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THE INTERACTIVE DEVELOPMENT OF SOCIAL SMILING
Daniel Messingeraand Alan Fogelb
aDEPARTMENT OF PSYCHOLOGY, UNIVERSITY OF MIAMI, CORAL GABLES, FL 33124, USA
bDEPARTMENT OF PSYCHOLOGY, UNIVERSITY OF UTAH, SALT LAKE CITY, UT 84112, USA
I. OVERVIEW
A. THEORETICAL ORIENTATION
B. THE NEUROPHYSIOLOGY OF SMILING
C. TEMPERAMENT-BASED STUDIES OF SIGHTED INFANTS AND SMILING IN
BLIND INFANTS
II. EARLY SMILING
A. NEONATAL SMILING
B. THE EMERGENCE OF SOCIAL SMILING
C. THE EARLY DEVELOPMENT OF SOCIAL SMILING
III. QUANTITY AND QUALITY
A. DIFFERENT TYPES OF SMILING: DIFFERENT TYPES OF POSITIVE EMOTION?
B. SMILES AS INDICES OF CONTINUOUS POSITIVE EMOTIONAL PROCESSES
C. SMILES AS CONTINUOUS INDICES AND SMILES AS DISTINCT TYPES—A
RAPPROCHEMENT?
IV. THE INTERACTIVE DEVELOPMENT OF SMILING
A. OVERVIEW OF INTERACTIVE SMILING
B. THE DEVELOPMENT OF SOCIAL SMILING IN INTERACTIVE CONTEXT
C. SMILING INTERACTION DYNAMICS
D. INFANTS’PERCEPTIONS OF INTERACTIVE SMILING
V. SMILING AND ATTENTION TO THE CAREGIVER
A. SMILES AND AROUSAL MODULATION
B. THE EARLY COORDINATION OF SMILING AND GAZING AT THE
CAREGIVER’S FACE
C. THEORETICAL PERSPECTIVES RELEVANT TO SMILES AND GAZE AVERSION
VI. SMILING AND REFERENTIAL COMMUNICATION
VII. PRAGMATICS: THE REPRESENTATIVENESS, DISCRIMINANT, AND PREDICTIVE
VALIDITY OF INFANT SMILING
A. REPRESENTATIVENESS OF SMILING
B. SMILING IN ATYPICALLY DEVELOPING INFANTS
C. SMILING AND DEVELOPMENTAL OUTCOMES
VIII. SUMMARY AND CONCLUSIONS
ACKNOWLEDGMENTS
REFERENCES
327
Advances in Child Development and Behavior Copyright © 2007 Elsevier Inc. All rights reserved.
R.V. Kail : Editor
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Infant smiles elicit feelings of sympathetic engagement from researchers as
well as parents. Early social smiles appear to be direct behavioral expressions of
positive emotional engagement. This apparent link between behavior and mean-
ing lies behind a century of research on the causes, emotional significance,
behavioral correlates, and developmental consequences of infant smiles. In this
chapter, we review that literature with a critical eye, focusing on the emergence
and early development of social smiling, the possibility that different types of
smiles index different types of positive emotion and new evidence that smiles
index a single dimension of positive emotion, the interactive development of dif-
ferent types of smiling and the origins of emotion regulation, the integration of
smiling into referential communication, and the use of smiles to distinguish
between infants and predict outcomes. The review covers the results of studies
of infant perception, infant smile production, observers’ ratings of those smiles,
and the smiling of nonhuman primates. We begin with a theoretical overview,
review the neurophysiology of smiling, and examine the heritability of smiling
and lessons from the smiling of blind infants. Throughout, our intent is to pres-
ent new findings and highlight areas of potential investigation.
I. Overview
A. THEORETICAL ORIENTATION
More than a century of research into emotional expression has produced a rich
diversity of theoretical perspectives. Here we provide a brief overview of those
perspectives as they pertain to the development of smiling. No attempt has been
made to explicate each perspective or its variants fully. Instead our goal is to
identify the strengths of these perspectives and situate our own approach with
respect to them. This will involve noting areas of overlap—as well as divergence—
between theoretical perspectives on the development of smiling.
Cognitive/constructivist (differentiation) approaches suggest that discrete
affects develop from earlier more diffuse states. Joy, for example, develops out of
states of pleasurable positive valence (Sroufe, 1979, 1995; Sroufe & Waters,
1976). This perspective is part of a long theoretical tradition suggesting that emo-
tions occur only in the presence of a cognitive interpretation of affective valence
(Barrett, 2006; Bridges, 1932; Sroufe, 1995). Smiles in the first 2–3 months are
thought to index pleasure and to occur when the infant experiences a relaxation
in cognitive tension related to recognizing a visual stimulus. The development
of an increasing capacity for cognitive engagement is thought to lead to more
dramatic drops in arousal and more specifically joyful emotion (Sroufe, 1995;
Tomkins, 1962). These developments are thought to occur around 9 months and
to be paralleled by more intense infant smiling and laughing (Sroufe, 1995).
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Differential and discrete emotion theories champion the straightforward
hypothesis that infant facial expressions such as smiles are the product of dis-
crete affect programs (Ackerman, Abe, & Izard, 1998; Izard & Ackerman, 2000;
Lewis, 2000). These neurophysiologically based affect programs simultaneously
trigger expressive actions such as smiles and feeling states such as joy. By posit-
ing that infant smiles are direct indices of joy, this perspective has facilitated
extensive research in which smiles are measured among different infant popula-
tions at different ages. This theory focuses on structures within the organism that
are responsible for emotion and its expression. Recent articulations of differen-
tial emotion theory, however, have stressed a functional role for emotions. Joy,
for example, is thought to motivate social approach behaviors and the continua-
tion of interactions. At a societal level, smiles are seen as communicating posi-
tive feelings and facilitating social cohesion. An early propensity toward joy, as
expressed in smiling, is hypothesized to facilitate extraverted personality traits.
Functional perspectives focus on the role of emotions such as joy in the creation
and maintenance of relationships with the environment, particularly with significant
others (Barrett, 1993; Campos et al., 1994; Witherington, Campos, & Hertenstein,
2001). This perspective has served to direct attention to vocal, gestural, and whole-
body expressions of emotion in context, warning against exclusive reliance on
smiles or other facial expressions of emotion. Potentially relevant to functionalist
perspectives are ethological attempts to understand smiles solely as communicative
signals to conspecifics (Fridlund, 1994). Ethological approaches have generated
impressively clear research results on the communicative functions of smiles and
similar expressions in monkeys, chimpanzees, and human beings (Bard et al., 1992;
Burrows et al., 2006; Mizuno, Takeshita, & Matsuzawa, 2006; Redican, 1975; van
Hooff, 1972). Functionalist approaches stress the importance of identifying the
infant’s goal orientation in a given situation and suggest, along with other
approaches, that joy is a product of goal attainment.
Our approach uses dynamic systems as a higher order theoretical orientation
with which to integrate insights from other perspectives (Camras, 2000; Fogel
et al., 1992; Messinger, Fogel, & Dickson, 1997; Thelen & Smith, 1994a, 1994b;
Thelen, 1991; Witherington et al., 2001). A dynamic systems approach focuses
on social smiling as a reflection and constituent of an interactive relationship.
The focus is the bottom–up interrelationship of constituents of positive emo-
tional expression as they emerge in social contexts. This approach has also
focused on the temporal dynamics of social smiling, their rise and fall in time,
and the relation of such emergent processes to emotional development more gen-
erally. This has involved examining the creation of smiles and other facial
expressions in real time and the possible ramifications of such real-time
processes for emotional development.
From a dynamic systems perspective, expressive configurations such as smiles
are conceptualized as constituents of infant emotional processes. The expression
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The Interactive Development of Social Smiling 329
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is part of what the infant feels and is central to the infant’s ongoing interchange with
the environment. Smiles are an emotional signal to the self as well as the interactive
partner. They are simultaneously experiential and social. As such, the dynamics of
facial expression can shed light on the dynamics of emotion.
By using a dynamic systems approach as a higher order theoretical framework,
we seek in part to emphasize areas of overlap and agreement between different
perspectives. Differing theoretical perspectives define emotion in different ways
and emphasize different research agenda, creating overlaps between perspectives.
Both functional and dynamic systems approaches, for example, locate emotion in
the relationship of the infant to his or her environment. A cognitive/constructivist
perspective highlights developing cognitive capacities in the emergence of smil-
ing in a fashion that exemplifies the dynamic systems emphasis on nonobvious
components in the bottom–up emergence of emotional expressions. Though only
differential emotion theory may emphasize the logical primacy of the neural com-
ponents of positive emotional functioning, no perspective challenges their impor-
tance. Finally, both differential emotion theories and dynamic systems
approaches are concerned with the temporal dynamics of smiles—albeit for dif-
ferent reasons.
B. THE NEUROPHYSIOLOGY OF SMILING
The neural origins of smiling are clear (Elliot, 1969; Williams et al., 1989).
