no social experience. Additionally, the
underlying mechanisms for these behaviors have a
common signature in animals due to the role of
various brain structures, particularly the limbic
system, and the recruitment of physiological processes that serve to increase the survival of the
organism (Panksepp, 1982). These survival responses
are aided by the nervous systems bias for processing
negative information at high levels of arousal
(Cacioppo et al., 1999). These reflexive and adaptive
behaviors are arguably the building blocks from
which more complex and flexible forms of emotional
responses evolved and, even in advanced species such
as humans, they are ever vigilant.
The second development is that socially living species have means to communicate with one another
about emotion, through visual, auditory, tactile, or
chemosensory signals. The communication system
and the signals therein need not be specific or referential, or even self-conscious, for that matter. There
need not be a specific association, for example,
between the signal, e.g., a facial expression, and its
emotional meaning, e.g., fear, although this has been
suggested in humans (Ekman, 1992). Rather, these
signals are predictive of the general motivation and/
or tendency of the organism to engage in a series of
actions given a set of social and environment conditions (van Hooff, 1973). The signals, however, must
be easy to recognize and discriminate from other
signals and/or noise in the environment, or their
information content and predictive value will be
lost. Thus, in addition to the signal being discrete
and distinctive, the receivers of the signal must be
tuned to its detection. Because of the strong relationship between facial expressions and emotion in
humans, much of this section will focus on evidence
for homologous facial expressions in humans and
related species and introduce the development of a
behavioral coding system, similar to that used for
humans, that will prove extremely influential in identifying the underlying meaning of these signals.
Finally, greater flexibility in communication systems, more complex social environments, and
individual social relationships fueled by an expanding
neocortex contributed to the evolution of socially
derived emotions, or self-conscious emotions, such
as guilt, shame, pride, and embarrassment. These
emotions are rooted in a basic awareness of the self
and the unobservable mental states of others, a concept known as theory of mind. The absence of these
socially derived emotions is, in many cases, associated
with various forms of psychopathy and neurodevelopmental disorders such as autism (Heerey et al., 2003;
Hillier and Allinson, 2002; Levenston et al., 2000).
Though there is little conclusive evidence for theory
of mind in species apart from humans, it will be
argued that a precursor to theory of mind must
have been an awareness of others emotions, a
basic form of empathy, which appears to be present
in rudimentary forms in mammals, including our
closest-living primate cousins (Parr, 2001; Preston
and de Waal, 2002; Povinelli and Preuss, 1995).
4.28.1.2 Emotion Underlies Adaptive Behavior
4.28.1.2.1 Subconscious evaluative processes

Emotion involves behavioral reflexes that represent
adaptive responses by an organism to environmental
challenges. These basic reflexes can be deconstructed
to include approaching things judged to be positive, or
appetitive responses, and avoiding things judged to be
negative, or aversive responses. This basic bivalent
system was derived from research on unconditioned
reflexes in animals, with appetitive motivational
systems including behaviors such as ingestion, copulation, and nurturing young and aversive motivational
systems including behaviors such as withdrawal and
the rejection of noxious stimuli. Furthermore, there is
evidence that these basic evaluative systems are implicitly associated with motor responses that aid in the
adaptive responding of the organism. Studies have
found, for example, that muscle extension is more
often associated with negative affective responses,
such as withdrawal and avoidance, than with muscle
flexion, which is associated more with positive
responses, or approach (Cacioppo et al., 1993). In
this experiment, stimuli were judged more pleasant
when individuals flexed their arms as if pulling an
item toward them than when their arms were
extended, as if pushing the item away (Cacioppo
et al., 1993). These stimuli consisted of neutral
Chinese ideographs, ruling out the possibility that
subjects had preconceived affective attitudes toward
these stimuli that subconsciously affected their evaluations. Additionally, these effects were not found
when subjects simply observed someone engaging in
The Evolution of Human Emotion
muscle flexion and extension, indicating that the

motor action itself was necessary for differential
evaluative responses. Similarly, response latencies to
either push or pull a lever when presented with affective words were faster when the flexion action of pull
was paired with a positive emotional word-stimulus
and when the extension action of push was paired
with a negative emotional word-stimulus than when
push and pull were incongruently paired with positive
and negative stimuli, respectively (Chen and Bargh,
1999). These associations were not the result of any
conscious processes, in that subjects did not report
any awareness of the association between their behavior and their affective evaluations. In addition, when
asked to form intentional, conscious judgments about
certain stimuli, such as semantic characteristics compared to evaluative characteristics, these responses
weakened (Bargh et al., 1996). Finally, these processes
were found for novel, abstract stimuli that were rated
as being either positively or negatively valenced
(Duckworth et al., 2002). This provides further
support for the influence of unconscious, affective
evaluative processes on the automaticity of adaptive
behavioral responses (Murphy and Zajonc, 1993).
At this primitive level, appetitive and aversive behavioral responses are modulated by specific neural
circuits in the brain that share a common neuroarchitecture among mammals. These brain systems are
genetically hard-wired to enable animals to respond
unconditionally to threatening, or appetitive, stimuli
using specific response patterns that are most adaptive
to the particular species and environmental condition
(Berridge, 1996; Panksepp, 1982). When aversive
stimuli are detected, for example, receptors in the
sensory cortex and thalamus are activated. These sensory afferents activate the amygdala directly, leading
to a cascade of responses that enable the organism to
escape or reject the current situation (LeDoux, 2000).
The same information travels via a slower route to the
cortex and then back to the amygdala, providing the
organism with an opportunity for postcognitive emotional evaluation. Appetitive systems, on the other
hand, have a rich history in studies of the nucleus
accumbens and mesolimbic dopamine system that are
involved in regulating the bodys response to reward
and pleasure (see Berridge, 2003). Although it is still
common for the neural control of emotional behavior
to reside solely on the shoulders of the limbic system
(MacLean, 1949; Panksepp, 1982), studies have implicated a variety of brain structures in both cortical and
subcortical regions including the amygdala, cingulate
cortex, hypothalamus, insular cortex, orbitofrontal
and prefrontal cortices, and even brainstem sites and
cerebellum (Allman et al., 2001; Berridge, 2003; Lane
et al., 1998; Parvizi et al., 2001). Studies in both
449
humans and animals using a variety of techniques are

now showing that a single brain area subserving emotion is drastically simplistic, in fact, just plain wrong.
Rather, the brain appears to have distributed connectivity among regions that individually play key roles in
the experience of emotion, but only collectively provide the color for emotional experience (for excellent
reviews, see Berridge, 2003; Buck, 1999).
4.28.1.2.2 Emotions are negatively biased The
evaluations described above are, however, not
without influence and/or interindividual variability.
Stimuli are evaluated not only with respect to environmental change but are weighted in relation to the
individuals current motivation within that environment. To determine which response is most adaptive
given a set of internal and environmental conditions, animals, like humans, rely on a basic system
of appraisals that evaluate environmental events
according to their self-relevance. Appraisals refer
to implicit, rapidly occurring evaluations made
about the significance of an object or event and are
likely to differ depending on the individual, his or
her previous history, and his or her current condition (Scherer, 2000). In terms of emotion, similar
patterns of appraisals may emerge across individuals, resulting in similar emotional experiences.
When objects and events are appraised as being
conducive to achieving an important personal goal,
happiness may result, whereas events that are
appraised as occurring suddenly, with uncertain
and potentially threatening consequences, are likely
to result in emotions such as fear (Scherer, 2000).
Whereas appraisals are considered a form of cognition, they are not necessarily conscious, although
conscious awareness and control of behavior may
occur later in the processing stage in some species.
From an evolutionary perspective, species should
arguably be more invested in aversive, defensive
response systems in some situations than appetitive,
positive response systems. If an individual does not
safely avoid the dangers of predation, he or she will
not be able to seek out mates and reproduce, and thus
contribute his or her genetic investment to future
generations. Thus, individuals might be in a constant
state of vigilance, with defensive systems ready to
respond if dangers are detected. Moreover, positive
and negative motivational systems may be co-activated, having nonreciprocal associations rather than
occur along a single bivalent dimension. Thus, an
animal may choose to approach a food source in the
presence of a potential predator if its feeding motivation is high, co-activating appetitive and defensive
systems. Similarly, a human may refrain from eating
his or her favorite dessert when on a diet. Thus, an
improvement in the traditional bivalent system,

where positive and negative motivations lie at opposite ends of a continuum, Cacioppo and Berntson
(1994) have proposed that attitudes and emotions
are better viewed according to a model of evaluative
space. Evaluative processes refer to the neural circuitry and subsequent behavioral adaptations involved
in processing the affective significance of a stimulus.
This is opposed to nonevaluative processes that refer
to the discrimination and categorization of such
stimuli (Cacioppo et al., 1999). According to the
evaluative space model, positive and negative
responses are under the regulation of separable motivational substrates that can act independently of one
another (Cacioppo and Berntson, 1994). Therefore,
dimensions of positivity and negativity can be activated reciprocally or individually or they can be
uncoupled with each dimension either co-activating
or co-inhibiting the other.
According to the evaluative space model, the
positive motivational system is characterized by
greater activation when the arousal level of the
system is low. So, at low levels of arousal, individuals tend to respond with greater positive
responses than negative responses. This also
makes sense from an evolutionary perspective.
Positive emotional behaviors, such as copulation,
maternal care, and grooming, are all highly social
interactions that are best served when individuals
are calm and not likely to be easily driven into a
heightened state of defensive arousal. In contrast,
the negativity bias, as it has been termed, is defined
as greater output in the negative motivational system than in the positive motivational system, given
the same degree of activation, or level of evaluative
input. Evidence for these two dimensions has been
found in a number of studies. Negative stimuli, for
example, elicited larger event-related potential
responses in humans than positive pictures, even
when subjects were not required to make any affective evaluations of the stimuli, evidence of the
negativity bias (Ito and Cacioppo, 2000). In addition, Ito et al. (1998) used regression analyses to
assess peoples arousal ratings for a variety of emotional stimuli. As predicted by the regression
parameters, a shallower slope and higher value at
low levels of arousal were found for positive arousal ratings (higher intercept value), whereas a
steeper regression slope with greater ratings of
negativity at higher levels of arousal was found
for negative arousal ratings (negativity bias).
Thus, the model helps to explain the evolution of
distinguishable motivational systems in animals that
allow for the co-occurrence of exploration and selfpreservation (Cacioppo et al., 1999). These models
are particularly useful for developing theories about

the evolution of human emotion because they lay a
framework for understanding the behavior of animals in an ever-changing and increasingly complex
social and ecological environment. Basic drive systems are constantly present, but control over these
basic reflexes creates a myriad of potential outcomes that have helped to shape the evolution of
animal behavior and emotion. These concepts will
become important for the discussions in the final
section of this article.
4.28.1.3 The Innate Expression of Internal
Arousal Systems
4.28.1.3.1 Hedonic facial reactions to taste One

of the earliest and most conspicuous behavioral
manifestations of these arousal systems is the production of facial expressions. Although numerous studies
have examined both the perception and production
of facial expressions in human infants (Izard, 1971;
Nelson, 1987), fewer studies have focused on these
distinctions in nonhuman primates. However, evidence to date suggests that some facial expressions
may have strong innate components, occurring in
primates soon after birth, with little or no prior social
experience with conspecifics.
One set of evidence for the innate production of
facial expressions comes from a series of elegant
studies in humans and nonhuman species on the
faciogustatory response to various tastes and smells.
Sweet, sour, and bitter stimuli, for example, produced highly similar patterns of spontaneous facial
displays in both adult humans and neonatal infants;
i.e., neonates were less than 16 h old and were tested
before their first feeding experience (Steiner and
Glaser, 1995). These authors found very stereotypical facial reactions in all subjects in response to these
gustatory and olfactory stimuli that could be divided
according to basic hedonic valence. Sweet stimuli
produced facial relaxation, retraction of the mouth
corners into a basic smile, and licking and sucking
movements (see The Evolution of the Sweetness
Receptor in Primates). Bitter tastes produced depression of the mouth corners and elevation of the upper
lip, whereas sour tastes produced pursing of the lips
(Steiner, 1974). Based on these facial response patterns, stimuli could be divided into two broad
hedonic or motivational categories: one of acceptance, consummation, and pleasure, and the other
suggestive of rejection, repulsion, and aversion
(Steiner and Glaser, 1984).
To determine the evolutionary commonality of
these innate facial reactions, Steiner and colleagues
examined facial responses to tastes in numerous
species of nonhuman primates including prosimians,

New World monkeys, Old World monkeys, and
hominoids (Steiner and Glaser, 1984, 1995; Steiner
et al., 2001). Facial reactions were coded using
detailed ethograms of facial movements, including
components of the facial action coding system
(FACS) developed by Ekman and Friesen (1978) to
characterize human facial movements according to
their underlying facial musculature (see Section
4.28.2.2.2.1) and for ethological descriptions of primate facial expressions (Andrew, 1963). Also
important to these studies is the concept of homology
described in the second section of this article (see
Section 4.28.2.1). In brief, it is important to show
that the pattern of facial reactions and accompanying
behavior is homologous across the species tested,
thus enabling researchers to conclude that the behavior is the result of similar affective evaluations
mediated by similar neural substrates. Results found
that facial reactions and behaviors in nonhuman primates could be grouped according to positive and
negative hedonic dimensions and that these affective
behavioral reactions were similar across species and
taste categories (Steiner et al., 2001). Reactions
observed in all species shared universal components,
including a rhythmic pattern of tongue protrusions in
response to the sweet stimuli and an open-mouth
gape with head shake in response to the bitter stimuli.
Furthermore, across taxonomic groups, taste-elicited
affective reactions were more similar among closely
related species. Hominoid-specific expressions, for
example, included actions involving the lips and middle part of the face. A smile in response to sweet
stimuli, for example, was observed only in apes and
humans. Old World monkeys showed characteristic
brow elevation in response to the sweet stimuli, a
pattern not observed in the other species. Reactions
specific to New World species included a tongue protrusion pattern that categorized bitter versus sweet
stimuli. Therefore, these gustofacial responses are
innate, stimulus-dependent communication signals
common among related primate species that reflect
the organisms ability to differentiate afferent sensory
stimuli along basic hedonic dimensions (Steiner, 1974;
Steiner et al., 2001). As such, these facial patterns can
be used to measure and compare emotional responses
across species and provide evidence for an innate and
phylogenetic relationship between facial expressions
and emotional experience.
4.28.1.3.2 The role of social experience One of
the first psychologists to speculate about the
relationship between emotion and social behavior
was Harry Harlow at the Wisconsin Regional
Primate Research Center in Madison, Wisconsin.
451
His research focused on the emotional needs of

young rhesus monkeys (Macaca mulatta) during
their early stages of development. Although these
studies did not explicitly emphasize the importance
of facial expressions or emotional communication,
this research was pivotal in documenting the severe
emotional and behavioral consequences that result
when young rhesus monkeys are deprived of social
contact with their mother from birth and are raised
in social isolation (Harlow et al., 1971). The attachment of an infant to its mother was not simply based
on the need for food, but on the even more fundamental need for what Harlow termed love and
affection. These studies also provided an experimental format for examining nature versus nurture issues,
such as which behaviors are expressed innately and
which require social experience. Regardless of the
specific application, these studies raised a critical
awareness within the primatological community,
and far beyond, as to the importance of early social
experience for normal social and emotional development (Harlow and Mears, 1983).
During this period, Gene Sackett, a student of
Harlow, demonstrated that socially nave monkeys produced appropriate facial expressions and
behavioral responses when shown photographs of
threatening conspecifics compared to photographs
of conspecifics with playful or fearful expressions,
monkeys engaged in sex, or control photographs
depicting nonsocial stimuli (Sackett, 1966). The
key conclusion from these studies was that social
experience was not necessary for the production of
species-typical facial expressions; rather, these
expressions were the product of an innate releasing
mechanism and could be elicited in a morphologically intact form in the complete absence of social
experience (Sackett, 1965). When these isolated
monkeys were later introduced to a social group,
however, they were unable to respond appropriately
to the range of facial displays and complex
emotional messages produced by their new group
mates. It seemed that although the appropriate production of facial expressions may be the result of
innate mechanisms, the comprehension of facial displays made by other individuals in a dynamic social
context required a period of normal social and emotional development.
Sacketts studies suggest that the subtle contextdependent meaning of facial expressions can be
learned only from direct social experience. A direct
gaze, for example, is interpreted by rhesus monkeys
as being threatening; hence an important component of a threat face is to stare directly at the
opponent (Hinde and Rowell, 1962; van Hooff,
1962). But do monkeys really understand these
cues from birth or must they see others engage in

these interactions before they understand their
meaning? To study the development of how infant
rhesus monkeys respond to a direct open-mouth
threat, 1-, 3-, and 7-week old rhesus infants were
tested on their responses to the faces of conspecifics
with direct or averted gaze (Mendelson et al., 1982).
These faces were presented using projection slides.
No differences in viewing were detected in the
1-week-old infants. By 3 weeks of age, however,
infant monkeys looked for a longer time at the
faces with the direct gaze than at those with the
averted gaze. This increased viewing was accompanied by negative emotional behaviors; i.e., the
individuals showed submissive squealing, grinned,
and lip-smacked at the direct-gaze faces. By 7 weeks
of age, the infants avoided looking at the direct-gaze
faces altogether. Instead, these infants preferred to
look at the faces with the averted gaze and no longer
produced emotional responses in their presence.
These results suggest that by 3 weeks of age, rhesus
monkey infants understand the social implications
of the direct stare and respond submissively to this
threatening stimulus. These infants, however, do
not as yet have the social competence or knowledge
to avoid looking at these faces. By 7 weeks of age,
the infants behavior changed dramatically. They
now learned to respond to this socially threatening
stimulus by looking away, a response that is
critically important for integration into a rhesus
macaque social group.
Further evidence for the specific role of facial
expressions in social communication was provided
in a series of studies by Izard, one of the founders of
facial expression research in humans and infants
(Izard, 1971). In a series of studies, Izard and
colleagues transected the facial nerve (cranial
nerve VII) of 3-year-old monkeys and examined the
behavioral and emotional consequences when these
individuals were physically unable to make facial
expressions. How would individuals get by when
the primary tool for social and emotional communication was not at their disposal? Although these
studies were never published in a peer-reviewed
format, preliminary results suggest a number of
important findings. (The preliminary report was
published in Izards seminal book The Face of
Emotion, 1971, pp. 385391.) First, the animals
that received facial nerve transections displayed
more aggression, mounting, and general activity
than their cage mates. Second, when returned to
their social group, experimental subjects showed
greater displacement activities, threats, and attacks
than group mates and eventually dropped in
rank. Third, the relationship between the operated
females and their infants was compromised. Infants

appeared not as strongly attached to their mothers
and spent more time apart from her interacting
with other, unoperated group members. Results
suggest that communicating through facial means
is an important, and perhaps necessary, ability for
social integration and the expression of typical
social behavior.
A series of intriguing studies was performed by
Robert Miller and his colleagues. They demonstrated that rhesus monkeys could communicate
affective information to one another using facial
expressions. Specifically, Miller et al. (1959)
exposed monkeys to a photograph of a familiar
group mate with a neutral face. The presentation
of this conditioned stimulus (CS) was paired with a
shock that subjects could avoid only by pressing a
lever in their test cage. Subjects quickly learned to
press the lever when this face appeared, thereby
avoiding the shock, i.e., standard operant conditioning. Next, subjects were shown another photograph
of the same CS individual, but this time making a
fearful facial expression. When subjects were shown
this new stimulus, they produced spontaneously significantly more avoidance responses than during the
acquisition of the conditioned response when the CS
was the same monkey with a neutral face. This
suggests that a negative facial expression is much
more effective in communicating an upcoming
aversive event, i.e., the shock, than a neutral face,
illustrating that at some level the monkeys understood its inherent negative emotional meaning.
Similar findings have been reported in humans
using implicit priming studies. Winkielman et al.
(1997) demonstrated that when humans were presented with photographs of smiling faces for 10 ms,
too quick for conscious perception, they rated neutral stimuli as being more pleasant than if primed
with frowning faces or blank slides.
In a second study, Miller et al. (1963) tested
whether a stimulus monkey and a responder monkey could cooperate in producing an avoidance
response. In this paradigm, only the stimulus individual could see the CS that signaled the upcoming
shock, but unlike the previous situation, this individual had no access to the avoidance lever. In another
room, the responder monkey could access the lever,
but it could not see the projection screen that displayed the CS. The responder monkey could see
only a live video feedback of the face of the stimulus
monkey in the other room. The idea was that
changes in the facial expression of the stimulus individual as it viewed the CS would be sufficient to
communicate the upcoming danger to the responder
monkey, who in turn would press the lever so that
they both would avoid the shock. The result of

this cooperative avoidance paradigm was that the
responder monkey produced more lever presses
during the period when the CS was visible to the
stimulus monkey, indicating that the stimulus
monkeys facial expression was sufficient in communicating the appropriate affective information to
the responder monkey.
These studies serve to demonstrate several important characteristics of affective facial expressions in
nonhuman primates. First, these expressions have
an innate component. This includes both the production of specific facial expressions and the type of
information they communicate. Threatening facial
expressions are better for communicating negative
events, congruent with their emotional quality, than
neutral faces. Interestingly, this was not found for
positive facial expressions, supporting the concept
of a negativity bias in the evolution of affective
communication (Ito et al., 1998) and perhaps the
fact that these monkeys were in a heightened state of
arousal in this aversive conditioning paradigm.
Second, they provide an excellent reminder of the
importance of normal social development and social
experience for learning the appropriate meaning of
facial expressions and how to use them with sufficient skill when interacting with conspecifics.
4.28.2 Assessing Emotion through

Facial Movement
Emotion, to this point, has been described primarily
as an automatic, adaptive process with a strong
innate component. Its social expression and utility
in maintaining social cohesion, however, require
experience and learning. Emotion is also an experiential process that includes a strong subjective
component unique to each individual. Because this
process may never be fully understood or achieve
direct comparison both within and between species,
emotion must be studied at a more concrete, observable level. The human literature has provided a rich
history for the study of observable emotion through
facial actions and expressions. From the early
empirical work of French neurologist Duchenne de
Boulogne, who was the first to electrically stimulate
facial muscles to create emotional expressions, to
more contemporary studies by Paul Ekman and
others, the association between facial movement
and emotion provides a means for identifying and
measuring emotions in naturalistic and experimental contexts (Duchenne de Boulogne, 1862; Ekman
and Friesen, 1975; Izard, 1971; Tomkins and
McCarter, 1964).
453
Additionally, facial expressions provide a robust

level of comparison for understanding the evolution
of emotion for several reasons. First, the facial
expression repertoires of related species, despite
highly varied patterns of social organization, are
very similar. Common facial expressions have been
described in many different species of nonhuman
primates, suggesting that they were important behaviors in our evolutionary history (see The Evolution
of Parallel Visual Pathways in the Brains of
Primates). Furthermore, some of these expressions
are elicited in similar social contexts, which is suggestive of, although not evidence for, a common
function or meaning. Second, the mimetic facial
musculature that forms the structure of facial
expressions is highly conserved across primate species. This indicates that, with few exceptions, the
facial behavior of related species can be compared
directly in a manner that reinforces evolutionary
continuity in the form of expressive behavior.
Third, a large body of multidisciplinary research,
as has already been discussed, strongly supports
the association between facial expressions and emotion in primates. Humans in many diverse cultures
are able to identify basic facial expressions using
emotion labels, leading to the claim that facial emotions are biological universals, not culturally derived
behavior patterns. Finally, this cross-cultural
research has been aided considerably by the development of an objective, highly detailed coding
system for analyzing facial movements according
to their units of production, the mimetic facial musculature. Therefore, facial expressions represent a
highly salient and empirically robust unit of measurement for understanding the evolution of emotion
in primates. These different points are discussed
below.
4.28.2.1 Are Primate Facial Expressions

Homologous?
4.28.2.1.1 Facial expression repertoires are similar

among closely related species Although the order
of Primates can be characterized by striking differences
in social organization and behavior across species,
the appearance of facial expressions has remained
remarkably similar. Contemporary research over the
past half-century has considerably advanced our
understanding of the communicative repertoire of
nonhuman primates. This includes detailed descriptive
reports of facial expressions in a variety of primate
species including chimpanzees, bonobos, macaques,
and capuchin monkeys (de Waal, 1988; Hinde and
Rowell, 1962; van Hooff, 1962; Andrew, 1963;
Goodall, 1968; Parr et al., 2005; Weigel, 1979). The

two main goals of this research have been to document
the range of communication systems present in our
closest ancestral lineage and examine whether these
facial expressions are similar, both morphologically
and functionally, to our own.
This similarity in the appearance of facial displays
is due, in part, to a general conservation of the facial
muscles that underlie these expressions (discussed
below), which show a similar basic plan across
mammals (Huber, 1931), and to ritualization, a
process by which a formerly adaptive, unspecialized
behavior becomes divorced from its originally adaptive context to take on a different and typically more
communicative meaning. The result of this ritualization process has been that signals become easily
recognizable, highly conspicuous, and often stereotypical in their movement, helping to ensure that
they are easily detected and understood by members
of the same species.
Due to the association in humans between facial
expressions and emotion, comparing the characteristics of facial expressions between related species
would be insightful for making general assumptions
about the emotional quality of nonhuman primates
facial behavior. That said, determining homology in
behavior is a particularly daunting task because
there are many levels on which to draw such
comparisons. Behavior can be homologous due
to its genetic basis, ontogenetic development, morphological structure, nervous innervation, and/
or behavioral function (Lauder, 1994; Redican,
1982). Indeed, a character may be continuous
throughout evolution on one of these levels, but
shift from the ancestral character on another level.
This can make the identification of homologous
traits both difficult and controversial (Cartmill,
1994). In determining the most optimal unit of analysis, researchers are often self-serving; i.e.,
primatologists might use behavioral appearance,
whereas molecular biologists might use protein
structure. In addition, a behavior might be strikingly
similar between species at one level of analysis, i.e.,
such as the appearance of facial expressions, but
closer examination of other levels including the
ontogeny, underlying musculature, and social function, could reveal dissimilarity. This raises an
important point with regard to understanding the
homology of primate facial displays: visual appearance alone is insufficient to make assumptions about
the homologous nature of facial displays because
different species have different facial shapes that
may influence the appearance of facial actions
made by the same muscle, or the facial actions may
look similar but the muscular basis for these
movements might be different. Thus, for the comparison between human and nonhuman primate facial
expressions, appearance and musculature together
provide a better and more evolutionarily stable unit
of analysis for understanding the evolution of emotion than appearance or social function alone.
Several expressions have been addressed in terms
of human and nonhuman primate homology, particularly the silent bared-teeth (sbt) display, often
called the fear grin, and the relaxed open-mouth
face, or play face. These have been compared to
the smile and laughter displays of humans, respectively (Preuschoft and Van Hooff, 1995; Waller and
Dunbar, 2005). The sbt consists of a retraction of
the mouth corners, pulling the lips away from the
teeth while the mouth remains closed. The evolutionary origin of this movement is suggested to be a
protective response in drawing the lips away from
noxious stimuli (Andrew, 1963). Through ritualization, this movement has come to signal social
submission and/or appeasement, although its use is
quite varied. In the chimpanzee, for example, the sbt
has been observed in aggressive contexts and more
positive emotional contexts, such as affinitive behavior and play, and thus seems to have diverged
considerably from its association with fear (Parr
et al., 2005). Van Hooff (1973) recognized this
important deviation and suggested that in some
highly developed taxa, the sbt might have a reassuring function associated with attachment tendencies.
The muscle action that accomplishes this movement
in both humans and chimpanzees is contraction of
the zygomaticus major, although there has been
debate about whether the same visual appearance
can be achieved through the contraction of the risorius, which pulls the mouth corners laterally, or the
platysma, which pulls the mouth corners downward
on the jaw (Redican, 1982). These phylogenetic
comparisons are important to fully understand the
homologous relationship between underlying structure and observable function and how these have
been shaped by evolution to fit the specific needs of
each species.
4.28.2.1.2 Primate facial expressions share structural
elements The mimetic muscles involved in the
production of facial expressions have changed little
over the course of primate evolution. It has even
been argued that they have been shaped by evolution specifically to aid visual communication
(Huber, 1931). The facial muscles in all primates
are formed from two basic sheets the sphincter
colli superficialis and the sphincter colli profundus
(Huber, 1931). The latter provides the material for
the majority of the facial muscles, particularly
those that are involved in expressive movements,