Smiles occur when the zygomatic major muscle contracts, pulling the corners of
the lips upward and laterally (see Figure 1). The zygomatic is innervated by the
facial nerve, the seventh cranial nerve, which emanates from the facial nucleus.
The facial nucleus is an aggregation of motor neurons in the ventrolateral region
of the lower pontine tegmentum, at the level of the pons in the brain stem. By
contrast, afferent sensation from the face during smiling is carried by the fifth
cranial nerve, the trigeminal. This afferent feedback may be a physiological
basis for the facial-feedback hypothesis. Empirical support for this hypothesis
indicates that the process of smiling can itself contribute to the experience of joy
(Izard, 1981; Soussignan, 2002).
The neurophysiological evidence of an affect program for joy is less than
clear. The facial nucleus receives two sets of inputs. Voluntary or deliberate smil-
ing (being asked to produce a smile) is thought to originate in the cortical motor
strip and travels to the nucleus via pyramidal tracts (Rinn, 1984). However, most
social smiling in infancy is spontaneous and expressive and, according to differ-
ential emotion theory, is a motor expression of an affective neural program for
joy. Spontaneous facial expressions involve an “extrapyramidal” pathway that
involves subcortical (e.g., basal ganglia) as well as deep cortical structures such
as the amygdala.
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Reviews of neuroimaging studies in adults (Barrett & Wager, 2006) suggest
that joyful responses may not be associated with a specific pattern of activation
(Murphy, Nimmo-Smith, & Lawrence, 2003; Phan, Wager, Taylor, & Liberzon,
2004). One meta-analysis reviewed suggests an association between joy and
activation of the rostral supracallosal anterior cingulate cortex (Murphy, Nimmo-
Smith, & Lawrence, in press). Another suggests an association between joy and
activation of the basal ganglia, a set of structures associated with voluntary
movement (Phan et al., 2004). One possibility is that anterior cingulate cortex, a
section of limbic cortex, is associated with joyful responses, whereas basal gan-
glia are involved in related action tendencies. Nevertheless, the lack of consis-
tency does not readily suggest support for an affect program as there is no
consistent neural pathway for joy.
Stronger meta-analytic evidence (Barrett & Wager, 2006) supports the supposi-
tion that positive affect and approach-oriented emotional orientations are associated
with greater left than right cerebral activation both overall (Murphy et al., 2003) and
specifically in frontal areas (Wager et al., 2003). This pattern of activation also
accompanies emotionally positive Duchenne smiles, which involve constriction of
the eyes, in infants (Fox & Davidson, 1988). These left frontal areas, however, are
not dedicated structures. Instead, specific elements of perceiving and acting joyfully
in an interactive situation (e.g., smiling while gazing at and moving toward a parent)
may yield more consistent patterns of neurophysiological activation than investiga-
tions of abstracted emotion categories such as joy (Barrett & Wager, 2006). As sug-
gested by a dynamic systems approach, the neural “structure” of joyful smiling is
likely to be both embodied and interactive (Fogel & Thelen, 1987).
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The Interactive Development of Social Smiling 331
Fig. 1. Six-month-old infant displaying a high-amplitude interactive smile involving eye constric-
tion and mouth opening.
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C. TEMPERAMENT-BASED STUDIES OF SIGHTED INFANTS AND
SMILING IN BLIND INFANTS
In this section, we examine temperamental approaches to the smiling of
sighted infants, which provide an overview of factors impacting the expression
of positive emotion. These temperamental approaches are complemented by
reports on smiling in blind infants, which illustrate how smiling develops in the
absence of visual input.
There tends to be a gap between broad-scope temperamental approaches to
infant positive emotion expression and more detailed interactive approaches.
Investigations of temperament often employ genetically informative designs and
employ linear modeling of heritable and environmental variance of indices of
positive emotion. Interactive approaches investigate the development and in-
time formation of positive emotional communication. The approaches are ulti-
mately, however, complementary views of similar phenomena at different levels
of analysis.
Patterns of parental response reveal the influence of both genetic and envi-
ronmental effects on infant positive emotion expression (Goldsmith, Buss, &
Lemery, 1997; Goldsmith et al., 1999). This is in contrast to reports on negative
emotion in which heritability estimates tend to be higher and environmental
influences less pronounced. Shared environmental effects on infant expression
of positive emotions include caregiving effects such as the impact of
parent–child interaction.
Genetically informative temperament studies are typically based on parental
reports of positive emotion (Goldsmith et al., 1997, 1999). Parents’ reports of
infant smiling and laughter sometimes are and sometimes are not significantly
correlated with investigator observations of positive emotion expressions
(Bridges et al., 1993; Rothbart, 1986). One possibility is that parental ratings are
relatively uninformative when the parents engage in high levels of emotionally
positive play with their infants (Hane et al., 2006). It is only the ratings of par-
ents who engage in low levels of mutually positive play with their infants that
are predictive of observed infant smiling. Clearly, genetically informative stud-
ies of investigator-observed expressions are necessary to shed light on the rela-
tive impact of heritable and environmental factors on infant social smiling.
The development of smiling in blind infants provides intriguing clues into the
role of environmental influences in the emergence of positive facial expressions
(Fraiberg, 1975; Freedman, 1964; Ganchrow, Steiner, & Daher, 1983; Rogers &
Puchalski, 1986; Thompson, 1941). Social smiling in blind infants occurs in
response to events such as hearing a familiar voice. It typically elicits a parental
response. Perhaps as a consequence, these social smiles become more frequent
between 4 and 12 months. However, the smiles of blind infants are less frequent
and briefer (more fleeting) than those of sighted infants. Deficits in smiling are
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observed in blind infants after 2 or 3 years of age. On the one hand, normative
experiences of caregiving are sufficient for the emergence of smiling; on the
other hand, visually mediated interactive smiling appears to play an important
role in maintaining smiles in real time (i.e., the duration of smiles) and in devel-
opmental time (i.e., the reduced smiling of older blind infants). Research with
blind infants suggests that the emergence of social smiling is experience expec-
tant, occurring even in the absence of visual feedback. The interactive intensifi-
cation of smiling depends, however, on visual engagement. From a dynamic
systems perspective, the absence of mutually reinforcing visually mediated feed-
back in the form of reciprocal smiling probably plays a role in these deficits. In
the next section, we broaden our scope to examine the early development of
smiling in typically developing infants.
II. Early Smiling
A. NEONATAL SMILING
In early development, neonatal smiling gradually becomes linked to environ-
mental stimulation, setting the stage for the emergence of social smiling. In this
section, we describe the association of neonatal smiles with particular behavioral
states, their cortical origins, and observer studies of neonatal smiles. We go on
to describe the anatomical topography of neonatal smiles and the subsequent
development of smiling in response to sensory stimuli that set the stage for social
smiling.
Neonatal smiles appear to be experience expectant. They occur in sleeping and
drowsy states of rapid eye movement (REM) at an average rate of one smile per
5 min. Smiles during sleep are referred to as spontaneous or endogenous smiles
because they have no obvious external cause (Emde et al., 1978; Emde &
Koenig, 1969a, 1969b; Emde, McCartney, & Harmon, 1971; Harmon & Emde,
1972a, 1972b; Messinger et al., 2002; Wolff, 1987). Newborns also smile,
though less frequently, during other behavioral states, including states of alert-
ness (Dondi et al., 2006).
A case report of neonatal smiling in an infant with microcephaly suggests a
subcortical origin for neonatal smiling (Emde & Koenig, 1969a, 1969b; Emde
et al., 1971; Harmon & Emde, 1972a). Developing cortical inhibition of smil-
ing is suggested by the findings that infants born prematurely show more
neonatal smiling than full-term infants and that this spontaneous smiling
declines with age.
Neonatal smiles illustrate the dynamic principle of developmental hete-
rochronicity (Fogel & Thelen, 1987). Smiles are present physically before they
are integrated into patterns of social engagement and interaction that provide
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evidence for joyful emotion. Neonatal smiles can, in fact, have a relatively
mature form in which the zygomatic shows moderately strong contraction and
the eyes are constricted to form a Duchenne smile (Messinger et al., 2002). This
association between the strength of smiling and the strength of eye constriction
reflects an early, apparently neuromuscular, synergy.
In humans, zygomatic contractions during sleep appear to decline in fre-
quency as stronger zygomatic contractions during alert states become more fre-
quent toward 1 month of age (Harmon & Emde, 1972a; Wolff, 1987). This
pattern in human infants has similarities with accounts of smiling in young
chimpanzees (Mizuno et al., 2006). Chimpanzees also smile during REM sleep;
this smiling declines in the first 2 months of life as social smiling increases.
Although smiles can have an apparently mature form at birth, these patterns of
increasingly strong and bilateral zygomatic contraction suggest a developmental
process of neuromuscular coordination and synchronization that is consistent
with a dynamic systems perspective.