and the former develops into the platysma, a broad
sheath of muscle fibers in the neck region. In
general, the complexity and subtlety of the facial
musculature as a whole are features that are unique
to the order of Primates, but the relative size and
differentiation of these two muscle sheets do vary
between primate species. There is greater differentiation observed in the sphincter colli superficialis
and, moreover, this differentiation is attributed to
the more highly expressive species (Huber, 1931).
Another interesting feature of this muscle sheet is
that the individual muscles that arise from it often
attach directly to the skin, which is in contrast to
other skeletal muscles that attach to bone and connective tissue. This provides confirmatory evidence
that the primary function of the muscles derived
from the sphincter colli superficialis is to produce
movement of the facial landmarks, i.e., skin, providing the basis for visual communication. There is
also evidence linking the evolution of facial expressions and elaboration of the facial musculature to
brain function. Sherwood et al. (2004) reported
phylogenetic differences in the organization of neurons enriched with neurofilament protein in the
primary motor cortex among nonhuman primates.
Species with more elaboration in the mimetic facial
muscles and greater repertoire of facial expressions, such as great apes and humans, showed a
greater density of neurons that might contribute to
greater dexterity and more voluntary control of the
facial region. In addition, the volume of the facial
nucleus in the pons of the brainstem was larger
than would be predicted based on standard phylogenetic regression in great apes and humans, again
suggesting greater spontaneous control of the facial
musculature in hominoids than in other nonhuman
primate species (Sherwood et al., 2004). Thus,
there appears to be a phylogenetic relationship
between facial expression repertoire and neural
control of the facial musculature.
An understanding of the phylogenetic nature of
the facial muscles can inform us about interesting
species differences in facial movements by tracing
the origin of these movements back to their muscular basis. Prosimians, for example, an evolutionarily
older group of primates, having split from the ancestors of anthropoids 4045 Mya, have very fine
control of their ear movements through action of
the postauricular muscles. Contraction of this muscle retracts the posterior portion of the scalp and
results in the action of ear flattening. This muscle is
also present in the cercopithecine primates; however, it has less influence over ear movement and
instead serves primarily to retract the scalp in
455
collaboration with frontalis. Thus, in one species,

contraction of this muscle produces noticeable differences in ear movements, but in other species, it
acts mostly to change the appearance of the scalp. In
humans and some species of great apes, further
differentiation between the actions of the postauricular and frontalis muscles has resulted in a
separation between the actions of the ears and
scalp. As a result, ear movement is not associated
with brow or scalp movement (Burrows et al., 2006;
Waller et al., 2006). Some have suggested that
because of the previous connection between the
actions of the postauricular and frontalis muscles,
the brow movements of humans are vestiges of ear
perking movements in lower mammals, for example, when orienting attention (Andrew, 1963). It has
been suggested that brow movements can act as
conversational signals of emphasis and attention,
invoking the phylogenetic origin of these muscle
actions (Ekman, 1977).
An examination of the buccinator muscle provides an illustration of how muscles can be
released from their original adaptive function and
through ritualization can come to play important
roles in social communication. The buccinator is a
muscle that lines the buccal pouch in many primates
and aids primarily in the manipulation of food in the
mouth. In humans, the buccinator is used during
mastication and when contracted it also dimples
the cheek fat, an expressive movement associated
with contempt and, in contrast to other emotional
expressions, does not appear to be present in primate species other than humans (Matsumoto and
Ekman, 2004). Thus, although some interesting differences between species can be discussed, primates
appear to share displays that are similar in appearance (expressions), in their structural elements
(underlying musculature), in their use in particular
social contexts (function), and in their ability to
communicate
information
to
conspecifics
(meaning). Thus, facial expressions provide a robust
unit of behavior for comparing emotional communication across related species.
4.28.2.2 Assessing Similarity in Human Facial
Expressions
4.28.2.2.1 Facial expressions as biological universals

Numerous reviews have been written regarding
the ability of humans to recognize emotion from
facial expressions (Ekman, 1992; Izard, 1994;
Russell, 1995). The two main claims from this
work have been that facial expressions of emotion
are described by people in similar ways and are
displayed in response to similar emotional
experiences regardless of culture. Considerable

debate still surrounds these premises, largely due
to the presence of well-known display rules and
various methodological issues that arise when conducting cross-cultural research (Russell, 1995).
Display rules represent culturally specific social
norms that dictate when and when not to express
certain emotions and/or behaviors in social contexts. One of the most well-cited studies is that of
Ekman and colleagues (1972). They showed stressinducing films to college students in the United
States and Japan when the subject was either alone
or in the presence of an experimenter from the same
cultural group. When alone, the students in both
groups made facial expressions that differed only
minimally; however, in the presence of an experimenter, the Japanese students inhibited their
negative facial expressions more often and showed
more smiling than the American students (Ekman
and Friesen, 1971, cited in Fridlund, 1994). This is
presumed to be the result of the collectivistic
Japanese culture to control negative emotional
expression in public as a way of facilitating a harmonious community (Shioiri et al., 1999).
Since this study, display rules have become an
accepted mechanism for the regulation of emotion,
although these studies have largely viewed regulation of emotion as occurring through the inhibitory
control of facial expressions. Matsumoto et al.
(2005) have developed a new approach that goes
beyond simple measures of inhibition or suppression. According to the display rule assessment
inventory (DRAI), individuals may express emotion
with no inhibitions, amplify or deamplify the intensity of the expression, mask the true expressions
with either a neutral face or another expression
type, or qualify their expression, which involves
showing the true expression together with a smile.
In another study, these authors requested American,
Russian, and Japanese subjects to try and feel a set of
basic emotions in four hypothetical social settings:
interactions with family members, with close friends,
with colleagues, or with strangers. Americans were
found to have the greatest amplification scores,
whereas Japanese had higher deamplification and
qualification scores (Matsumoto et al., 2005). Thus,
the DRAI provides a more sensitive and detailed tool
for the measurement of cultural variation in the use
of different display rules.
Cultural differences are also present in the ratings
of facial emotions. Izard (1971), for example, tested
the ability of American, European, Japanese, and
African individuals to identify basic facial emotions
from photographs of Americans and found some
cultural variation in emotion recognition accuracy.
American and European subjects showed the best

overall recognition, whereas Japanese and African
subjects showed quite poor recognition. Indeed, some
expressions, i.e., anger, seem to be poorly recognized
across cultures, whereas other expressions, i.e., happiness, are almost universally recognized. Several
studies have attributed such discrepancies to in-group
expertise effects. In other words, individuals are best
at identifying facial emotion when posed by members
of their own race, or at least of races for which they
have considerable experience; i.e., JapaneseAmericans would be good at discriminating
Caucasian facial expressions, but Japanese students
who have lived only in Japan would not. This
phenomenon is very similar to the other-race effect
described for general face processing and cannot be
accounted for by simple motivational differences
at judging faces of another ethnic group (Tanaka
et al., 2004). Elfenbein and Ambady (2003), for
example, found that recognition rates for six basic
emotions, happiness, fear, anger, disgust, sadness,
and surprise, were significantly better when the judges
were of the same ethnic origin as the posers of the
facial expressions. Similar results were found when
the ethnicities of the rater and the poser were different, but the rater had had considerable experience
within the culture of the posers country, i.e.,
Tibetan raters living in China or African raters living
in the United States (Elfenbein and Ambady, 2003).
Thus, emotion recognition judgments were influenced
by the degree of exposure individuals had with the
ethnicity in question. No such investigation has been
made into potential cultural or regional differences in
expressive behavior in nonhuman primates. That primates might show cultural variation in their use of
communicative facial behaviors has not been suggested up to this point, despite evidence showing
cultural variation in other types of behavior. Such an
investigation, however, would be extremely interesting and informative.
4.28.2.2.2 An objective coding system links
expressive movement to muscle action
4.28.2.2.2.(i) The FACS In one review, Paul et al.
(2005) suggested that the activity of the facial muscles would provide a useful endpoint for comparing
emotion in animals and humans if related facial
expressions in animals could actually be identified.
Due in part to the issues mentioned above, such as
problems in identifying the homologous characters
of facial behavior, very few studies have attempted
to directly compare particular facial expressions in
human and nonhuman primates. Darwins (1872)
seminal book The Expression of the Emotions in
Man and Animals remains one of the most detailed
comparisons of facial expressions across species and

it claims that, to understand human emotional
expressions, one must first understand emotional
expressions in animals. Even with renewed interest
in this question, contemporary studies suffer from
many of the same problems that Darwin encountered, namely, what unit of measurement to use and
how to directly compare behavior across species
without relying on anthropomorphic interpretations.
In humans, the development of an objective and
extremely detailed coding system for measuring
facial movements has virtually eliminated potential
emotional biases that can arise when interpreting
facial expressions. The FACS, developed by Ekman
and colleagues, identifies a series of action units
(AUs) that represent the movements of underlying
facial muscles (Ekman and Friesen, 1978). This
enables researchers trained in this technique to
describe faces in terms of visible action units
rather than emotions. When a person is happy, for
example, he or she typically smiles. However, smiles
can be posed, insincere, and even deceptive (Ekman
and Friesen, 1982; Ekman et al., 1988). Using the
FACS system, however, smiles associated with genuine enjoyment, or so-called felt smiles, were found
to be associated with contraction of the zygomaticus
major, which retracts the lips over the teeth (AU12),
and contraction of the obicularis oculi (AU6), which
produces slight wrinkles around the eyes, sometimes
called crows feet (Frank et al., 1993; Krumhuber
and Kappas, 2005). The AU6 smile is often referred
to as the Duchenne smile, after the seminal work on
facial expression measurement by the neurologist
Duchenne de Bologne (1862), which predated
Darwins book. Subjects rated smiles associated
with genuine enjoyment, compared to those associated with false enjoyment, more accurately when
those smiles contained contraction of the obicularis
oculi and these individuals were viewed as being
more positive. Researchers also found that there
was less variability in smiles that contained AU6,
suggesting that the presence of an AU6 is a reliable
indicator that the smile is associated with genuine
enjoyment (Frank et al., 1993).
Various studies have validated the usefulness of
the FACS system for identifying universal facial
emotions and the unique involvement of individual
AUs in their categorization. Kohler et al. (2004)
used certified FACS coders to rate human facial
expressions using action unit codes and then analyzed whether each facial emotion was associated
with unique action unit identifiers. These FACS ratings revealed different patterns of action units for
expressions of posed and elicited happy, sad, angry,
and fearful expressions. Though there was some
457
overlap in action units recorded for each facial

expression category, both the presence and absence
of unique units, or unit combinations, enabled an
identifying pattern to be found for each emotion
type happiness: unique AU6 (cheek raiser) and
AU12 (lip corner puller), absent AU4 (brow
lower), and AU20 (lip stretcher); sadness: unique
AU17 (chin raiser), absent AU26 (jaw drop);
anger: unique AU9 (nose wrinkler) and AU16
(lower lip depressor), absent AU1 (inner brow
raiser); fear: unique AU5 (upper lid raiser) and
AU2 (outer brow raiser), absent AU7 (lid tightener)
and AU10 (upper lip raiser) (Kohler et al., 2004).
4.28.2.2.2.(ii) The chimpanzee FACS Our understanding of the evolution of emotion would be
considerably advanced if such a rigorous and objective system could be applied to comparisons of
human and nonhuman primate facial expressions.
An FACS system for identifying chimpanzee facial
movements based on the underlying facial musculature has been developed (Vick et al., 2003). This
involved cataloguing thousands of videos and still
photographs of naturally occurring chimpanzee
behavior and identifying recurring facial movements. The muscular basis for these movements
has also been verified through an extensive review
of the comparative anatomy literature and through
direct intramuscular stimulation of both humans
and chimpanzees to verify the appearance of
facial movement when muscles are stimulated
(Waller et al., 2006). Additionally, facial dissections
have been performed to identify the presence or
absence and precise location of facial muscles in
the chimpanzee to help in validating the behavioral
and physiological approaches described above
(Burrows et al., 2006). These studies confirm the
homologous nature of chimpanzee mimetic facial
muscles and the action they produce when contracted. These studies are critical for comparing
emotional expressions in chimpanzees and humans.
The development of a chimpanzee facial coding
system will be extremely valuable for understanding
similarities and differences in the facial movements of
chimpanzees and humans. The use of such a system
could, for example, provide a direct assessment of
whether sbt displays differ among species where this
expression has an appeasing, reassuring function
versus a fearful, submissive function. One might
assume that the emotional differences would also be
associated with different muscle action patterns. The
chimp FACS has already validated the subjective
categorization of nine chimpanzee facial expressions:
the bared-teeth display (bt), play face (pf), hoot face
(ho), relaxed-lip face (rl), neutral (n), scream (sc),