Influenced by a dynamic systems perspective, Wolff (1987) documented the
developmental emergence of infant smiling in response to first auditory and then
visual stimuli in the first 2 months of life (Field et al., 1986; Spitz, 1946; Sroufe &
Waters, 1976). In the first week of life, infants do not smile reliably in response to
sounds, visual stimuli, tactile stimulation, bouncing, or the like. Toward the end of
the second week, half of the infants in Wolff’s sample smiled regularly in response
to the human voice when they were awake. By the fourth week, most infants smiled
to both human and nonhuman sounds, although the human voice was more attrac-
tive. At 5 weeks, the combination of voice and face was a better elicitor of smiling
than either of the two alone. By 8 weeks, infants smiled only after making visual
contact with the mother’s face (Harmon & Emde, 1972a; Spitz, 1946; Wolff, 1987).
An explanation of the apparent shift in the capacity of first auditory and then
visual stimuli to elicit smiling might invoke features of the developing nervous
system first in a uterine and then in an extrauterine environment (Huttenlocher,
1999; Lickliter & Bahrick, 2001). New descriptive and experimental studies
such as those pioneered by Wolff are warranted. They would indicate whether
individual differences in central nervous system maturity and/or early experi-
ence with smile-eliciting stimuli are related to the development of smiling
responses to mechanical stimuli and indicate whether such smiling responses are
linked to the emergence of social smiling (Kawakami et al., 2006).
B. THE EMERGENCE OF SOCIAL SMILING
Smiles develop their familiar social form during interaction. Although mothers
report the emergence of social smiles at about 1 month, experimenters are able
to elicit social smiles between 1 and 2 months (Anisfeld, 1982). The emergence
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of social smiling, however, appears to be contingent on postconceptional age in
both preterm and full-term infants. This suggests social smiling is a function of
neurological maturity rather than number of weeks in the postnatal environment,
a possibility that appears ripe for further empirical study.
Social smiling develops as infants spend more time in states of alert inactivity
(i.e., not fussing/crying) that facilitate gazing at the caregiver’s face (Lavelli &
Fogel, 2005). Social smiles, in fact, emerge in a period marked by the develop-
ment of new patterns of visual attention. Although 1-month-olds gaze alternately
at the edge of the head and the eyes, 2-month-olds gaze between the edge of the
head, the eyes, and the mouth. This more integrative pattern of gazing is likely
to encourage attention to the facial expression of others. Thus, linked compo-
nents of neural maturity, state regulation, and perceptual competence appear to
be necessary for the emergence of social smiling.
Social smiles are not present at birth. From an evolutionary perspective, the
function of smiles is to keep parents and other potential caregivers close at hand
(Bowlby, 1982). It is not clear, however, that observational studies have sys-
tematically examined whether infant smiles, in fact, predict increased parental
proximity. Nevertheless, it appears plausible that earlier social smiling would
increase an infant’s inclusive fitness. It may be, of course, that heritable changes
associated with the earlier emergence of social smiling are not available during
the first month of postnatal physiological consolidation and energy conserva-
tion (Rovee-Collier, 1996; Sroufe & Waters, 1976). There is, however, some
evidence suggestive of potentially heritable differences in the development of
social smiling.
Group differences have been documented in the emergence of social smiling
in an Israeli sample (Anisfeld, 1982). Both tester and maternal observation indi-
cate that Sephardi Jewish infants engaged in social smiling about 1 month before
Ashkenazi Jewish infants. Such a difference suggests a background of poten-
tially heritable individual variability in the timing of the onset of social smiling.
If such differences are, indeed, heritable, age of social smiling may be subject to
evolutionary pressure. A crucial issue here is the psychological meaning of the
emergence of social smiling to parents. A testable hypothesis with clear evolu-
tionary implications holds that the emergence of social smiles would be associ-
ated with parental reports of increases in a feeling of connection or even a
willingness to sacrifice for the newly smiling infant.
C. THE EARLY DEVELOPMENT OF SOCIAL SMILING
In this section we outline the developmental emergence of social smiling in a
dyadic context. Inspired by Trevarthen’s microanalytic observations (Murray &
Trevarthen, 1986; Trevarthen, 2001), we examine how early smiling emerges
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from attentional expressive configurations (Lavelli & Fogel, 2002) (see Figure 2).
We employ a dynamic systems perspective to find parallels between the real-
time and the developmental emergence of positive facial expressions during
social exchanges in the first 3 months of life.
In the first month, infants transition between neutral gazes away from
mother’s face and simple attention to her face (i.e., gazing at the mother’s face
without any sign of emotional engagement). The second month sees a sequen-
tial pattern of infant simple attention to mother’s face, concentrated attention to
her face, smiling at mother, and then cooing expressions also directed toward
mother. This pattern is an interactive replication of findings that dynamically
link cognitive processes to the emergence of social smiling as predicted by both
cognitive/constructivist and dynamic systems approaches. Early social smiling
is frequently preceded by a 3- to 20-s period of brow knitting and visual fixa-
tion on the mother’s face (Anisfeld, 1982; Lavelli & Fogel, 2005; Oster, 1978).
The brows then relax, indexing apparent cognitive recognition, and a smile
appears. Real-time occurrences of this attention-related smiling pattern may,
then, be the occasion for the developmental emergence of smiling. Research
further specifying the type of cognitive processing preceding the occurrence
and developmental emergence of social and nonsocial smiles would strengthen
this conclusion.
During the second month maternal expressions change in a manner that parallel
developmental changes in the infant’s patterns of attention and emotion during
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336 Daniel Messinger and Alan Fogel
a. Neutral/Simple
Attention. Reflexes and
vegetative movements.
Relaxed neutral
expression, possible
visual attention, quiet
alert.
c. Excited Attention.
Brow raising (AU 1+2)
& strong fast limb
movements. Mouth
closed or only partially
open. High-arousal &
sustained visual attention
with motor excitement.
e. Attentive Smile. Lip
corner raising (AU 12)
with mouth only partially
open. Frequent motor
quiet. Relaxed
expression of pleasure
during visual attention.
b. Concentrated Attention.
Brow knitting (AU 3); motor
quiet. Lower face still with lip
pursing, or mouth partially
open. High-arousal &
sustained visual attention with
“effortful” concentration.
d. Astonished Attention.
Strong brow raising (AU 1+2);
motor quiet, relative facial
stillness. Eye widening (AU
5); jaw dropping and mouth
open in “o”-shape.
“Fascinated,” motionless
visual fixation.
f. Cooing Expression. Lip
shaping for cooing, with upper
lip raising / protrusion, or lip
& tongue “pre-speech”
movements. Approaching
postural orientation; arm
raising with arm / hand
waving.
(a) (b)
(c) (d)
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Fig. 2. Infant expressive configurations during mother–infant face-to-face communication
(0–3 months). Source: Lavelli and Fogel (2005). AQ14
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face-to-face communication (Lavelli & Fogel, 2002). Maternal neutral expressions
decrease in conjunction with an increase in approach-oriented emotionally positive
expressions in which mothers talk and smile simultaneously (talk/smile). At a
dyadic level, infant smiling and cooing expressions become sequentially linked
with maternal talk/smile in the second and third month. These sequential linkages
are bidirectional. Maternal talk/smile, infant smile, and infant cooing expressions
can cycle between each other in multiple patterns, suggesting the existence of a
positive emotional attractor in the social communication system.
Taken together, these findings suggest that the smile does not occur alone but
rather develops in a complex relation with other facial expressions, infant atten-
tion, and maternal facial expressions and attention. There is, in other words, a
dynamic social–communicative system in which smiling develops and stabilizes.
This suggests that smiling gradually develops as infants and their caregivers
cocreate specific forms of social communication. In support of this proposition,
2-month-olds smile less at a stranger who is either more or less contingently
responsive than the infant’s mother (Bigelow & Rochat, 2006). That is, dyad-
specific levels of interactive contingency that affect smiling levels develop by
2 months of age.
III. Quantity and Quality
Some smiles appear to be coy, others gleeful, and yet others riotous. In this
section, we explore evidence suggesting that different types of smiling express
qualitatively different types of positive emotion. This issue is theoretically mean-
ingful. A multiplicity of emotionally different smiles would challenge the dis-
crete emotion theory proposition of a single affect program for joy. In the next
section, we present evidence for an alternate possibility—that social smiles
express different degrees of a single dimension of positive emotion or joy—and
attempt to integrate those perspectives. We begin this section by exploring the
possibility that the presence of the Duchenne marker (eye constriction) and of
mouth opening may index qualitatively different dimensions of emotional mean-
ing in smiles.
A. DIFFERENT TYPES OF SMILING: DIFFERENT TYPES OF
POSITIVE EMOTION?
1. Smiles Involving Eye Constriction—Duchenne Smiles
Researchers have long argued that Duchenne smiles (Duchenne, 1990 [1862])
involving eye constriction (produced by the orbicularis oculi and pars lateralis)
are qualitatively different from smiles without eye constriction (see Figure 3).
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One hypothesis is that (adult) smiles involving eye constriction are an expression
of joy, but smiles without eye constriction are a nonemotional social signal
(Ekman, Davidson, & Friesen, 1990). A similar distinction has been made for
infants (Dawson et al., 1997; Fox & Davidson, 1988). Ten-month-olds are more
likely to produce smiles involving eye constriction when approached by their
smiling mothers but are more likely to produce smiles without eye constriction
when approached by an impassive stranger. Concurrent EEG recordings indicate
that 10-month-olds’ smiling with eye constriction is associated with greater rel-
ative activation of the left than the right frontal cerebral hemisphere (Fox &
Davidson, 1988). Similar differences in relative activation are found in adults
and appear to reflect greater approach orientation (Ekman et al., 1990; Murphy
et al., 2003). This suggests that by 10 months there are at least two qualitatively
different smiles: smiles with eye constriction used to express joyful engagement
and smiles without eye constriction indexing a more cautious or less involved
engagement.
A similar argument can be made for the qualitative distinctiveness of smiles with
eye constriction produced by infants during face-to-face interactions with their
mothers: Between 1 and 6 months, infants engage in relatively more smiling with
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338 Daniel Messinger and Alan Fogel
Smile Amplitude (Mean +- 1 SD)
5.0
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Fig. 3. Smile types.
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eye constriction than smiling without eye constriction when their mothers are smil-
ing (Messinger, Fogel, & Dickson, 2001). During these smiles with eye constric-
tion, they produce more speech-like syllabic sounds than during smiling without
eye constriction, suggesting greater engagement with their partners (Hsu, Fogel, &
Messinger, 2001). The results suggest smiling with eye constriction is a way to
engage with the joyful expressions of another, a way to share positive affect during
an ongoing interaction. One hypothesis is that infant smiles involving eye constric-
tion are used to reciprocate the smiles of a social partner and, perhaps especially, to
reciprocate the eye constriction smiling of another (Bachorowski, 1999).
The presence of eye constriction in an expression may, then, index qualitatively
different emotional processes than are present in expressions without eye constric-
tion. Eye constriction, for example, appears to index qualitative change in its occur-
rence with cry-faces, the prototypic infant negative expressions. Standard
descriptions indicate that intense eye constriction transforms the cry-face from a dis-
crete expression of anger into one of distress (Bolzani-Dinehart et al., 2005; Izard,
Dougherty, & Hembree, 1983; Messinger, 2002; Oster, Hegley, & Nagel, 1992).
One hypothesis is that as eye constriction reduces the visual field it may con-
tribute to a focus on the object of the emotion and to feelings of being caught up
by the emotion (Messinger, 1994). Infant smiles with eye constriction may
involve increased salience of positive feeling and also communicate this to the
receiver. As such, smiles with eye constriction may be perceived to be more
authentic infant expressions of joy than smiles without.
2. Smiles Involving Mouth Opening—Play Smiles
Another facial action that may produce qualitative changes in the meaning of
infant smiles is mouth opening produced by jaw dropping. Mouth opening is
associated with more rapid breathing, with vocalizations, and with laughter. Just
as eye constriction may index positive emotional engagement with another,
mouth opening may index aroused excitement and playfulness.
Other evidence concerning the function of open-mouth smiling comes from
studies of primates (Bard et al., 1992; Burrows et al., 2006; Plooij, 1979; Redican,
1975). Chimpanzee zygomatic contraction produces a display of silent bared teeth,
which seems to be a signal of submission (“I mean you no harm”) that is fre-
quently issued to a dominant individual. In chimpanzees, it has also come to be a
signal of affiliation that is followed by behaviors such as holding out a hand.
Among human beings and their predecessors, the silent bared teeth display may
have evolved into smiling that does not involve pronounced mouth opening.
By contrast, the relaxed open-mouth display—also called a play face—is thought
to be evolutionarily linked to human laughter and has morphological similarities
with open-mouth smiling (Plooij, 1979; van Hooff, 1972; Waller & Dunbar, 2005).
Both communicate a playful orientation that has an aroused quality. The chimpanzee
relaxed open-mouth display, although common in affiliative contexts, is uniquely
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linked to play. When two chimpanzees both engage in relaxed open-mouth displays,
play bouts tend to last longer (Waller & Dunbar, 2005). In chimpanzee infants, it
originates in mock biting play with the mothers (Plooij, 1979). One possibility is
that, in human infants as well, open-mouth smiles reflect and communicate states of
excited arousal and are a prototypic expression of social joy.
Like chimpanzees, human infants also engage in mouth opening that is not asso-
ciated with smiling or with negative expressions, such as the “cooing expression”
shown in Figure 2 (Kaye & Fogel, 1980; Messinger et al., 2001). These mouth-
open displays tend to occur during positive periods of face-to-face interaction such
as when the mother is smiling and making exaggerated displays and when the
infant is gazing at the mother. Intriguingly, this suggests that mouth opening, like
smiling, may be a characteristic of a relatively positive infant emotional engage-
ment with the environment.
Relaxed open-mouth displays may also be phylogenetic precursors of human
laughter. In infants, laughter is a smile-linked vocalization that appears to index
intense positive emotion. Social routines (including tickling) and visual surprises
(covering and uncovering objects) become more potent elicitors of laughter in
the first year of life (Nwokah et al., 1999, 1994; Sroufe & Waters, 1976; Sroufe &
Wunsch, 1972). After 4 months of age infants laugh more frequently and the
mean duration of these laughs increases. At the same time, the duration of the
laughs of individual infants and mothers becomes more correlated. In the second
year of life, the onsets and offsets of infant and mother laughs that overlap move
increasingly closer in time. Both of these developments suggest the development
of dyad-specific patterns of positive communication (Nwokah et al., 1994). Such
correspondences between partners are suggested by a dynamic systems perspec-
tive is also likely to characterize dyadic patterns of smiling.
Nonhuman relaxed open-mouth displays also have special ties to human open-
mouth smiling. During face-to-face interaction, infants between 1 and 6 months
of age engage in more open-mouth smiling when gazing at their mothers’ faces.
Among adults, open-mouth smiles involving eye constriction tend to occur in
response to humorous stimuli (Ruch, 1997). Although neonates in sleeping and
drowsy states emit smiles with eye constriction, smiles with mouth opening are
much less frequent, offering indirect support for the arousal hypothesis
(Messinger et al., 2002). This pattern of results suggests an association between
positive social engagement, arousal, and smiles involving mouth opening. In
support of this association, still images of smiles with greater mouth opening are
rated as involving more arousal than digitally edited versions of the same smiles
involving less mouth opening (Bolzani-Dinehart et al., 2003, 2005). The associ-
ation between mouth opening and arousal is also seen in ratings of the negative,
cry-face expression (Bolzani-Dinehart et al., 2005).
We have suggested that expressions involving eye constriction index the
increased salience of the emotional experience and that expressions involving mouth
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opening index increased arousal. These qualitative distinctions between facial
expressions can be mapped onto circumplex models of emotion (Barrett & Russell,
1999; Russell, 1980; Yik, Russell, & Barrett, 1999) (see Figure 4). In this model,
positive (pleasant) and negative (unpleasant) affect define two horizontal poles.
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Fig. 4. An illustrative circumplex showing emotional valence on the horizontal axis and arousal
on the vertical axis. Sad and angry faces indicate negative emotional valence, while smile-faces indi-
cate positive emotional valence. Greater mouth opening indicates greater arousal regardless of emo-
tional valence. At the highest level of arousal, the distinction between positive and negative
emotional valence is lost. At the lowest level of arousal, no emotional valence is conveyed. Figure
and caption courtesy of Mark Sheskin.
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We hypothesize that such positive (smile) and negative (cry-face) expressions
involve eye constriction. These expressions may communicate that the infant is
in the throes of a “deeper” emotional experience. This valence dimension is at
right angles to an arousal dimension. Emotion expressions high in arousal are
hypothesized to involve mouth opening. Among infants, this would involve
smiles with mouth opening in the upper right quadrant and cry-faces with mouth
opening in the upper left quadrant. At the top of this pole, arousal becomes so
extreme as to dominate the valence. In the same way, expressions of extreme
arousal are hypothesized to involve extreme mouth opening that stretches out
facial features, erasing the distinctive positive and negative characteristics of the
expression.
3. Smiles Involving Both Eye Constriction and Mouth Opening—Duplay Smiles
Based on the meaning of their facial constituents, infant smiles that combine
eye constriction and mouth opening are hypothesized to index sharing experi-
ences of aroused positive engagement. During face-to-face interactions, these
smiles are relatively more likely when infants are gazing at their smiling moth-
ers (Messinger et al., 2001). Levels of this type of smiling also vary systemati-
cally over the episodes of the face-to-face/still-face procedure (Adamson &
Frick, 2003; Delgado, Messinger, & Yale, 2002; Moore, Cohn, & Campbell,
2001; Tronick et al., 1978). Levels of combined open-mouth smiling with eye
constriction are relatively elevated during the initial face-to-face interaction.
They are relatively depressed during the stress of parental nonresponsivity in the
still-face and the emotional regrouping that characterizes the reunion episode
(Acosta et al., 2004; Weinberg & Tronick, 1994).