Table 1 Predicted classification of nine chimpanzee facial expressions using chimp FACS by discriminant functions analysis
Chimpanzee facial expressions assignment category
bt
pf
ho
rl
n
sc
al
po
wh
bt
pf
ho
rl
sc
al
po
wh
78.9
0.0
0.0
0.0
0.0
5.6
20.0
0.0
11.1
13.2
87.5
0.0
0.0
0.0
2.8
20.0
0.0
0.0
0.0
0.0
100.0
60.0
16.7
0.0
20.0
84.6
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
40.0
75.0
0.0
20.0
0.0
11.1
7.9
6.3
0.0
0.0
0.0
91.7
0.0
0.0
0.0
0.0
6.3
0.0
0.0
0.0
0.0
20.0
0.0
0.0
0.0
0.0
0.0
0.0
8.3
0.0
0.0
7.7
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
7.7
77.8
al, alert face; bt, bared-teeth; ho, hoot face; n, neutral; pf, play face; po, pout face; rl, relaxed-lip face; sc, scream; wh, whimper.
alert face (al), pout (po), and whimper (wh). One

hundred and seventy-eight individual chimpanzee
expressions from 63 different individual chimpanzees
were FACS coded using 10 action units in the chimp
FACS (by two trained chimp FACS coders), AU6,
AU9, AU10, AU12, AU16, AU17, AU22, AU25,
AU26, and AU27. These were then subject to a discriminant functions analysis, similar to the approach
used by Kohler et al. (2004). According to this analysis, over 74% of the expressions were categorized
correctly after cross-validation using chimpanzee
FACS action units. The classification matrix can be
seen in Table 1. Expression types that were not accurately classified included the relaxed-lip face, the alert
face, and the pout. Based on this kind of analysis,
prototypical action units that best characterize each
expression type can be identified, a tool that will be
extremely useful when comparing directly the homologies between emotion expressions in chimpanzees
and humans.
Table 2 provides a comparison of prototypical
facial expressions in chimpanzees and humans and
gives their collectively coded action units according to the human FACS and the newly developed
chimp FACS. These are matched not only according to their morphological similarity and
involvement of similar muscle movements, but
according to their functional similarity as well. It
is not possible to provide a detailed assessment of
the proposed function of chimpanzee facial displays
in this article. Readers are referred to numerous
excellent reviews and ethograms for detailed descriptions (Goodall, 1968; van Hooff, 1967, 1973;
Marler, 1965; Parr et al., 2005). In brief, the bulging-lip face is typically displayed by males after a
dominance display, suggesting its association with
displaying status and superiority. The bared-teeth
display can be silent or can be accompanied by a
scream, squeak, or bark vocalization. It is used
in many different situations including times of

uncertainty, to signal appeasement and/or friendly
contact, when fearful, and during times of extreme
excitement, such as feeding time. No study to date
has attempted to determine whether the baredteeth displays used in each of these contexts can
be distinguished morphologically, as in the case
of the Duchenne smile. Chimpanzees scream in
many contexts, including during aggressive/assertive situations, after receiving aggression, and in
protest of anothers actions. The panthoot is used
to signal excitement over long distances and most
often precedes a dominance display, or bluff display, and is often accompanied by piloerection. The
pout is given when individuals are denied access to
something and are most typically seen in weaning
infants and during times of distress. The relaxed
open-mouth display, or play face, is used almost
exclusively during playful interactions with other
individuals.
4.28.3 The Evolution of Social Emotions

4.28.3.1 Building Blocks for Complex Emotions
Group living offers many advantages to the individual, including access to resources (mates, food, and
shelter), predator defense, and the ability to defend
resources from intergroup encounters. Yet, group
living also incurs costs, for although animals in
groups are able to access and defend a greater number of resources, they also experience increased
intragroup competition for these valuable resources.
Many animal species have evolved strategies
for dealing with these costbenefit conflicts, but
many primates have mastered a particular quality
of behavior that allows complex, interactive groups
to form and remain stable for long periods of time.
We refer to this as sociality. Sociality reduces the
Table 2 Chimpanzee and human facial expressions characterized by the chimpanzee and human FACS systems
Chimpanzee display
Prototype AUs
Equivalent human facial

expression?
Bulging-lip display
AU17 + AU24
Angry face
Silent bared-teeth
display
AU10 + AU12 + AU16 + AU25
Smile
Scream
AU10 + AU12 + AU16 + AU25 + AU27
Scream
Panthoot
AU22 + AU25
Relaxed open-mouth
display
AU12 + AU25 + AU26
Laughter
AUs in italics are found in the chimpanzee display and the proposed human equivalent.
Human images from Matrinez, A. M. and Benavente, R. 1998. The AR Face Database. CVC Technical Report No. 24.
Taken from Waller, B. M. 2005. Facial Expressions in Chimpanzees and Humans: Measurement and Meaning. PhD. thesis,
Department of psychology, University of Portsmouth.
costs associated with group living by facilitating the

formation of flexible dominance hierarchies and
assisting in the formation of long-lasting relationships, including alliances, coalitions, and cooperative
behaviors (Boesch, 2002; de Waal, 1989).
Arguably, the difference between groups of animals that exist with sociality and those that exist
without sociality is the presence of a complex, yet
flexible system of communication. It is in this
capacity that the relationship between distinctive, observable facial movements and underlying
emotional states might be more central for understanding sociality than previously considered.
Once emotional states are expressed, interpreted
by group members, and responded to in socially
appropriate ways, requiring a prolonged period
of social learning during early development, they
become part of a dynamic, interactive social
network, or society. In addition, the cognitive
processes necessary for both the effective production and efficient processing of signals within such
a communicative system are also likely to
have undergone selection and may have even
co-evolved within this system (i.e., see social
brain hypothesis in Dunbar, 1998). The end result
is that animal relationships and societies are
hinged on emotional communication and the
more complex the society/relationship, the greater
the need for the expression, perception, and perhaps most importantly, the experience of emotion.
The presence of nonlinear hierarchies, intragroup
and intergroup encounters, and complex social
organizations replete with dynamic and reciprocal
social relationships have contributed to the
advancement of social emotion/motivation systems
beyond the innate, reflexive survival mechanisms
described above. Here we will describe several
unique qualities of the social organization of
chimpanzees and how this may have placed
demands on their communication system leading
to the evolution of social emotions.
4.28.3.1.1 Complex social environments and social
relationships The ability to recognize and monitor
not only ones own relationships, but also the relationships among other individuals, though striking
in chimpanzees, is not a skill unique among anthropoid primates. Many other primate species show
complex forms of social knowledge (e.g., Cheney
and Seyfarth, 1990). Social knowledge is critical
for navigating a social environment in which
knowing who is your friend and, perhaps more
importantly, who is your aggressors friend is crucial
to avoiding conflict and maintaining access to
resources. Valuable social and physical resources
(e.g., grooming bouts, food sharing, and alliances)

are traded between individuals in a biological marketplace where traders must not only keep up with
their own trading partners and transactions, but
also keep track of commodity flow among others
(Henzi and Barrett, 2002; Noe and Hammerstein,
1995). Primates, and chimpanzees in particular, are
known to share food in exchange for grooming bouts
(de Waal, 1997), engage in cooperative hunting
(Boesch, 2002), and form coalitions (Watts, 1998).
Such mental record keeping in complex societies
typically involves triadic interactions, where individuals monitor and manipulate the behavior of others,
not only in reference to themselves, but with reference to others. Triadic reconciliations have been
reported in a number of species, where the former
aggressor in a conflict will engage in affiliative interactions with kin members of the victim and not the
victims themselves (Aureli et al., 1992; Call et al.,
1996). Moreover, individuals who witness conflicts
have been found to increase affiliative behavior with
each other, despite having played no direct role in the
conflict itself (Judge and Mullen, 2005).
The result of these complex interactions is that
many societies have developed rules for social
behavior that function to maintain order within
the group. Some rules are basic and are likely to be
present in many animals (i.e., do not bite the alpha
male, do not kill infants), but others are more complex (i.e., the tit-for-tat reciprocity described among
chimpanzees; de Waal, 1997). These require that
group members recognize one another at the individual level, remember interaction partners, keep
track of the details of the interaction, including the
type of commodity involved, remember these events
for some duration of time, make the decision to
respond or not respond at some point in the future,
and subsequently adjust their knowledge about the
interaction partners for future reference. These
details are specifically challenging for individuals
that live in dispersed social systems in which individuals are not always in visual proximity and can
travel individually or in small subgroups for periods
of time (see Section 4.28.3.1.2). The basic assumption underlying social emotions, described below, is
that they require individuals to understand that
social rules and norms apply to their behavior and
that violating these rules and norms will have social
consequences. Among nonhuman primates, social
transgressions are typically addressed by the alpha
male of a group, who may physically punish those
individuals who break social rules, but other group
members, including females, may also play pivotal
roles. De Waal (1982; 1989) has elegantly provided
numerous descriptions of such interventions. Among
captive animals, humans may become entangled in

such triadic interactions involving transgressions of
behavioral norms that we have come to impose on
our simian colleagues. The following anecdote was
observed by the lead technician in L.P.s laboratory:
I had positioned the computer cart in front of the animals
cage for testing and loaded the software program. While
holding the joystick panel up to the cage, Patrick (the only
male in the group) was messing around with me while I tried
to secure the top hook. Julie was sitting calmly and awaiting
her turn, but then I noticed she began to fiddle with something
below the panel. She used her two index fingers to fish the
cord that ran from the back of the joystick to the computer
through the caging. When I realized what she was doing,
I tried to pull the cord from her, but she grabbed it and bit it
at the same time. So this severed the cord from the joystick
and she ran off with it. I proceeded to remove the joystick
panel and the cage mates were all screaming. I looked into the
cage and the older females were screaming at Julie. Lulu (47
years old) was above her on a perch and Wenka (52 years) was
positioned at her side. Julie was on the floor below them
against the wall. She was screaming with bared teeth and
reaching out to Lulu with an open palm, a typical gesture
used by chimpanzees when requesting reconciliation or reassurance. A few moments later Julie returned to the front of the
cage and handed the cord to me, unsolicited, through the
mesh. She then turned back to the older females and continued
to gesture for reconciliation. Patrick, the only male in the
group, was in the back doorway displaying. Later that afternoon, I went out to their group and Julie presented for me to
groom her and allowed this for almost an hour! She was sweet
and nonaggressive, quite different from her typical behavior
toward me (May 2005).
All behavioral interpretation can follow a high or

low cognitive road. The high-level interpretation of
this scenario is that the older females in the group,
who often take initiative in helping to resolve group
disputes, recognized that Julie had done something
inappropriate, i.e., grab and break the joystick. This
action led the researcher to remove the joystick panel,
which, despite the individual who is working on a
task, is often associated with everyone getting some
kind of food treat. They responded by berating Julie
for her actions. Julies only response was to use
her communication skills to request forgiveness, by
extending her open hand and baring her teeth,
signaling her need for reassurance and for the
screaming to end. Some time later, she allowed the
researcher to groom her, perhaps in an attempt to reestablish a good social bond with the researcher after
her bad behavior. A low-level interpretation might be
that the old females were somehow disturbed by the
broken joystick and responded with an egoistic bout
of screaming, which would reveal that they were each
affected in the same manner by the incident as they
collectively targeted Julie. As in the high-level interpretation, Julie responded with social cues that she
has learned will sometimes terminate conflict. Her
461
grooming tolerance later might have been an attempt

to receive some treats she missed earlier.
4.28.3.1.2 Nonlinear hierarchies and fissionfusion

societies Many species of primates maintain stable
groups through a linear and despotic dominance
hierarchy (e.g., rhesus macaques, Macaca mulatta;
de Waal and Luttrell, 1985). According to such a
system, dominance relationships between two individuals are unambiguous and stable: the dominant
animal will always win the resource through force
and intimidation, and this is not likely to change
during the lifetime of the individuals. However,
some species have more flexible, egalitarian styles
of dominance, in which power relationships can
be more fluid and complex (e.g., chimpanzees,
Pan troglodytes; de Waal, 1982). Contests are
won through cooperation and alliances rather than
aggression and specific dominance relationships are
dependent on the presence or absence of other individuals alliance partners and can change often
throughout ones lifetime.
Preuschoft and van Hooff (1995) have proposed
that the use and function of communicative signals
among primates vary in accordance with dominance style, reflecting the specific demands placed
on the communication systems of species with
different social hierarchies. A full description of
this hypothesis (the power asymmetry hypothesis
of motivational emancipation) is outside the scope
of this article (Preuschoft and van Hooff, 1995,
1997). Briefly, species with strict dominance hierarchies show clear signals of affiliation,
appeasement, and submission that can be easily
distinguished from one another in both their morphological form and context of use, or social
function. The sbt display in rhesus macaques, for
example, is a highly ritualized facial expression of
submission that is unidirectionally performed by a
subordinate individual toward a dominant (de Waal
and Luttrell, 1985). In contrast, species with a more
relaxed, nonlinear dominance style will show less
predictability between display types and their associated social function. The homologous sbt display
in Tonkean macaques, for example, might be performed by the dominant individual in some
contexts, and its form has become blended with
that of an appeasement display, changing its social
function in this species (Preuschoft, 1992). The
same is true of the chimpanzee sbt display, which
is often used during sexual contacts, during play,
and during uncertainty (Parr et al., 2005; Waller
and Dunbar, 2005). In sum, the architecture of a
flexible social environment requires signals to have
meanings that are transferable across different situations and, as a consequence, the demands
placed on cognitive flexibility are increased as
species must develop strategies for dealing with
increasingly flexible communication systems (Parr
et al., 2005). If communicative signaling is additionally influenced by emotional state, it follows
that species living in complex social groups must
also possess well-developed emotional processing
skills, as they must be able to interpret the different
meanings associated with similar facial displays
used in different emotional contexts.
An addition to the cognitive complexity placed on
species living in relaxed dominance hierarchies, such
as the chimpanzee, is the nature of their society
itself. Chimpanzees, as is characteristic of most ape
societies, live in a dispersed social system, what is
referred to as a fissionfusion society. (Spider monkeys (Ateles spp.) are perhaps unique among
monkeys in that they have fissionfusion structure.)
In contrast to other primate group structures, fissionfusion societies are not characterized by
constant, gregarious, group living, where all individuals travel and sleep together, but instead each
chimpanzee community is composed of small foraging groups that unite after varying periods of time
(Nishida, 1979). The large complete group is, nonetheless, bonded interindividually, and complex,
long-term relationships exist among group members
(Goodall, 1986). This presents a taxing cognitive
challenge for these species as they must be able to
keep track of and remember not only their own
social relationships, but the relationships among
other individuals who they may not see together
for long periods of time. During that time, new
relationships may have formed and these social
changes must be processed in the absence of direct
experience, i.e., by directly observing and interpreting behavior with reference to previous knowledge.
A hypothesis to explain the relationship between
complex societies, advanced cognitive abilities, and
unusually large brain size compared to body size
among hominoids has been postulated. The social
brain hypothesis proposes that large neocortex
volume and superior sociocognitive skills coevolved to deal effectively with the increasing
demands stemming from large and complex social
groups and more specifically the increased number
of individual relationships that one can sustain
(Dunbar, 1998). Large brains, such as those present
in chimpanzees and humans, equaled better cognitive processing speed and the ability to keep track of
many individuals at once, including interindividual
relationships, and remember social events over
longer periods of time. In fact, the part of the brain
that shows the strongest relationship with group