The meaning of different types of infant smiles is revealed in peekaboo and
tickle games between mothers and infants (Fogel et al., 2006). Both games
involve a setup phase and a more intensely emotional climax phase. In peeka-
boo, the setup is the covering of the mother’s face (“Where’s mommy?”), and the
climax is the uncovering (“Peekaboo”). Infants were more likely to smile during
the climax than during the setup of peekaboo games but this pattern did not vary
by type of smile.
Different phases of tickle games were associated with different types of smil-
ing. In tickle games, the setup is the approach of the mother’s hands toward the
infant’s body (“I’m gonna get you”), and the climax is the act of tickling
(which may be accompanied by maternal vocalizations). Among infants at
6 and 12 months of age, combined open-mouth smiles with eye constriction
tended to occur during the climax rather than during the setup phase of tickle
games. This parallels the finding that, at home, 12-month-olds’ combined open-
mouth smiling with eye constriction predominates during physical play with par-
ents (Dickson, Walker, & Fogel, 1997). These findings offer additional support
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for the view that smiling involving eye constriction and mouth opening indexes
sharing experiences of aroused positive engagement.
Approach and withdrawal indexed by patterns of gazing and movement dur-
ing games also contribute to the meaning of smiles (Fogel et al., 2000). During
peekaboo games, for example, infants tend to gaze at the parent during all types
of smiles, suggesting approach-oriented visual attention. During the climax of
tickle games, by contrast, infants engaging in open-mouth smiles with eye con-
striction show mixed patterns of both gazing at and away from parents. Such pat-
terns may correspond to feelings of enjoyment of active participation in a highly
arousing situation and enjoyment of escape. These findings suggest that the same
smiling actions can reflect different positive emotions depending upon co-occur-
ring infant actions and the dynamics of the social process.
B. SMILES AS INDICES OF CONTINUOUS POSITIVE
EMOTIONAL PROCESSES
In addition to evidence suggesting the existence of qualitatively different pos-
itive emotions indexed by different types of smiles, there is also strong evidence
that smiles vary in the degree to which they express a single joyful positive emo-
tion. This argument rests on examination of the strength of the smile action itself
(smile amplitude, a continuous measure of the strength of zygomatic contrac-
tion), consideration of the role of amplitude in smiles involving eye constriction
and mouth opening, the distribution of these types of smiles in different periods
of interaction, rating studies, and the results of automated measurements being
used to describe smile processes in time.
1. Smiling as a Continuous Action
Physiologically, smiles are continuous neuromuscular processes. The strength
of zygomatic contraction determines, other things being equal, the amplitude of a
smile, the extent of upward and lateral lip corner movement. If zygomatic con-
traction indexes positive emotion, it follows that stronger contraction indicates
more intensely positive emotion. In fact, adults’self-reported feelings of pleasure
are correlated with the amplitude of zygomatic major contraction in studies using
both observational (Ekman, Friesen, & Ancoli, 1980) and electromyographic
methods(Hess et al., 1989). Similarly, smile amplitude appears to index directly
the infant’s positive emotional engagement with ongoing activities. Tickle games
elicit higher amplitude smiling than peekaboo games. The climax of both games
involves smiles of higher amplitude than the setup phases. Perturbations that
involve dampening the climaxes of the games—such as substituting pretend for
real tickling—result in lower-amplitude smiles (Fogel et al., 2006).
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2. Smile Amplitude in Different Types of Smiles
Coding of the mean amplitude of different types of smiles suggests anatomical
constraints (Fogel et al., 2006) and the possibility that different types of smiles
index different degrees of positive emotion. Despite evident variability within
each type of smile, simple smiles show the lowest mean amplitude followed by
open-mouth smiles, smiles with eye constriction, and then smiles that involve
both mouth opening and eye constriction (see Figure 3). Both in the presence and
in the absence of mouth opening, smiles with eye constriction tend to involve
stronger zygomatic contraction. This is likely due to the synergistic functioning
of these muscles. The muscles are agonists that raise the cheek and may share
common pathways of innervation (Williams et al., 1989). This synergy is also
presumably responsible for the tendency of some interactive smiles to “recruit”
eye constriction as their amplitude increases (Messinger, Fogel, & Dickson, 1999;
Messinger et al., 1997). By contrast, the tendency of smiles involving mouth
opening to involve stronger zygomatic contraction than smiles without seems to
resist those anatomical constraints. Stronger mouth opening is likely to be some-
what antagonistic to upward lip corner movement. This patterning is consistent
with the view that eye constriction and mouth opening index the increased positive
emotional intensity of smiling.
3. The Distribution of Smiles Types During Interaction
Even absent the dimension of smile amplitude, the occurrence of different
types of smiles in different social situations supports the argument that infant
smiles index a continuous positive emotion dimension. Simple smiles—those
involving neither eye constriction nor mouth opening—are more likely to occur
during periods of interaction likely to elicit positive emotion than are nonsmiles.
These are periods of time when infants gaze at their mothers and when their
mothers smile. By the same token, infant smiles involving eye constriction and
mouth opening are relatively more likely than simple smiling in the same social
situations. A conclusion is that simple smiles are more emotionally positive than
neutral expressions, but smiles involving eye constriction or mouth opening are
more emotionally positive than simple smiles. Different types of smiles, then,
may reflect a continuous likelihood distribution of occurrence in affectively con-
gruent situations, suggesting support for an underlying continuous dimension of
positive emotion.
4. Rating Studies
The view that all infant smiles are emotionally positive but some infant smiles
are more positive than others (Messinger et al., 2001) is supported by observers’
ratings of still images of smiles. Undergraduates rate simple smiles as more emo-
tionally positive than nonsmiling neutral expressions (Messinger et al., 2001).
They rate smiles involving eye constriction and smiles of greater amplitude more
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positively than, respectively, smiles without eye constriction and smiles of lower
amplitude (Bolzani-Dinehart et al., 2005). Smiles involving mouth opening also
tend to be rated more positively than smiles without mouth opening, but this
effect can be more subtle. The association between mouth-open smiles and
greater positive emotion sometimes requires a rater who is a parent of an infant
or is visible to a nonparent student rater only when video clips (rather than still
images) are displayed (Cassel et al., 2004).
Indirect support for the emotional intensity hypothesis stems from parallel
findings with cry-faces. Student raters perceive cry-faces involving greater eye
constriction (all cry-faces involve at least some eye constriction) as more nega-
tive than the same cry-faces with minimal eye constriction (Bolzani-Dinehart
et al., 2005; Messinger, 2002). They perceive cry-faces involving greater mouth
opening as more negative than cry-faces with less mouth opening. This suggests
that the features that index stronger positive affect in smiles also index greater
negative affect when they occur with some negative expressions.
5. Automated Measurements of Smiles
The research we have reviewed suggests that infant smile amplitude, eye con-
striction, and, perhaps to a lesser extent, mouth opening, are cumulative indices
of positive emotional intensity. A premise of this research is the existence of
distinct types of smiling. Emerging research techniques, however, are offering
portraits of smiling and infant–mother interaction as continuous processes in
time (Cohn & Kanade, in press; Cohn & Schmidt, 2004; Cohn et al., 1999;
Messinger et al., 2005; Schmidt et al., in press; Schmidt, Cohn, & Tian, 2003).
We have complemented software measurements of facial features indexing the
intensity of infant and mother smiles (see Figure 5) with nonexpert real-time ratings
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Fig. 5. Four-month-old infant and mother smiling interaction captured by Automated Face Analysis
at Carnegie Mellon University, Robotics Institute. Analysis compliments of Jeffrey Cohn, Ph.D. Each
partner’s face is outlined to illustrate lip movement, mouth opening, and eye constriction, and these
outlines are reproduced in iconic form to the right of each partner.
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of the affective valence of the smiles (Messinger et al., 2005). Moment-by-moment
analyses using software measurements reveal that, during face-to-face interaction, a
single infant or mother smile can ebb and flow in amplitude over periods of 20–30 s
(see Figure 3). Such lengthy smiling does not correspond to discrete emotion
accounts of smiles as relatively brief, highly constrained (Ekman & Davidson, 1994;
Frank, Ekman, & Friesen, 1993).
Infant and mother interactive smiles have a continuous structure. In the
course of their smiles, both infants and mothers show a high correlation between
smile amplitude and eye constriction. That is, when infants and mothers smile
more strongly they also show greater eye constriction. It is frequently argued that
Duchenne smiles express joy but non-Duchenne smiles are a social signal unre-
lated to positive emotional expression (Ekman et al., 1990; Frank et al., 1993;
Soussignan, 2002). Eye constriction that waxes and wanes within a smile, how-
ever, may divide a smile into periods in which it is and is not a smile with eye
constriction. It seems unlikely that some of those periods are emotional while
others are not.