complexity is the newer region of the neocortex, not
phylogenetically older regions, such as the amygdala
or areas of visual cortex (Joffe and Dunbar, 1997).
Moreover, Barrett et al. (2003) have suggested that
maintaining group cohesion in light of such temporal
and geographical distance is far more demanding in
terms of computational and cognitive load than a
group that preserves a constant grouping structure,
such as that found among most cercopithecines.
Therefore, there is compelling evidence that social
cognition and brain evolution are mutually
interactive.
In sum, facial cues may provide information
about the consequences of social interactions even
when group mates do not directly witness all the
details of those events. Thus, facial expressions can
be used not only to reason about the immediate
motivation of the signaler, i.e., they are upset,
hurt, or angry, but also to understand something
about an event that was not observable, i.e., a
change in social status. This distinction is similar to
what has been described as knowledge by acquaintance versus knowledge by description. Knowledge
by acquaintance is an innate understanding based
on direct immediate perceptual experience, has
been selected for throughout evolution, and is
commonly found in most animals. In contrast,
knowledge by description is a more general process
whereby experience, conditioning, and cognition
collectively provide the means to reconstruct raw
data into an internal representation of reality (see
Buck, 1999). Thus, this latter skill gives one the
ability to reason about events in which the details
of the events are not all immediately present.
Although this does not indicate that nonhuman
primates, such as chimpanzees, are able to attribute
or reason about the mental states of other individuals, an ability referred to as theory of mind,
this emotional reasoning ability, or emotional
awareness, allows them to infer something about
the quality of unobserved interactions among group
mates. In sum, emotional communication and emotional awareness facilitate social cohesion and
increases the quality of social relationships.
4.28.3.2 Social Emotions
Although researchers have described basic or biological emotions for several decades, some theorists
have begun describing a new generation of emotions
that appear to be specifically involved in social regulatory processes. These are considered secondary
emotions, or social emotions, given their function
in evaluating social interaction (Buck, 1999;
Keltner, 2003). Moreover, some of these social emotions have been viewed as moral, self-conscious
emotions as they occur in response to the violation
of social rules and moral behavior (Eisenberg, 2000),
require an understanding of the consequences of
ones actions and the expectations of others, and
function to promote reconciliation and apology
(Keltner and Buswell, 1997). These emotions are
considered unique to humans and, to date, there is
little justification to argue for their existence in
other animals (Harris, 2003).
Although there is no general agreement as to the
number of discrete social emotions, most theorists
agree that they require some degree of self-assessment, or self-consciousness, and an evaluation of
others compared to basic, or biological, emotions.
Bennett and Hacker (2005) have identified these
as pride, shame, humiliation, regret, remorse, and
guilt. Others have limited the self-conscious emotions to include embarrassment, pride, guilt, and
shame (Keltner and Buswell, 1997; Tangney et al.,
1996). Social emotions have also been regarded in
terms of their reciprocal contingencies, i.e., whether
the goal was achieved or not. These include pride/
guilt, envy/pity, joy/sorrow, arrogance/shame, and
jealousy/trust (Buck, 1999). Regardless of the number and/or psychological arrangement of these
emotions, they share in common a degree of selfconsciousness that is not typically invoked when
referring to basic emotions such as fear, anger, happiness, sadness, surprise, or disgust. That said, social
emotions are not always independent of biological
emotions and are often extensions of basic emotions
or include emotion blends.
4.28.3.2.1 Facial displays of pride, embarrassment,
guilt, and shame Distinct displays have been associated with pride, embarrassment, and shame. Pride,
for example, is associated with an upward head turn
(AU53) and slight Duchenne smile (AU6 + AU12)
with pressed lips (AU24) (Shiota et al., 2003). Pride
may be unique among the self-conscious emotions in
that it is associated with positive affect, like happiness, whereas most self-conscious emotions are
negative. Displays of pride may function to draw
social attention to the individual, signal success at a
socially valued endeavor, or highlight ones important status within the group (Shiota et al., 2003).
Unlike the basic emotion of happiness, however,
pride does not appear to be recognizable from the
face alone, with greatest recognition rates found in
forced-choice tasks involving entire body postures
(Tracy and Robins, 2003).
Embarrassment is described by a sequence of gaze
aversion and gazing downward, smiling and smile
463
control, a downward head turn to expose the neck,

and face touching (Keltner, 1995; Keltner and
Buswell, 1997). When these expressive components
occur together, embarrassment is recognized up to
92% of the time from its facial expression alone
(Keltner, 1995). This is comparable to, if not greater
than, recognition rates of basic emotions from their
expressive displays (see review by Fridlund, 1994).
According to several theories, embarrassment is
associated with an acute sense of how others evaluate their behavior and social identity (Tangney
et al., 1996). Thus, it can often occur when an
individual fails to act in accordance with these
socially defined conventions. These conventions
must be known by others; for example, one might
not experience embarrassment after tripping in a
private situation compared to tripping in public
(Keltner and Buswell, 1997). Moreover, the experience of embarrassment is less intense in the presence
of family and close friends, individuals who would
be very forgiving when social norms are violated,
than in the presence of strangers (Lewis et al., 1991).
Finally, theorists have speculated that embarrassment has evolutionary origins in the appeasement
behavior of animals. Appeasement, including bowing
the head, gaze aversion, and face touching in nonhuman primates, restores social harmony, decreases
the likelihood of future negative interactions and
aggression, and reduces the interindividual distance
among group members. Furthermore, these displays may have an earlier ontogenetic onset than
previously considered, with reports of coy smiles
appearing in human infants at approximately 23
months of age (Reddy, 2000). Thus, it functions
to restore relationships after social transgressions
(Keltner and Buswell, 1997).
Shame is typically displayed as a coordinated
sequence of downward gaze and head movements
and lowered posture. Shame typically occurs when
ones actions fail to live up to the expectations of
others, when ones personal standards are not met,
or when one fears criticism or disapproval from
others (Harris, 2003). Thus, shame necessitates an
understanding of the expectations of others, the
expectations of ones self, and the ability to weigh
ones own actions against them. Shame can, for
example, occur in the absence of onlookers and
appears to be most associated with failure to fulfill
obligations either to the self or to others (Tangney
et al., 1996). Guilt is similar to shame, but is different
in that the transgression involves deviation from a
moral rule or norm (Harris, 2003; Tangney, 1992).
Therefore, in general, guilt is more society-focused,
or focused on the specific behavior involved, whereas
shame is more self-focused. Although distinctions
can be drawn between shame and guilt, both of these

emotions correlate with feelings of empathy, suggesting a strong relationship between these emotions and
perspective taking (Harris, 2003). Although Tangney
(1991) found that when controlling for level of
shame, guilt was more associated with empathic
responsiveness than shame. There is no associated
facial expression or postural expressive pattern
described for guilt and it often results from the selfappraisal that one has put a low level of effort toward
a situation.
These last three emotions do not have known
correlates in nonhuman primates. Most of their
behavioral elements are similar to those described
for appeasement displays (Keltner and Buswell,
1997). Behavioral responses similar to shame, for
example, have been observed by the author in the
context of cognitive research on captive chimpanzees at the Yerkes Primate Center. Subjects are
typically tested in pairs, with one going first while
the other waits, and then their roles switch. This
sequence has been reinforced for over 10 years of
studies and very rarely does the subject waiting
misbehave. If such misbehavior occurs, subjects
might grab at the experimenter, or attempt to distract the testing subject by grabbing his/her hands
away from the joystick, soliciting play, etc. When
this behavior is discouraged by the experimenter,
the chimpanzee will often lower its face, rubbing it
with its hands, close its eyes tightly, and retreat to a
corner of the enclosure. Although these are anecdotes and do not occur frequently, they suggest
that the subjects understand the rules of the game
and when their attempts to disrupt these conventions cause them to be scolded by the
experimenter, they express behavior roughly consistent with the shame/guilt descriptions provided
above.
4.28.3.2.2 Asymmetrical versus symmetrical facial
expressions Another aspect of social emotions
that makes them distinctive from basic emotions is
that they often involve more exaggerated forms of
expression and are often more asymmetrical. These
exaggerations, or embellishments, can include winks
or brow raises that are typically unilateral in their
execution. The wink, for example, involves the eye
closing (action unit LAU46), which can refer to a
private message, be suggestive, or teasing. A unilateral outer eyebrow lift (LAU2) can be questioning,
doubtful, or an expression of interest. The unilateral
upper lip raise (LAU10) and the unilateral nose wrinkle (LAU9) are typically involved in expressions of
contempt or disgust. More specifically, contempt has
been shown to involve a unilateral lip corner raise
and tighten (LAU12 + LAU14; Matsumoto and

Ekman, 2004). Although contempt is often referred
to as a basic emotion, this is debated in the literature
(Izard and Haynes, 1988) and studies have shown
that scenarios involving contempt can indicate an
assessment of anothers low social status or ones
own demonstration of moral superiority (Keltner
and Haidt, 1999). It is unclear, although doubtful,
that such embellishments or patterns of asymmetry
are present in nonhuman primates despite findings
that many of their basic expressions involve asymmetrical components (Fernandez-Carriba et al., 2002).
These asymmetries reflect a greater intensity of the
displays associated with one side of the face or the
other and do not involve the inclusion of unilateral
embellishments.
4.28.3.3 Brain Systems Involved in Social
Emotions
In a review of neuroimaging studies of emotion,

Phan et al. (2002) conducted a meta-analysis of emotion studies using both positron emission
tomography and functional magnetic resonance
imaging (fMRI). This included 55 studies using only
healthy human subjects published through the year
2000. They further categorized studies according
to whether the task involved a distinct cognitive
component, such as emotion naming, emotion
identification or ratings, and recall/encoding or
recognition, or noncognitive tasks involving the passive presentation of emotional stimuli. The results
revealed the most commonly activated region,
regardless of the type of task or emotion employed
in the study, to be the medial prefrontal cortex
(MPFC). Researchers have, for example, consistently
reported activation of the MPFC during the processing of photographs designed to elicit either pleasant
or unpleasant emotion, compared to neutral photographs (George et al., 1993; Kesler-West et al., 2001;
Lane et al., 1997). Specifically, the rostralventral
area of the MPFC has been shown to respond to
individual emotions (BA9 + BA10). This region
extends into the anterior, emotion-processing region
of the cingulate cortex, which will be discussed
below. Moreover, this region is separable from
the orbitofrontal region (BA11 + BA12), which,
although associated with processing positive and
negative emotional images, is thought to play a predominant role in the monitoring and evaluation of
the quality of social versus nonsocial information
(Damasio et al., 2000; Northoff et al., 2000).
The emotion of fear was found to be strongly
associated with activity in the amygdala (Phan
et al., 2002). This finding supports data from
numerous areas of psychology and neuroscience

that have shown the amygdala to involve a direct,
fast-acting pathway for the precognitive and emotional aspects of stimulus processing. The amygdala
has been implicated in the processing of fearful
facial expressions, whether processed implicitly or
explicitly (see The Development and Evolutionary
Expansion of the Cerebral Cortex in Primates;
Adolphs, 1999; Morris et al., 1998; Whalen et al.,
1998), during fear conditioning (Davis, 2000;
LeDoux, 2000), and in phobias (Lang et al., 2000).
Because of the primacy of fear processing in the
amygdala, and its association with implicit autonomic arousal, some researchers have speculated
that the amygdala is not so much tied to the processing of basic fearful stimuli, but rather is tuned to
detect salient stimuli in the environment, even at
subconscious levels (LeDoux, 2000). Therefore,
the amygdala is critically involved in aiding the
allocation of necessary biological resources to aid
the organisms response to potentially threatening
environmental stimuli.
The region of the cingulate cortex is interesting for
the processing of emotion because it bridges the
numerous brain areas including the amygdala and
orbitofrontal cortex (OFC). Numerous studies have
identified activity in the anterior cingulate in
response to emotion processing (Damasio et al.,
2000; George et al., 1993; Keightley et al., 2003;
Lane et al., 1998). Additionally, the cingulate gyrus
can be divided into a rostralventral region (BA25,
BA33, and the rostral portion of BA24) that is
involved in emotional awareness, and a more dorsal
region that is involved in cognition and attention
(Drevets and Raichle, 1998). Researchers have
demonstrated selective activation of both the MPFC
and the anterior cingulate when subjects were
required to make an emotional appraisal of photographs, but activations were restricted to the
amygdala and insular regions when the task involved
only passive viewing, suggesting the specific involvement of these regions in more attentive, selfconscious emotion processing (Taylor et al., 2000).
Interestingly, researchers have identified the presence of specialized projection neurons in layer
V-b of the anterior cingulate cortex in great apes
and humans, but not in gibbons or monkeys
(Nimchinsky et al., 1999). These cells, referred to
as spindle cells because of their shape, might play a
key role in the integration of sensory inputs related
to emotion, vocal production, and the recognition of
emotional faces, as described above. They lie in a
region of the cingulate just superior to the genu of
the corpus callosum (BA24), a region shown to be
active during the recall of guilt emotions by Shin
465
et al. (2000), described below. Thus, the anterior