The finding that eye constriction changes continuously in concert with smile
amplitude suggests difficulties with the division between Duchenne and non-
Duchenne smiles in infancy. Such dichotomies appear to rest on underlying con-
tinuous changes in smile intensity. This suggests the need for new units of
analysis that transcend smile types. The rise and flow of a single smile in time is
one candidate; another potential unit of analysis is a bout of infant smiles that
may have brief periods of nonsmiling between them. Ultimately, however, infant
smiling is a constituent of a real-time interactive process and the most appropri-
ate unit of analysis is likely to be dyadic. To understand this process, we begin
with an examination of the characteristics of mothers’ interactive smiles.
The differences between infant and mother interactive smiling are as reveal-
ing as the similarities. When infants engage in higher amplitude smiles and
engage in greater eye constriction, they also engage in greater mouth opening. It
is not clear, however, whether associations between smile amplitude and mouth
opening are as strong as between smile amplitude and eye constriction. To some
degree, then, infant smiles appear to involve a single joyful process that is simul-
taneously indexed by two to three facial indices of emotional intensity.
Unlike infants, mothers do not consistently open their mouths to a greater
extent when smiling more strongly. Instead, mouth opening in mothers may be
used both in coordination with speaking and to make exaggerated visual displays
and vocalizations. For example, mothers often repeatedly open their mouths as
they draw their head back from infants and then move their head toward the infant
and close their mouth in a pattern that often involves vocalizing. In some ways,
the caregiver’s role is more complex than that of the infant. Caregivers are
expected both to elicit pleasant, ideally positive, engagement from the infant and
to respond to the infant joyfully in a fluid fashion.
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C. SMILES AS CONTINUOUS INDICES AND SMILES AS
DISTINCT TYPES—A RAPPROCHEMENT?
We have suggested that smiles are, on the one hand, discrete communications
of qualitatively different engagement states and that, on the other hand, they are
continuous signals of the intensity of emotional engagement. How can these
views be integrated? A theoretically satisfying synthesis is that qualitatively dis-
crete positive emotional “attractors”—such as a particular type of smiling in a
particular interactive moment—may self-organize in response to underlying
continuous processes (Chow et al., 2005; Weerth & Geert, 2000).
Currently, however, there may be no definitive resolution to this tension. Just
as light behaves both as a particle and as a wave (Compton & Shankland, 1973),
smiles may function both as discrete indices of specific states of engagement and
as flowing indices of positive engagement. It may be productive, at this juncture,
to adopt the view of social smiling most conducive to a specific phenomenon or
research question while remaining open to the complementary perspective.
Vocalizations, for example, tend to be embedded in the course of a smile such that
the smile is punctuated by the vocalization (Yale, Messinger, & Cobo-Lewis,
2003; Yale et al., 1999). This may create a qualitatively distinct attention-getting
positive emotional expression, or it may serve as an intensifier of facially com-
municated affect (Hsu et al., 2001).
IV. The Interactive Development of Smiling
Whether smiles index a related family of positive emotions or a single emotion
of joy, smiling develops within real-time interactions between infants and social
partners. In this section, we examine interactive smiling and its development from
a dynamic systems perspective. We ask how infants’ smiles are coordinated with
mothers’ smiling and with infants’ gazes at mothers’faces and describe how these
patterns develop to usher in the onset of intentional communication.
A. OVERVIEW OF INTERACTIVE SMILING
Mothers smile more readily than infants. Between 2 and 5 months, mothers’
smiles and other displays such as head nodding and vocalizing are typically nec-
essary to elicit infants’ smiles. But infants frequently do not smile in response to
mother. Mothers’smiles and other displays are not sufficient to elicit infant smil-
ing (Symons & Moran, 1994). An infant smile, by contrast, is typically sufficient
to elicit a mother smile. But infant smiles are by no means necessary to elicit
mother smiles as mothers often smile in the absence of an infant smile (Cohn &
Tronick, 1987; Kaye & Fogel, 1980). When mothers smile in response to
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infants’ smile onsets, they do so within 2 s (Malatesta & Haviland, 1982; Van
Egeren, Barratt, & Roach, 2001).
Interactive smiles are not series of onsets, but continuous processes. Infant and
mother influence not only the onsets of each other’s smiles but the offsets as
well. Mothers rarely break off bouts of mutual smiling. Instead, they terminate
their smiles only after their infants have stopped smiling. When infants gaze
away from mother, they typically terminate their smiles soon after. Thus the
infant’s prototypical experience of smiling is smiling with another.
During face-to-face interactions, infant smiles are often pursued by mothers
and fathers. Fathers tend to employ a more physical style of play with their
infants (e.g., bouncing games), whereas mothers rely more on visual and audi-
tory expressive displays to elicit smiles (Dickson et al., 1997). Perhaps as a con-
sequence, infant positive emotional displays with mother build more gradually
but positive emotional displays such as smiling appear more suddenly with
father (Feldman, 2003).
Generally speaking, caregivers use a wide range of stimulating actions in
multiple modalities (e.g., variations in vocal intensity and pitch, smile inten-
sity, and moving their faces close to the infant), which facilitates the occur-
rence of complex, repeated, interactive patterns. Caregivers’ tickling and
high-pitched vocalizing, for example, might be followed by an infant smile,
the infant gazing away from the caregiver, and a decrease in smiling followed
by the infant gazing again at the caregiver. One possibility is that, in some
respects, the caregiver’s role in this interactive system is analogous to provid-
ing energy in the form of heat to chemical solutions (Hill & Moylan, 1976). The
continuous provision of heat can yield a Benard cell that displays repeating,
complex, but not entirely predictable, visual patterns (Prigogine & Stengers,
1984). Infant–caregiver play is also an open system in which the caregiver’s
positive expressive energy facilitates the emergence of complex, repeating, not
entirely predictable interactive patterns.
B. THE DEVELOPMENT OF SOCIAL SMILING IN
INTERACTIVE CONTEXT
Social smiling is typically studied in industrialized societies and typically
studied during face-to-face interactions with a parent (see Figure 5). Infants
smile for approximately 20% of face-to-face interactions. When observations are
conducted on a weekly basis between 2 and 6 months, individual infants typi-
cally show stable quantities of smiling in face-to-face interactions (Malatesta
et al., 1989). Although approximately one-quarter of the variance in the devel-
opment of smiling during this period is related to individual differences
between infants, the origins and correlates of these differences are not well
understood.
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Between 2 and 6 months, infants spend increasing amounts of time smiling
(Malatesta et al., 1989, 1986). They become more likely to gaze at mother when
she is smiling or creating other facial displays and become more likely to smile
in response to maternal smiles (Cohn & Tronick, 1987; Kaye & Fogel, 1980; van
Beek, Hopkins, & Joeksma, 1994). Infants’ tendency to initiate smiles—even in
the absence of a previous maternal smile—becomes pronounced between 6 and
9 months (Cohn & Tronick, 1987), signaling the infant’s increasingly active,
positive participation in the interaction.
Most of the types of smiling identified in the previous section arise during mul-
tiple periods of face-to-face interaction in the first 6 months of life (Messinger
et al., 2001). Simple smiles that involve neither eye constriction nor mouth open-
ing, for example, arise in periods characterized by both the presence and absence
of the infant’s gaze at mother’s face and the presence and absence of mother smil-
ing (see Figure 6). This suggests that infants’ use of less affectively intense simple
smiling does not become more specific with age. This is surprising as simple smil-
ing, by 12 months of age, predominates during pleasurable but not extremely
arousing activities such as book reading (Dickson et al., 1997).
In contrast with simple smiling, open-mouth smiling involving eye constriction
shows a distinct developmental trajectory. Between 1 and 6 months of age, infants
become increasingly likely to use open-mouth smiling with eye constriction—
which is almost certainly high-amplitude smiling—to interact with their mothers
when their mothers are smiling. They become increasingly less likely to engage in
this smiling when they are not gazing at mother and mother is not smiling. In sum,
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Age Period in MonthsAge Period in Months
Proportion of Simple Smiling Involving
Neither Mouth Opening or Eye Constriction
Proportion of Combined Open-Mouth
Smiling with Eye Constriction
Fig. 6. Open-mouth smiling with eye constriction increases when infants are gazing at their mothers’
faces while their mothers are smiling. It decreases when infants are not gazing at their mothers while
their mothers are not smiling. By contrast, smiling with neither characteristic, that is, smiling alone,
tends to increase irrespective of where the infant is gazing and whether or not the mother is smiling.
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infants’ increasing tendency to engage their smiling mothers with open-mouth
smiling with eye constriction between 3 and 6 months appears to reflect their
growing capacity to engage dynamically in intensely joyful interactions.
C. SMILING INTERACTION DYNAMICS
In interaction, caregiver and infant continuously provide and receive social
information, via changes in facial expression, vocal tone, touch, movement, and
the direction of infant gaze (Cohn & Tronick, 1987; Feldman, 2003; Feldman &
Greenbaum, 1997; Feldman, Greenbaum, & Yirmiya, 1999; Feldman et al.,
1996; Fogel, 1988, 1993). To examine interactive emotional influence, we
employed the automated measurements of smile intensity in infants and in
mothers discussed earlier. As noted earlier, eye constriction and mouth open-
ing were associated in infants, and smile amplitude and eye constriction were
associated in mothers. This suggests at the outset that infant’s use of mouth
opening in smiles is not directly related to mother’s use of mouth opening.