cingulate appears to play an important role in the
processing of emotion, particularly when the emotion is explicitly evaluated, or processed with
specific reference to the self, and these specializations may be unique to hominoids.
Although numerous studies have examined the
neural responses to basic emotions, some of which
are described above, fewer studies have examined
self-conscious emotions or those that may involve
perspective-taking skills (Phan et al., 2002).
Takahashi et al. (2004), for example, measured
brain activity using fMRI as subjects were asked to
rate the emotional content of short sentences
describing situations of guilt or embarrassment.
They revealed greater activation in the MPFC, left
posterior superior temporal sulcus (STS), and visual
cortex. Embarrassment was also associated with
greater activation in the left OFC, anterior temporal
cortex, and the anterior right temporal cortex.
Distinguishing the two categories of emotion, however, was the finding of greater activation of the
right temporal cortex, bilateral hippocampus, and
visual cortex for embarrassment and greater activation of the MPFC for guilt (Takahashi et al., 2004).
Shin et al. (2000) found greater activation of the
anterior temporal poles, anterior cingulate gyrus,
and left anterior insular cortex during a relived-emotions task involving guilt than during a task involving
neutral emotion. Thus, it appears from the associated
brain regions that guilt involves more self-conscious
emotion processing than does embarrassment.
When comparing responses to self-conscious emotions that involved either intentional or unintentional
(embarrassing) violations of social norms using
fMRI, Berthoz et al. (2002) found greater activity in
the left medial and superior prefrontal cortex, anterior cingulate gyrus, left inferior parietal cortex, and
left superior occipital gyrus. Specific judgments involving moral issues activated anterior prefrontal cortex
(BA9 + BA10), posterior cingulate (BA31), and angular gyrus (BA39) (Greene et al., 2001). Moll and
colleagues reported activation in similar regions: the
MPFC, anterior temporal cortex, angular gyrus, and
globus pallidus; however, in another study, they
included an important control for the neural systems
activated by emotion judgments by presenting moral
and nonmoral emotional stimuli (Moll et al., 2002).
Regions activated during the nonmoral condition
included the amygdala, lateral OFC, and some areas
of visual cortex. Moral judgments, however, activated the medial OFC, left temporal pole, and STS
in a region near the angular gyrus. Comparing the
two regions revealed selective activation of the medial OFC and STS in the moral compared to the
nonmoral condition. Thus, moral emotion judgments

appear to exclusively activate OFC and STS and can
be distinguished from self-conscious emotions that
additionally activated the medial prefrontal cortex,
portions of temporal cortex, and anterior cingulate
cortex (Moll et al., 2002).
Self-conscious emotions are, thus far, uniquely
human traits and appear to be integrally associated
with brain structures that also subserve theory of
mind skills, including the medial prefrontal cortex,
the anterior cingulate cortex, and the orbitofrontal
cortex, as described above. Studies have examined
the recognition of self-conscious emotions and their
association with theory of mind skills in autistic
children. Autism is a pervasive developmental
disorder characterized by impaired language function, decreased social responsiveness, deficits in
communication and emotional expressiveness, and
repetitive or stereotypical behavior before the age of
3 years. Individuals diagnosed with autism spectrum
disorder also have poorly developed perspectivetaking skills (Dawson et al., 2002) and lack of
empathy and theory of mind (Baron-Cohen et al.,
2001; Joseph and Tager-Flusberg, 2004; Mundy,
2003). Impairments in joint attention skills in autistic individuals, for example, are more strongly
correlated with impairments in tasks that rely on
the ventromedial prefrontal cortex, an area that is
associated with general affective, motivational, and
social behavior (Dawson et al., 2002). Heerey et al.
(2003) examined the ability of autistic children to
identify from photographs both self-conscious emotions, such as embarrassment and shame, and nonself-conscious emotions, such as contempt, anger,
disgust, fear, happiness, sadness, and surprise.
They found that the children with autism showed
no differences in their ability to identify the non-selfconscious emotions compared to the control children, and these scores were uncorrelated with
theory of mind skills, but the autistic children
were significantly impaired in recognizing the
self-conscious emotions. In addition, for both
groups of children, their performance on selfconscious emotions was significantly correlated
with their theory of mind skills (Heerey et al.,
2003). Hillier and Allinson (2002) examined the
responses of children with and without autism to
several levels of embarrassment: one in which the
individuals behavior is conspicuous to others, one
in which the individual takes into consideration
how the audience evaluates his or her behavior,
and one in which the embarrassing event happens
to a friend. As opposed to other studies, children
with autism showed deficits only when interpreting
scenes of empathic embarrassment the last
scenario, in which the embarrassing event happens

to the friend of the storys protagonist and the subject was asked to rate how the protagonist felt
(Hillier and Allinson, 2002). Thus, their deficits in
embarrassment occurred only in the context of
empathic awareness.
Self-conscious social emotions, such as those
described above, do not take the place of more
primitive, basic emotions that are primarily under
the control of subcortical structures and their
interconnections. As Berridge (2003) has stated, subcortical systems do not lose their basic function in
higher organisms, but they may give up some of
their autonomy in terms of the degree to which higher
cortical systems can modulate their functions or regulate the emotional experience. Emotion regulation is
a growing area of research that will reveal important
new insights into the role of specific brain regions
involved in the cognitive control of emotion. These
areas are, not surprisingly, similar to the brain areas
involved in self-conscious emotions, most
specifically the medial and lateral prefrontal cortices and anterior cingulate cortex (Beauregard et al.,
2001). What may fundamentally differ between
humans and other animals, despite the evolutionary
similarity in the organization of basic emotive brain
circuits and connectivity (LeDoux, 2000), is the likelihood that these circuits have more elaborate,
reciprocal connections to higher cortical areas
involved in both the self-regulation of emotion and
the experience of self-conscious emotions. These reciprocal interconnections provide the individual with
information as to the nature and meaning of their
emotional experiences (Panksepp, 1982).
4.28.3.4 Precursors in the Evolution of Human
Emotion: A Final Word
This article has drawn a rough trajectory through

various aspects of emotion and its impact on
communication and the organization of primate
societies, from reflexive, biologically adaptive behaviors to complex social interactions. The important
theme therein is that in primates, both human and
nonhuman, the ability to understand emotion in
others is critical for maintaining social interactions.
One way in which individuals are able to learn
about the emotional states of others is through the
process of emotional contagion. Primitive emotional contagion has been referred to as . . . the
tendency to automatically mimic and synchronize
expressions, vocalizations, postures and movements
with those of another person and, consequently,
to converge emotionally (Hatfield et al., 1994,
p. 153). Although this definition might be somewhat
limited, it does present a basis for comparative studies on the evolution of emotion across multiple
modalities, e.g., face, voice, and posture, in which
the presence, absence, or intensity of mimetic
convergence across individuals can be empirically
measured. Emotional contagion also describes a
mechanism for the interpersonal sharing of emotion,
or empathy, which features a matching of internal
states between individuals, in that individuals will
converge emotionally through the mimetic synchrony
of behavioral expression. This emotional synchrony
can be more specifically referred to as a kind of
resonance of physiological arousal between the
individuals. Similar changes in arousal between individuals can, under some conditions, result in similar
subjective feelings that can significantly affect the
subsequent behavior and emotional experience of
the observer in the absence of conscious awareness
(Dimberg, 1987; Vaughan and Lanzetta, 1980). This
type of emotional awareness, or low-level empathy,
functions to coordinate activity among group
members, facilitate social cohesion, and motivate
conciliatory tendencies and is likely to play a key
role in coordinating social behaviors in large-brained
social primates, such as hominoids.
Evidence for behavioral synchrony is widely
reported among numerous animal species from
schooling fish to the synchronized flying behavior
of birds. Researchers have reported evidence of contagious yawning in adult chimpanzees in response to
a video showing a conspecifics yawning compared
to conspecifics with open mouths (Anderson et al.,
2004). Thus, only the actual behavior and not
relevant aspects of the perceptual features of the
behavior were important to elicit this behavior,
similar to the data on reflexive crying in human
neonates, in which only the cries of age-matched
infants could elicit crying in subjects (Sagi and
Hoffman, 1976). Among primates, behavioral synchrony also takes the form of basic imitation. Infant
chimpanzees, like human neonates, have been
shown to imitate facial expressions shortly after
birth (Bard, 1998). Specifically, MyowaYamakoshi (1996) demonstrated facial imitation in
an infant chimpanzee between 5 and 11 weeks of
age, including mouth opening, tongue protrusion,
and lip protrusion, in response to posed expressions
by an experimenter. Notably, after 12 weeks, the
infant chimpanzee showed a marked decrease in
imitative performance (Myowa-Yamakoshi, 1996).
A similar study reported facial imitation in two
infant chimpanzees reared by their mothers within
their first week of life (Myowa-Yamakoshi et al.,
2004). These infants imitated a human who demonstrated mouth opening and tongue protrusion, but
467
this ability declined after 9 weeks of age, suggesting

that this innate ability seen in neonates might be
replaced by more socially communicative behaviors
early in development, similar to what is reported in
human infants (see Neurological Specializations for
Manual Gesture and Tool Use in Humans; Meltzoff
and Moore, 1977; Myowa-Yamakoshi et al., 2004).
According to these examples, neonatal imitation
is an innate/contagious process that provides not
only valuable sensorimotor feedback for matching
the behavioral state of another, but also provides an
avenue for proprioceptive feedback that may facilitate an understanding of the relationship between
facial expression and emotional responses. The
importance of this relationship for emotional communication was reviewed in Section 4.28.2.
Proprioceptive feedback, or affective resonance, in
the form of physiological changes can easily become
conditioned to specific internal or external events
facilitating the likelihood that an individual,
whether human or nonhuman, will show a similar
emotional response in a future context. Therefore,
one individuals emotional reactions may be considered a conditioned stimulus for unconditioned
emotional responses in an observer (Vaughan and
Lanzetta, 1980). Through these basic contagion
processes, individuals come to learn about their
own emotional states and the relationship between
these and others emotions during early ontogeny.
As a consequence, emotional contagion and its
affective resonance is one of the most powerful
mechanisms for transmitting emotional information
and facilitating coordinated actions and feelings
among social animals.
From an evolutionary perspective, it is not surprising that one of the primary modalities for the
transmission of emotional information is through
the face. This article has highlighted some of the
important issues in understanding the evolution of
human emotion. Section 4.28.1 described the adaptive function of emotion in aiding the survival of
living organisms. These innate biological reflexes
include facial expressions and body postures that
appear more tuned to processing negative information rapidly at high levels of arousal. Section
4.28.2 described the need for social animals to communicate about emotion and the importance of the
face in affective communication. This section revealed
that one of the primary modes for expressing emotion
and reading emotional signals from others shares
homologous mechanisms in humans and some nonhuman primates. Finally, Section 4.28.3 introduced
the presence of self-conscious or social emotions and
their relationship to specific brain regions that not
only differ from regions involved in basic emotions
but also appear to overlap with brain regions subserving moral problem-solving and theory of mind.
These emotions may be unique to humans. Although
some have suggested that chimpanzees might share
mental reasoning abilities, such as theory of mind,
with humans (Hare et al., 2001; Tomasello et al.,
2003), the data are scarce and limited to situations
in which individuals compete for food. Thus, though
clearly one role of emotion is to help an organism
respond rapidly and unconditionally to life-threatening situations with adaptive behavior that increases
survival, these emotion systems and the behaviors
they produce are also highly dependent on an individuals life history, early experience, and cognitive
perceptions in a complex social environment. Thus,
one of the key roles of emotions is to free the individual from responding unconditionally. This provides
humans, and perhaps related species, with a greater
ability to speculate about emotion, engage in emotionally complex relationships, and attribute
emotional states to others.
References
Adolphs, R. 1999. Social cognition and the human brain. Trends
Cogn. Sci. 3, 469479.
Allman, J. M., Hakeem, A., Erwin, J. M., Nimchinsky, E., and
Hof, P. 2001. The anterior cingulate cortex: The evolution of
an interface between emotion and cognition. Ann. NY Acad.
Sci. 935, 107117.
Anderson, J. R., Myowa-Yamakoshi, M., and Matsuzawa, T.
2004. Contagious yawning in chimpanzees. Proc. R. Soc.
Lond. B 271, S468S470.
Andrew, R. J. 1963. The origin and evolution of the calls and
facial expressions of the primates. Behaviour 20, 1109.
Aureli, F., Cozzolino, R., Cordischi, C., and Schucchi, S. 1992.
Kin-oriented redirection among Japanese macaques: An
expression of a revenge system? Anim. Behav. 44, 283291.
Bard, K. A. 1998. Social-experiential contributions to imitation
and emotion in chimpanzees. In: Intersubjective
Communication and Emotion in Early Ontogeny
(ed. S. Braten), pp. 208227. Cambridge University Press.
Bargh, J. A., Chaiken, S., Raymond, P., and Hymes, C. 1996. The
automatic evaluation effect: Unconditional automatic attitude
activation with a pronunciation task. J. Exp. Soc. Psychol. 32,
104128.
Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., and Plumb, I.
2001. The Reading the Mind in the Eyes test revised version:
A study with normal adults, and adults with Asperger syndrome or high-functioning autism. J. Child Psychol. Psychiat.
42, 241251.
Barrett, L., Henzi, P., and Dunbar, R. I. M. 2003. Primate cognition: From what now? to what if? Trends Cogn. Sci. 7,
494497.
Beauregard, M., Levesque, J., and Bourgouin, P. 2001. Neural
correlates of conscious self-regulation of emotion.
J. Neurosci. 21, 16.
Bennett, M. R. and Hacker, P. M. S. 2005. Emotion and cortical
subcortical function: Conceptual developments. Prog.
Neurobiol. 75, 2952.
Berridge, K. 1996. Food reward: Brain substrates of wanting and