In other words, infants and mothers are not precisely imitating the form of
each other’s smiles.
In examining how each partner influenced changes in the other’s positive
expressions, we identified two initial patterns. One dyadic pattern was charac-
terized by rapidly repeating, tightly linked rises and falls in infant and mother
smiling that were punctuated by the mother tickling the infant. Another pattern
involved slower, less synchronous rises and falls in infant and mother smiling
and a less prominent role for mother tickling. The ultimate goal of this research
is to document how each partner influences the rate of change, the actual emo-
tional dynamics, of the other partner’s expressions (Boker & Nesselroade, 2000;
Chow, 2005; Rotondo & Boker, 2002).
D. INFANTS’PERCEPTIONS OF INTERACTIVE SMILING
Infants’ perceptions of the smiling of others also shed light on the develop-
ment of positive emotion. Researchers often examine infant smiling within inter-
active contexts marked by responses to maternal smiles and vocalizations.
Rarely, however, is this work integrated with investigations of the conditions
under which infants recognize smiles. In fact, however, it is important to explore
infants’ comprehension of emotion expressions in an ecological context similar
to that in which they communicate using these expressions. By 3½ months,
infants gaze longer at a dynamic facial expression (happy or sad) that matches
that of a concordantly presented vocalization, even after a brief delay. The effect
is present, however, only when the infant’s mother—not an unfamiliar female
tester—produces the displays (Kahana-Kalman & Walker-Andrews, 2001;
Montague & Walker-Andrews, 2002).
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Contextual information—provided by peekaboo—also appears to facilitate
early recognition of smiling expressions (Montague & Walker-Andrews, 2001).
When 4-month-olds participate in peekaboo games in which a tester’s
happy/surprised expressions are systematically replaced with anger, fear, or sad-
ness expressions, infants show greater interest and surprise and different patterns
of visual attention to the discrepant expressions.
V. Smiling and Attention to the Caregiver
A. SMILES AND AROUSAL MODULATION
Although smiles are approach-oriented signals of enjoyment, infants may also
use smiles to manage arousal. Arousal in infants is indexed by increased heart
rate and by arousal-modulation activities such as mouthing objects and gazing
away from engaging stimuli (Weinberg & Tronick, 1996). As in adults
(Cacioppo et al., 2000), an infant’s heart rate is more rapid during smiling than
during neutral expressions (Emde et al., 1978). Infants tend to mouth their hands
while smiling, suggesting that smiles may be involved in tension reduction.
Smiles typically occur while gazing at the caregiver’s face (Weinberg & Tronick,
1994) and this may also may be relevant to infant arousal modulation. Face-to-face
visual regard is a relative rarity among nonhuman primates. Among all primates,
including humans, face-to-face visual regard can be used a threat display. It is pos-
sible, then, that infant smiles can be used to maintain arousing face-to-face eye con-
tact (cf. Morris, 1967). We have, for example, observed smiles to occur in close
temporal proximity and even overlap negative emotional expressions. This occurs,
for example, as caregivers attempt to “cheer up” infants who have become overex-
cited in play or are recovering from the still-face perturbation (Weinberg & Tronick,
1996). Documentation of such patterns might suggest that smiles themselves can be
used to regulate arousal and that the arousal regulation capacity of infant smiles is
sometimes overwhelmed, leading to a negative expression.
B. THE EARLY COORDINATION OF SMILING AND GAZING AT
THE CAREGIVER’S FACE
From a developmental perspective, infants between 2 and 3 months of age
occasionally smile at a social partner (sometimes they smile at themselves in a
mirror) and then gaze away. Smiles in which infants gaze away before the peak
of the smile is reached have been described as communicating a “coy” quality
and naïve observers perceive some smiles with these characteristics as indicative
of shyness (Draghi-Lorenz, Reddy, & Morris, 2005; Reddy, 2000).
The coordination of smiles with gazing changes and becomes more precisely
patterned with age (Yale et al., 2003, 1999). Simulation studies suggest that, at
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3 months, the pattern of gazing away during a smile actually occurs less than
expected by chance (Yale et al., 2003, 1999). The simulation studies indicate that
3-month-olds tend to begin and end their smiles within the course of a gaze at
the parent’s face (Yale et al., 2003). That is, early expressions of positive emo-
tion are dependent on continuous visual contact with the parent. By 6 months,
infants redirect their attention after sharing positive emotional expressions with
their parents. They tend to gaze at mother’s face, smile, gaze away, and then end
the smile. Such gaze aversions—at least among 5-month-olds playing peeka-
boo—tend to occur during higher intensity smiles and smiles of longer durations
(Stifter & Moyer, 1991).
It is suggestive that toward 6 months of age infants become especially likely
to control their own positive emotion by gazing away from mother during the
course of a smile. This is also the period in which infants become adept at
using intense open-mouth smiles with eye constriction to participate in highly
arousing social situations. Infants are simultaneously becoming more actively
positive during interactions and becoming more active at regulating the condi-
tions under which they will become positive engaged (Messinger et al., 2001;
Yale et al., 2003).
C. THEORETICAL PERSPECTIVES RELEVANT TO
SMILES AND GAZE AVERSION
Theoretical perspectives hailing from social psychology may be relevant to
infant gaze aversion during smiles. One theoretical perspective holds that pos-
itive emotion occurs when an individual attains a goal faster than anticipated
(Carver, 2001, 2003). Goals are desired end states. When goals are attained
more rapidly than expected and positive emotion occurs, the individual is
likely to attend to other features of the environment including other potential
goals. This may be partially responsible for the broader, more creative cogni-
tive set of adults after they have experienced positive affect (Fredrickson,
2001; Fredrickson & Joiner, 2002).
Although infants’ goals are relatively inchoate, Carver’s (2001, 2003) proposal
may be relevant to infant’s proclivity to gaze away from the parent’s face during a
smile. Infants are learning to expect peaks and declines in arousal associated with
interactive smiling. The infant’s growing tendency to gaze away from the parent’s
face during a smile may index the infant’s developing comprehension that an affec-
tive climax has been reached; that is, in the most primitive sense, a goal has been
achieved. In this sense the infant’s smiling behavior may index the infant’s affective
and cognitive comprehension of their interface with the environment at a particular
moment (Fogel, Bosma, & Kunnen, 2001).
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VI. Smiling and Referential Communication
In this section, we examine infants’ developing capacity to utilize smiles to
communicate intentionally toward the completion of the first year of life. In
the first 6 months, infant emotional expressions appear to reflect, for the
most part, a primary, nonreflective communication of immediate experience
(Kaye & Fogel, 1980). Infants engage in intricate communicative smiling
exchanges at 6 months, but their smiles are the message. They do not clearly
communicate about external events. Surprisingly, the form of infant smiling
does not appear to change between 6 and 12 months (Fogel et al., 2006).
Instead, it is the timing of smiles and gazes at a social partner that changes as
smiles become vehicles for referential communications about external objects
and events.
By way of backdrop, between 8 and 12 months, infants begin to communicate
desires and experiences intentionally to their communicative partners (Adamson &
Bakeman, 1985). Infants create conventional or ritualized behavior patterns with the
apparent intent of influencing another. Infant smiles are more likely to accompany
protodeclarative communication, whose goal is showing or sharing, than protoim-
peratives, whose goal is obtaining an object or action (Kasari et al., 1990;
Messinger & Fogel, 1998).
Both smiles and protodeclarative gestures tend to occur in the context of coordi-
nated joint engagement in which the infant actively shifts attention between a toy
and a social partner (Adamson & Bakeman, 1985). These gestures and attentional
patterns are often referred to as triadic communication in that the infant refers to an
object or event outside the infant–partner dyad. Patterns of triadic joint engagement—
both those that are accompanied by smiles and those that are not—increase sub-
stantially between 5 and 9 months (Striano & Bertin, 2005). Yet the percentage of
infants who accompany a gaze between a toy and an adult with a smile is dramati-
cally less than the percentage of infants who only coordinate gazing between the toy
and the adult at 5, at 7, and at 9 months. This suggests that combining a smile with
a gaze at an attentive adult indexes a more complex communicative achievement
than gazing alone.
Anticipatory smiles are a specific temporal pattern of smiling and gazing at a
partner that may have special intersubjective significance (see Figure 7) (Venezia
et al., 2004). Anticipatory smiles occur when an infant smiles at an interesting
toy or event and then turns to gaze at another person while continuing to smile.
We have studied anticipatory smiles during infant initiations of joint attention in
which a tester places a windup toy on a table (Mundy, Hogan, & Doehring, 1996;
Seibert, Hogan, & Mundy, 1982). In this context, the infant’s smile while gazing
between the object and social partner appears to communicating something like,
“that was funny, wasn’t it?”
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Developmental and associated evidence suggests infants use anticipatory
smiles to communicate preexisting positive affect to another person. Infant antic-
ipatory smiles—whether occurring in interaction with mother or an experimenter—
increase between 8 and 12 months. This developmental increase is not seen in
rates of initiating joint attention generally or in other patterns of smiling
accompanying initiations of joint attention. The degree to which infants engage
in anticipatory smiling is associated with separate measures of their level of
intentional communication and understanding of means–end relationships
(Jones & Hong, 2001). This suggests that, when engaging in anticipatory smiles,
infants are coming to understand and refer to the relation of an adult and an
object. During anticipatory smiles, infants smile and, in real time, reference an
object to another. From a dynamic systems perspective, this real-time process
suggests how positive affect may motivate the development of early referential
communication (Adamson & Bakeman, 1985; Fogel & Thelen, 1987; Jones &
Hong, 2005; Venezia et al., 2004)
VII. Pragmatics: the Representativeness, Discriminant, and
Predictive Validity of Infant Smiling
This section reviews literature on the representativeness of laboratory studies
of infant smiling and differences in smiling between typically developing and at-
risk infants. We then examine associations of infant smiling with developmental
outcomes.
A. REPRESENTATIVENESS OF SMILING
Many of the studies reviewed in this chapter occurred in controlled labora-
tory settings. Interest in developmental outcomes, then, raises questions con-
cerning the stability and representativeness of findings. In Western
industrialized societies the quantity of infant smiling coded during the 3-min
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Fig. 7. Anticipatory smile. A 15-month-old infant gazes at an object (left), smiles at the object
(middle), and gazes at the experimenter while continuing to smile (right).
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face-to-face interactions with mother typically is correlated with infant affec-
tive state observed during 2–3 h home observations (Cohn et al., 1990). Infant’s
positive smiling reactions to social stimuli such as peekaboo are associated with
observed infant positive emotional tone during interactions with parents and
with parent ratings of their children’s day-to-day positive emotions (Aksan &
Kochanska, 2004). From a broader perspective, however, frustratingly little is
known concerning the frequency and duration of smiling outside of the struc-
tured face-to-face interactions that have been observed by researchers in the
day-to-day life of infants in industrialized societies. Rates and types of smiling
do, however, allow developmentalists to discriminate between typically and
atypically developing infants.
B. SMILING IN ATYPICALLY DEVELOPING INFANTS
Patterns of smiling allow us to distinguish typically developing infants from
infants at risk for different types of disturbed development. Infants at risk for
autism exhibit lower levels of smiling than typically developing infants (Cassel
et al., in press; Zwaigenbaum et al., 2005). Maternal depression and maternal
depressive symptomatology, particularly when chronic, tend to be associated
with less frequent infant smiling, at least during interactions with mother (Moore
et al., 2001). Smiles are more frequent among healthy infants than among those
with a history of neurological complications or other illnesses related to preterm
birth (Bigsby et al., 1996).
Infants at risk for developmental difficulties also show deficits in particular
types of smiling. Premature infants, for example, engage in lower levels of high
amplitude and/or open-mouth smiling during face-to-face interactions and
exhibit fewer high-amplitude smiles during peekaboo games with a trained
experimenter than do full-term infants (Eckerman et al., 1999; Segal et al.,
1995). This difference is likely due to premature infants’reduced capacity to tol-
erate highly arousing positive affect. An opposite pattern is seen in infants with
Down syndrome. These infants show a pattern of somewhat indiscriminate
intense smiling. They tend to direct smiles with eye constriction and mouth
opening both to the toys with which they are playing and to their mothers,
whereas typically developing infants direct these smiles only to their mothers
(Berger & Cunningham, 1986; Carvajal & Iglesias, 2001).
C. SMILING AND DEVELOPMENTAL OUTCOMES
Still-face studies are often the basis for investigations of the predictive validity
of early smiling. Individual infants show consistency in smiling levels over the
episodes of face-to-face/still-face, particularly between the interactive face-to-face
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and reunion episodes (Carter, Mayes, & Pajer, 1990; Cassel et al., in press; Moore
et al., 2001; Weinberg et al., 1999). Surprisingly, smiling at the still-face does not
increase after 1½ months of age (Bertin & Striano, 2006; Lamb, Morrison, &
Malkin, 1987), nor does it show developmental stability within infants (Moore
et al., 2001). The possibility that smiles during the still-face can be positively char-
acterized as bids for the parent’s attention deserves increased attention from
researchers.
There is some evidence that infant smiling in the face of the challenge of
the parental still-face may index emotional resilience. Six-month-old infants
who smile during the still-face are more likely to become securely attached at
12 months than infants who do not (Cohn, Campbell, & Ross, 1991). They are
also perceived by their parents as having fewer externalizing behaviors at
18 months than infants who did not smile during the still-face (Moore et al.,
2001). Still-face smiling may reflect an infant’s expectations of positive com-
munication and be associated with dyadic patterns of harmonious interaction
that subsequently lead to more optimal developmental outcomes.
Positive affect sharing indexed by anticipatory smiling may be one link between
early social smiling and subsequent social expressivity and competence (Parlade,
Messinger, & Mundy, 2006). Smiling by 6-month-olds in face-to-face interaction
with a parent and in the subsequent still-face positively predicts mean levels of antic-
ipatory smiling with a tester between 8 and 12 months. An infant’s experience with
early gratifying social interaction probably contributes to a continued tendency to
share positive affect with an adult. In fact, affectively positive infant joint attention
communications are, more generally, predicted by highly sensitive maternal caregiv-
ing (Hane & Fox, 2006). In addition, mean levels of anticipatory smiling predict par-
ent-reported social expressivity and social competence at 30 months (Parlade et al.,
2006). Infants who share smiles with relatively unfamiliar adults may be more moti-
vated than other infants to engage socially and emotionally with others.
Researchers motivated by a positive psychology perspective have become
involved in investigating the impact of positive emotions—above and beyond the
absence of negative emotion—on interpersonal competence and well-being.
Positive emotional experience in infants may, as in adults, broaden the scope of
attention and the behavioral repertoire and elicit positive responses from social
partners (Fredrickson, 2001; Fredrickson & Joiner, 2002; Harker & Keltner,
2001). One longitudinal study relied on an extreme groups design in which
infants were selected based on their emotional reactions to neutral stimuli at
4 months of age (Fox et al., 2001). Infants who engaged in more smiling,
neutral/positive vocalizations and motor movement were compared to infants
who had negative reactions or were not responsive to the stimuli. The infants
who showed earlier emotional positivity exhibited less behavioral inhibition in
unfamiliar situations over the first 2 years of life than other infants. They con-
tinued to show a more exuberant temperamental style at 4 years when they were
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more likely to talk and engage with peers (Fox et al., 2001). Similar results have
been reported among a normative sample of 18-month-olds observed during
reunions with mother in the Strange Situation (Abe & Izard, 1999). Infant smil-
ing involving eye constriction (Duchenne smiling) predicted parent ratings of
extraversion and openness to experience when children were 3½ years of age.
Smiling interactions involve coconstructing processes of responsive engage-
ment. Relationships characterized by this mutual positivity may have rela-
tively enduring developmental effects. Caregiver positive emotional
responsivity to the infant is associated with later internalization of social
norms and committed compliance to maternal requests (Kochanska, 2002;
Kochanska, Forman, & Coy, 1999). Experiences of affectively positive
responsivity, participation in the ebb and flow of joyful engagement, may
enable infants to experience their own joy as a mutual process. Joy is not only
shared but created in such interactions. The delight of engaging in a positive
process bounded by mutual expectations ultimately contributes to the creation
and internalization of social norms.
VIII. Summary and Conclusions
Infant smiles emerge even in the absence of visual feedback, but their interac-
tive development and intensification appear to be dependent on experiences of
visually mediated interaction. Although neonatal smiling has no clear emotional
content, social smiling emerges out of attentive engagement with an interactive
caregiver. This process illustrates the dynamic systems postulate that real-time
interaction is a window on developmental process.
On the one hand, specific dimensions of smiling may have qualitatively dif-
ferent psychologically meanings. On the other hand, different features of infant
smiling may reflect linked indices of a single dimension of positive emotion that
ebbs and flows in time. The resolution of this paradox will likely involve con-
tinued attention to the interactive flow of positive emotion communication. This
will be facilitated by new methods for measuring smiling and positive emotion
in time.
Smiling may simultaneously index a desire to interact and the dissipation of
arousal associated with that interaction. Infants’ capacity to become actively
and vigorously caught up in emotionally positive smile-mediated interaction
is linked to their ability to regulate that emotion by gazing away from their
interactive partners. Ultimately, this attentional control paves the way for
infant’s tendency to use smiles to initiate early referential communication with
a partner. These anticipatory smiles may provide a developmental bridge
between early emotionally positive dyadic responsivity and later patterns of
social competence.
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Acknowledgments
Work on this chapter was supported by NICHD 41619 and NSF 0418400 and
facilitated by the insights of numerous colleagues including Kim Bard, Sy-Miin
Chow, Jeffrey Cohn, Ruth Feldman, Heather Henderson, Peter Mundy, and
Meaghan Venezia-Parlade.
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