liking. Neurosci. Biobehav. Rev. 20, 125.
Berridge, K. 2003. Comparing the emotional brains of humans
and other animals. In: Handbook of Affective Sciences
(eds. R. J. Davidson, K. R. Scherer, and H. Hill Goldsmith),
pp. 2551. Oxford University Press.
Berthoz, S., Armony, J. L., Blair, R. J. R., and Dolan, R. J. 2002.
An fMRI study of intentional and unintentional (embarrassing) violations of social norms. Brain 125, 16961708.
Boesch, C. 2002. Cooperative hunting roles among Tai chimpanzees. Hum. Nat. Interdisc. Biosoc. Perspect. 13, 2746.
Buck, R. 1999. The biological affects: A typology. Psychol. Rev.
106, 301336.
Burrows, A. M., Waller, B. M., Parr, L. A., and Bonar, C. J. 2006.
Muscles of facial expression in the chimpanzee (Pan troglodytes): Descriptive, comparitive and phylogenetic contexts.
J. Anat. 208, 153168.
Cacioppo, J. T. and Berntson, G. G. 1992. Social psychology
contributions to the decade of the brain. Am. Psychol. 47,
10191028.
Cacioppo, J. T. and Berntson, G. G. 1994. Relationship between
attitudes and evaluative space: A critical review, with emphasis on the separability of positive and negative substrates.
Psychol. Bull. 115, 401423.
Cacioppo, J. T. and Gardner, W. L. 1999. Emotion. Annu. Rev.
Psychol. 50, 191214.
Cacioppo, J. T., Priester, J. R., and Berntson, G. G. 1993.
Rudimentary determinants of attitudes. II: Arm flexion and
extension have differential effects on attitudes. J. Pers. Soc.
Psychol. 65, 517.
Cacioppo, J. T., Gardner, W. L., and Berntson, G. G. 1999. The
affect system has parallel and integrative processing components: Form follows function. J. Pers. Soc. Psychol. 76,
839855.
Call, J., Judge, P. G., and de Waal, F. B. M. 1996. Influence of
kinship and spatial density on reconciliation and grooming in
rhesus monkeys. Am. J. Primatol. 39, 3545.
Cartmill, M. 1994. A critique of homology as a morphological
concept. Am. J. Phys. Anthropol. 94, 115123.
Chen, M. and Bargh, J. A. 1999. Consequences of automatic
evaluation: Immediate behavioral predispositions to
approach or avoid the stimulus. Pers. Soc. Psychol. Bull.
25, 215224.
Cheney, D. L. and Seyfarth, R. M. 1990. How Monkeys See The
World. University of Chicago Press.
Damasio, A. R., Grabowski, T. J., Bechara, A., et al. 2000.
Subcortical and cortical brain activity during the feeling of
self-generated emotions. Nat. Neurosci. 3, 10491056.
Darwin, C. 1872. Expression of the Emotions in Man and
Animals. 1955. Reprint, Philosophical Library.
Davis, M. 2000. The role of the amygdala in conditioned
and unconditioned fear and anxiety. In: The Amygdala
(ed. J. P. Aggleton), vol. 2, pp. 213287. Oxford
University Press.
Dawson, G., Munson, J., Estes, A., et al. 2002. Neurocognitive
function and joint attention ability in young children with
autism spectrum disorder versus developmental delay. Child
Dev. 73, 345358.
de Waal, F. B. M. 1982. Chimpanzee Politics: Power and Sex
among Apes. Johns Hopkins University Press.
de Waal, F. B. M. 1988. The communicative repertoire of captive
bonobos (Pan paniscus), compared to that of chimpanzees.
Behaviour 106, 183251.
de Waal, F. B. M. 1989. Peacemaking among Primates. Harvard
University Press.

de Waal, F. B. M. 1997. The chimpanzee service economy: Food
for grooming. Evol. Hum. Behav. 18, 375386.
de Waal, F. B. M. and Luttrell, L. M. 1985. The formal hierarchy
of rhesus macaques: An investigation of the bared-teeth display. Am. J. Primatol. 9, 7385.
Dimberg, U. 1987. Facial reactions, autonomic activity and
experienced emotion: A three component model of emotional
conditioning. Biol. Psychol. 24, 105122.
Drevets, W. C. and Raichle, M. E. 1998. Reciprocal suppression
of regional cerebral blood flow during emotional versus
higher cognitive processes: Implications for interactions between emotion and cognition. Cogn. Emot. 12, 353385.
Duchenne de Boulogne, G. B. 1862. The Mechanism of Human
Facial Expression (ed., transl., R. A. Cuthbertson), 1990.
Reprint, Cambridge University Press.
Duckworth, K. L., Bargh, J. A., Garcia, M., and Chaiken, S.
2002. The automatic evaluation of novel stimuli. Psychol.
Sci. 13, 513519.
Dunbar, R. I. M. 1998. The social brain hypothesis. Evol.
Anthropol. 6, 178190.
Eisenberg, N. 2000. Emotion, regulation, and moral development. Annu. Rev. Psychol. 51, 665697.
Ekman, P. 1972. Universals and cultural differences in facial
expressions of emotion. In: Nebraska Symposium on
Motivation (ed. J. Cole), vol. 19, pp. 207283. University of
Nebraska Press.
Ekman, P. 1977. About brows: Emotional and conversational
signals. In: Human Ethology: Claims and Limits of a New
Discipline (eds. M. von Cranach, K. Foppa, W. Lepenies, and
D. Ploog), pp. 169202. Cambridge University Press.
Ekman, P. 1992. An argument for basic emotions. Cogn. Emot. 6,
169200.
Ekman, P. and Friesen, W. V. 1971. Constants across cultures in
the face and emotion. J. Pers. Soc. Psychol. 17, 124129.
Ekman, P. and Friesen, W. V. 1975. Unmasking the Face. Prentice
Hall.
Ekman, P. and Friesen, W. V. 1978. Facial Action Coding System.
Consulting Psychology Press.
Ekman, P. and Friesen, W. V. 1982. Felt, false and miserable
smiles. J. Nonverbal Behav. 6, 238252.
Ekman, P., Friesen, W. V., and OSullivan, M. 1988. Smiles when
lying. J. Pers. Soc. Psychol. 54, 414420.
Elfenbein, H. A. and Ambady, N. 2003. When familiarity breeds
accuracy: Cultural exposure and facial emotion recognition.
J. Pers. Soc. Psychol. 85, 276290.
Fernandez-Carriba, S., Loeches, A., Morcillo, A., and
Hopkins, W. D. 2002. Asymmetry in facial expressions of
emotions by chimpanzees. Neuropsychologia 40, 15231533.
Frank, M. G., Ekman, P., and Friesen, W. V. 1993. Behavioral
markers and recognizability of the smile of enjoyment. J. Pers.
Soc. Psychol. 64, 8393.
Fridlund, A. J. 1994. Human Facial Expression. Academic Press.
Frijda, N. H. 1986. The Emotions. Cambridge University Press.
George, M. S., Ketter, T. A., Gill, D. S., et al. 1993. Brain regions
involved in recognizing facial emotion or identity: An oxygen15 PET study. J. Neuropsychiat. 5, 384391.
Goodall, J. 1986. The Chimpanzees of Gombe: Patterns of
Behavior. The Belknap Press of Harvard University Press.
Goodall, J. v. L. 1968. A preliminary report on expressive movements and communication in the Gombe stream chimpanzees.
In: Primates: Studies in Adaptation and Variability
(ed. P. C. Jay), pp. 313519. Holt, Rinehart and Winston.
Greene, J. D., Sommerville, R. B., Nystrom, L. E., Darley, J. M.,
and Cohen, J. D. 2001. An fMRI investigation of emotional
engagement in moral judgement. Science 293, 21052108.
469
Hare, B., Call, J., and Tomasello, M. 2001. Do chimpanzees

know what conspecifics know? Anim. Behav. 61, 139151.
Harlow, H. F. and Mears, C. E. 1983. Emotional sequences
and consequences. In: Emotion: Theory, Research, and
Experience (eds. R. Plutchik and H. Kellerman), vol. 2,
pp. 171197. Academic Press.
Harlow, H. F., Harlow, M. K., and Suomi, S. J. 1971. From
thought to therapy: Lessons from a primate laboratory. Am.
Sci. 59, 538549.
Harris, N. 2003. Reassessing the dimensionality of the moral
emotions. Br. J. Psychol. 94, 457473.
Hatfield, E., Cacioppo, J. T., and Rapson, R. L. 1994. Emotional
Contagion. Cambridge University Press.
Heerey, E. A., Keltner, D., and Capps, L. M. 2003. Making sense
of self-conscious emotion: Linking theory of mind and emotion in children with autism. Emotion 3, 394400.
Henzi, S. P. and Barrett, L. 2002. Infants as a commodity in a
baboon market. Anim. Behav. 63, 915921.
Hillier, A. and Allinson, L. 2002. Understanding embarrassment
among those with autism: Breaking down the complex emotion of embarrassment among those with autism. J. Autism
Dev. Disord. 32, 583592.
Hinde, R. A. and Rowell, T. E. 1962. Communication by postures and facial expressions in the rhesus monkey (Macaca
mulatta). Proc. Zool. Soc. Lond. 138, 121.
Huber, E. 1931. Evolution of Facial Musculature and Facial
Expression. Oxford University Press.
Ito, T. A. and Cacioppo, J. T. 2000. Electrophysiological evidence
of implicit and explicit categorization processes. J. Pers. Soc.
Psychol. 36, 660676.
Ito, T. A., Larsen, J. T., Kyle Smith, N., and Cacioppo, J. T. 1998.
Negative information weighs more heavily on the brain: The
negativity bias in evaluative categorizations. J. Pers. Soc.
Psychol. 75, 887900.
Izard, C. 1971. Human Emotions. Plenum.
Izard, C. E. 1994. Innate and universal facial expressions:
Evidence from developmental and cross-cultural research.
Psychol. Bull. 115, 288299.
Izard, C. E. and Haynes, O. M. 1988. On the form and universality of the contempt expression: A challenge to Ekman and
Friesens claim of discovery. Motiv. Emot. 12, 116.
Joffe, T. H. and Dunbar, R. I. M. 1997. Visual and socio-cognitive
information processing in primate brain evolution. Proc. R.
Soc. Lond. B 264, 13031307.
Joseph, R. M. and Tager-Flusberg, H. 2004. The relationship of
theory of mind and executive functions to symptom type and
severity in children with autism. Dev. Psychopathol. 16,
137155.
Judge, P. G. and Mullen, S. H. 2005. Quadratic postconflict
affiliation among bystanders in a hamadryas baboon group.
Anim. Behav. 69, 13451355.
Kappas, A. 2002. The science of emotion as a multidisciplinary
research paradigm. Behav. Proc. 60, 8598.
Keightley, M. L., Wincour, G., Graham, S. J., Mayberg, H. S.,
Hevenor, S. J., and Grady, C. L. 2003. An fMRI study investigating cognitive modulation of brain regions associated with
emotional processing of visual stimuli. Neuropsychologia 41,
585596.
Keltner, D. 1995. The signs of appeasement: Evidence for the
distinct displays of embarrassment, amusement, and shame.
Keltner, D. 2003. Expressions and the course of life:
Studies of emotion, personality, psychopathology from a
socialfunctional perspective. Ann. NY Acad. Sci. 1000,
222243.

Keltner, D. and Buswell, B. N. 1997. Embarrassment: Its distinct
form and appeasement functions. Psychol. Bull. 122, 250270.
Keltner, D. and Haidt, J. 1999. Social functions of emotions at
four levels of analysis. Cogn. Emot. 13, 505521.
Kesler-West, M. L., Andersen, A. H., Smith, C. D., et al. 2001.
Neural substrates of facial emotion processing using fMRI.
Cogn. Brain Res. 11, 213226.
Kohler, C. G., Turner, T., Stolar, N. M., et al. 2004. Differences
in facial expressions of four universal emotions. Psychiatry
Res. 128, 235244.
Krumhuber, E. and Kappas, A. 2005. Moving smiles: The role of
dynamic components for the perception of the genuineness of
smiles. J. Nonverbal Behav. 29, 324.
Lane, R. D., Reiman, E. M., Bradley, M. M., et al. 1997.
Neuroanatomical correlates of pleasant and unpleasant emotion. Neuropsychologia 35, 14371444.
Lane, R. D., Reiman, E. M., Axelrod, B., Yun, L., Holmes, A.,
and Schwartz, G. E. 1998. Neural correlates of levels of emotional awareness: Evidence of an interaction between emotion
and attention in the anterior cingulate cortex. J. Cogn.
Neurosci. 10, 525535.
Lang, P. J., Davis, M., and Ohman, A. 2000. Fear and anxiety:
Animal models of human cognitive psychophysiology.
J. Affect. Disord. 61, 137159.
Lauder, G. V. 1994. Homology, form, and function.
In: Homology: The Hierarchical Basis of Comparative
Biology (ed. B. K. Hall), pp. 151196. Academic Press.
LeDoux, J. E. 2000. Emotion circuits in the brain. Annu. Rev.
Neurosci. 23, 155184.
Levenston, G. K., Patrick, C. J., Bradley, M. M., and Lang, P. J.
2000. The psychopath as observer: Emotion and attention in
picture processing. J. Abnormal Psychol. 109, 373385.
Leventhal, H. 1991. Emotion: Prospectus for conceptual
and empirical development. In: Perspectives on Cognitive
Neuroscience (eds. R. G. Lister and H. J. Weingartner),
pp. 325348. Oxford University Press.
Lewis, M., Stanger, C., Sullivan, M. W., and Barone, P. 1991.
Changes in embarrassment as a function of age, sex and
situation. Br. J. Dev. Psychol. 9, 485492.
MacLean, P. D. 1949. Psychosomatic disease and the visceral
brain: Recent developments bearing on the Papez theory of
emotion. Psychosom. Med. 11, 338353.
Marler, P. 1965. Communication in monkeys and apes.
In: Primate Behavior (ed. I. DeVore), pp. 544584. Holt,
Rinehart and Winston.
Matrinez, A. M. and Benavente, R. 1998. The AR Face Database.
CVC Technical Report No. 24.
Matsumoto, D. and Ekman, P. 2004. The relationship among
expressions, labels, and descriptions of contempt. J. Pers.
Matsumoto, D., Yoo, S., Hirayama, S., and Petrova, G. 2005.
Development and validation of a measure of display rule
knowledge: The display rule assessment inventory. Emotion
5, 2340.
Meltzoff, A. N. and Moore, M. K. 1977. Imitation of facial and
manual gestures by human neonates. Science 198, 7578.
Mendelson, M. J., Haith, M. M., and Goldman-Rakic, P. S. 1982.
Face scanning and responsiveness to social cues in infant
rhesus monkeys. Dev. Psychol. 18, 222228.
Miller, R. E., Murphy, J. V., and Mirsky, I. A. 1959. Relevance of
facial expression and posture as cues in communication of
affect between monkeys. Arch. Gen. Psychiatry 1, 480488.
Miller, R. E., Banks, J. H. J., and Ogawa, N. 1963. Role of facial
expressions in cooperative avoidance conditioning in monkeys. J. Abnormal Soc. Psychol. 67, 2430.
Moll, J., de Oliveira-Souza, R., Bramati, I. E., and Grafman, J.

2002. Functional networks in emotional moral and nonmoral
social judgments. Neuroimage 16, 696703.
Morris, J. S., Ohman, A., and Dolan, R. J. 1998. Conscious and
unconscious emotional learning in the human amygdala.
Nature 393, 467470.
Mundy, P. 2003. Annotation: The neural basis of social impairments in autism: The role of the dorsal medialfrontal cortex
and anterior cingulate system. J. Child Psychol. Psychiat. 44,
793809.
Murphy, S. T. and Zajonc, R. B. 1993. Affect, cognition and
awareness: Affective priming with optimal and suboptimal
stimulus exposures. J. Pers. Soc. Psychol. 64, 723739.
Myowa-Yamakoshi, M. 1996. Imitation of facial gestures by an
infant chimpanzee. Primates 37, 207213.
Myowa-Yamakoshi, M., Tomonaga, M., Tanaka, M., and
Matsuzawa, T. 2004. Imitation in neonatal chimpanzees
(Pan troglodytes). Dev. Sci. 7, 437442.
Nelson, C. A. 1987. The recognition of facial expressions in the
first two years of life: Mechanisms and development. Child
Dev. 58, 889909.
Nimchinsky, E. A., Gilissen, E., Allman, J. M., Perl, D. P.,
Erwin, J. M., and Hof, P. R. 1999. A neuronal morphologic
type unique to humans and great apes. Proc. Natl. Acad. Sci.
USA 96, 52685273.
Nishida, T. 1979. The social structure of chimpanzees of the
Mahale Mountains. In: The Great Apes (eds. D. A. Hamberg
and E. R. McCowen), pp. 73121. Benjamin-Cummings.
Noe, R. and Hammerstein, P. 1995. Biological markets. Trends
Ecol. Evol. 10, 336339.
Northoff, G., Richter, A., Gessner, M., et al. 2000. Functional
dissociation between medial and lateral prefrontal cortical
spatiotemporal activation in negative and positive emotions:
A combined fMRI/MEG study. Cereb. Cortex 10, 93107.
Panksepp, J. 1982. Toward a general psychobiological theory of
emotions. Behav. Brain Sci. 5, 407467.
Parr, L. A. 2001. Cognitive and physiological markers of emotional awareness in chimpanzees, Pan troglodytes. Anim.
Cogn. 4, 223229.
Parr, L. A., Cohen, M., and de Waal, F. B. M. 2005. The influence
of social context on the use of blended and graded facial
displays in chimpanzees (Pan troglodytes). Int. J. Primatol.
26, 73103.
Parvizi, J., Anderson, S. W., Martin, C. O., Damasio, H., and
Damasio, A. R. 2001. Pathological laughter and crying, a link
to the cerebellum. Brain 124, 17081719.
Paul, E. S., Harding, E. J., and Mendl, M. 2005. Measuring
emotional processes in animals: The utility of a cognitive
approach. Neurosci. Biobehav. Rev. 29, 469491.
Phan, K. L., Wager, T., Taylor, S., and Liberzon, I. 2002. Functional
neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16, 331348.
Povinelli, D. J. and Preuss, T. M. 1995. Theory of mind:
Evolutionary history of a cognitive specialization. Trends
Neurosci. 9, 418424.
Preston, S. D. and de Waal, F. B. M. 2002. Empathy: Its ultimate
and proximate bases. Behav. Brain Sci. 25, 172.
Preuschoft, S. 1992. Laughter and smile in Barbary macaques
(Macaca sylvanus). Ethology 91, 220236.
Preuschoft, S. and van Hooff, J. A. R. A. M. 1995. Homologizing
primate facial displays: A critical review of methods. Folia
Primatol. 65, 121137.
Preuschoft, S. and van Hooff, J. A. R. A. M. 1997. The social
function of smile and laughter: Variations across primate
species and societies. In: Nonverbal Communication: Where

Nature Meets Culture (eds. U. Segerstrale and P. Mobias),
pp. 252281. Erlbaum.
Reddy, V. 2000. Coyness in early infancy. Dev. Sci. 3, 186192.
Redican, W. K. 1982. An evolutionary perspective on human
facial displays. In: Emotion in the Human Face (ed. P. Ekman),
pp. 212280. Cambridge University Press.
Russell, J. A. 1995. Facial expressions of emotion: What lies
beyond minimal universality? Psychol. Bull. 118, 379391.
Sackett, G. P. 1965. Response of rhesus monkeys to social stimulation presented by means of colored slides. Percept. Mot.
Skills 20, 10271028.
Sackett, G. P. 1966. Monkeys reared in isolation with pictures as
visual input: Evidence for an innate releasing mechanism.
Science 154, 14681473.
Sagi, A. and Hoffman, M. L. 1976. Empathetic distress in newborns. Dev. Psychol. 12, 175176.
Scherer, K. R. 2000. Emotion. In: Introduction to Social
Psychology: A European Perspective (eds. M. Hewstone and
W. Stroebe), 3rd edn., pp. 151191. Blackwell.
Sherwood, C. C., Holloway, R. L., Erwin, J. M., and Hof, P. R.
2004. Cortical orofacial motor representation in Old World
monkeys, great apes and humans. Brain Behav. Evol. 63,
82106.
Shin, L. M., Dougherty, D. D., Orr, S. P., et al. 2000. Activation
of anterior paralimbic structures during guilt-related scriptdriven imagery. Biol. Psychiatry 48, 4350.
Shioiri, T., Someya, T., Helmeste, D., and Wa Tang, S. 1999.
Cultural difference in recognition of facial emotional expression: Contrast between Japanese and American raters.
Psychiatry Clin. Neurosci. 53, 629633.
Shiota, M. N., Campos, B., and Keltner, D. 2003. The faces of
positive emotion: Prototype displays of awe, amusement and
pride. Ann. NY Acad. Sci. 1000, 296299.
Steiner, J. E. 1974. Innate, discriminative human facial expressions to
taste and smell stimulation. Ann. NY Acad. Sci. 237, 229233.
Steiner, J. E. and Glaser, D. 1984. Differential behavioral responses to
taste stimuli in non-human primates. J. Hum. Evol. 13, 709723.
Steiner, J. E. and Glaser, D. 1995. Taste-induced facial expressions in apes and humans. Hum. Evol. 10, 97105.
Steiner, J. E., Glaser, D., Hawilo, M. E., and Berridge, K. C.
2001. Comparative expression of hedonic impact: Affective
reactions to taste by human infants and other primates.
Neurosci. Biobehav. Rev. 25, 5374.
Takahashi, H., Yahata, N., Koeda, M., Matsuda, T., Asai, K.,
and Okubo, Y. 2004. Brain activation associated with evaluative processes of guilt and embarrassment: An fMRI study.
Neuroimage 23, 967974.
Tanaka, J. W., Kiefer, M., and Bukach, C. M. 2004. A holistic
account of the own-race effect in face recognition: Evidence
from a cross-cultural study. Cognition 93, B1B9.
Tangney, J. P. 1991. Moral affect: The good, the bad, and the
ugly. J. Pers. Soc. Psychol. 61, 598607.
Tangney, J. P. 1992. Situational determinants of shame and guilt
in young adulthood. Pers. Soc. Psychol. Bull. 18, 199206.
Tangney, J. P., Miller, R. S., Flicker, L., and Barlow, D. H. 1996.
Are shame, guilt and embarrassment distinct emotions?
Taylor, S. F., Liberzon, I., and Koeppe, R. A. 2000. The effect of
graded aversive stimuli on limbic and visual activation.
Neuropsychologia 38, 14151425.
Tomasello, M., Call, J., and Hare, B. 2003. Chimpanzees understand psychological states the question is which ones and to
what extent. Trends Cogn. Sci. 7, 153156.
Tomkins, S. S. and McCarter, R. E. 1964. What and where are
the primary affects: Some evidence for a theory. Percept. Mot.
Skills 18, 119158.
471
Tracy, J. L. and Robins, R. W. 2003. Does pride have a recognizable expression? Ann. NY Acad. Sci. 1000, 313315.
van Hooff, J. A. R. A. M. 1962. Facial expressions in higher
primates. Symp. Zool. Soc. Lond. 8, 97125.
Van Hooff, J. A. R. A. M. 1967. The facial displays of
the catarrhine monkeys and apes. In: Primate Ethology
(ed. D. Morris), pp. 768. Aldine.
van Hooff, J. A. R. A. M. 1973. A structural analysis of the social
behavior of a semi-captive groups of chimpanzees. In: Social
Communication and Movement (eds. M. von Cranach and
I. Vine), pp. 75162. Academic Press.
Vaughan, K. B. and Lanzetta, J. T. 1980. Vicarious instigation
and conditioning of facial expressive and autonomic
responses to a models expressive display of pain. J. Pers.
Vick, S. J., Waller, B., Smith-Pasqualini, M., Parr, L. A., and
Bard, K. A. 2003. The Chimpanzee Facial Affect
Coding System (FACS): Preliminary Findings. Paper presented at the 10th European Conference on Facial
Expression, Measurement and Meaning, Rimini, Italy,
September 1820.
Waller, B. M. 2005. Faciial Expressions in Chimpanzees and
Humans: Measurement and Meaning. PhD. thesis,
Department of psychology, University of Portsmouth.
Waller, B. M. and Dunbar, R. I. M. 2005. Differential behavioural effects of silent bared teeth display and relaxed open
mouth display in chimpanzees (Pan troglodytes). Ethology
111, 129142.
Waller, B. M., Vick, S. J., Parr, L. A., et al. 2006. Intramuscular
electrical stimulation of facial muscles in humans and chimpanzees: Duchenne revisited and extended. Emotion (in press).
Watts, D. P. 1998. Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behav. Ecol.
Sociobiol. 44, 4355.
Weigel, R. M. 1979. The facial expressions of the brown capuchin monkey (Cebus apella). Behaviour 68, 250276.
Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C.,
Lee, M. B., and Jenike, M. A. 1998. Masked presentations of emotional facial expressions modulate amygdala
activity without explicit knowledge. J. Neurosci. 18,
411418.
Winkielman, P., Zajonc, R. B., and Schwarz, N. 1997. Subliminal
affective priming resists attributional interventions. Cogn.
Emot. 11, 433465.
Further Reading
Bovet, D. and Washburn, D. A. 2003. Rhesus macaques
(Macaca mulatta) categorize unknown conspecifics according to their dominance relations. J. Comp. Psychol. 117,
400405.
Cheney, D. L. and Seyfarth, R. M. 1999. Recognition of other
individuals social relationships by female baboons. Anim.
Behav. 58, 6775.
Davis, M. and Whalen, P. J. 2001. The amygdala: Vigilance and
emotion. Mol. Psychiatry 6, 1334.
Ochsner, K. N. and Gross, J. J. 2005. The cognitive control of
emotion. Trends Cogn. Sci. 9, 242249.
Parr, L. A. and de Waal, F. B. M. 1999. Visual kin recognition in
chimpanzees. Nature 399, 647648.
Phillips, M. L., Young, A. W., Scott, S. K., et al. 1998. Neural
responses to facial and vocal expressions of fear and disgust.
Proc. R. Soc. Lond. B 265, 18091817.
472
Scherer, K. R. and Walbott, H. G. 1994. Evidence for universality

and cultural variation of differential emotion response patterning. J. Pers. Soc. Psychol. 66, 310328.
Surakka, V. and Hietanen, J. K. 1998. Facial and emotional
reactions to Duchenne and non-Duchenne smiles. Int. J.
Psychophysiol. 29, 2333.
Whiten, A., Goodall, J., McGrew, W. C., et al. 1999. Culture in
chimpanzees. Nature 399, 682685.
Relevant Websites
http://www.ninds.nih.gov National Institute of Neurological
Disorders and Stroke.
http://www.cellmigration.org Home for cell migration research
and information.
http://www.ncbi.nlm.nih.gov
National
Center
for
Biotechnology Information (NCBI).
www.chimpfacs.com Chimp facial action coding system.

The Evolution of Human Emotion

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

The Evolution of Human Emotion

Uploaded by

Copyright:

Available Formats

4.

28 The Evolution of Human Emotion

4.28.1 Introduction: Emotion Is Necessary for Survival

A trait or behavior in two related species that is attributable to a common

4.28.1 Introduction: Emotion

Emotion has long been viewed as an important

No matter the term, each of these phenomena

448 The Evolution of Human Emotion

and ultimately to identify and understand what is

This article will focus on three broad developments in

4.28.1.2.1 Subconscious evaluative processes