Infants and Young Children Vol. 16, No. 2, pp. 120–142 c ... · Emotional Expressions of Young...

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Infants and Young Children Vol. 16, No. 2, pp. 120–142 c 2003 Lippincott Williams & Wilkins, Inc. Emotional Expressions of Young Infants and Children A Practitioner’s Primer Margaret Wolan Sullivan, PhD; Michael Lewis, PhD Research on emotional development in infancy has benefited greatly from the use of video- tape technology and coding systems that allow detailed coding of facial movements. Today we know that a core set of human facial expressions, composed of specific movements in the brow, eye/cheek, and mouth regions of the face, are probably innate. Theorists continue to debate the meaning of these expressions as well as how they are organized and become regulated over the first several years of life. Despite continuing debate and research on these issues, early facial ex- pressions have practical, signal value for caregivers and practitioners alike. This article surveys what is known about the appearance and early normative, developmental course of emotional expressions, noting similarities and differences in special populations when available. Its goal is to provide practitioners with basic information to help them and the parents they serve become better able to recognize the expressive signals of the infants and young children in their care. Key words: emotion, emotional development, facial expressions, infants, nonverbal commu- nication S YSTEMS for deciphering the facial expres- sions of infants and young children were developed in the 1980s. These systems rep- resent important and needed tools for pro- moting more accurate, empirical study of early emotional development. With them, re- searchers are beginning to understand when infants first express particular emotion sig- nals facially, the organization of these signals, and their relation to other aspects of moti- vated behavior. While many important ques- tions about the meaning and developmental course of early expressions continue to be re- searched and debated, it is now recognized that most, if not all, of the facial components of the human expression repertoire can be ob- served shortly after birth (Camras, Holland, & Patterson, 1993; Izard & Malatesta, 1987; From the Institute for the Study of Child Development, UMDNJ-Robert Wood Johnson Medical School, New Brunswick, NJ. Corresponding author: Margaret Wolan Sullivan, In- stitute for the Study of Child Development, UMDNJ- Robert Wood Johnson Medical School (e-mail: sullivan@ umdnj.edu). Lewis & Michalson, 1983). Despite this find- ing, facial coding systems have only just be- gun to move out of the laboratory into clinical settings (Gilbert et al., 1999). This is unfor- tunate, because information about facial ex- pressions potentially has practical import for those working with infants, older, nonverbal children, and their caregivers. For practitioners, facial expressions are in- formative in 2 ways. First and foremost, they are social signals to others. Crying, vocaliz- ing, and bodily movements combine with fa- cial expression to provide cues to an infant’s status. Savvy caregivers no doubt make use of all of these cues in interpreting infant be- havior. Although psychologists may be reluc- tant to assign a specific emotion value to infant facial expressions, parents have no problem doing so. In fact, they routinely use facial expressions to attribute personality and intellectual characteristics to a young baby (Haviland, 1983). They also use facial expres- sions to gauge their own responses, thus help- ing to regulate their infants’ arousal and teach- ing them display rules (Malatesta & Haviland, 1982). Parents’ reading and interpretation of 120

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Infants and Young ChildrenVol. 16, No. 2, pp. 120–142c© 2003 Lippincott Williams & Wilkins, Inc.

Emotional Expressions ofYoung Infants and ChildrenA Practitioner’s Primer

Margaret Wolan Sullivan, PhD; Michael Lewis, PhD

Research on emotional development in infancy has benefited greatly from the use of video-tape technology and coding systems that allow detailed coding of facial movements. Today weknow that a core set of human facial expressions, composed of specific movements in the brow,eye/cheek, and mouth regions of the face, are probably innate. Theorists continue to debate themeaning of these expressions as well as how they are organized and become regulated over thefirst several years of life. Despite continuing debate and research on these issues, early facial ex-pressions have practical, signal value for caregivers and practitioners alike. This article surveyswhat is known about the appearance and early normative, developmental course of emotionalexpressions, noting similarities and differences in special populations when available. Its goal isto provide practitioners with basic information to help them and the parents they serve becomebetter able to recognize the expressive signals of the infants and young children in their care.Key words: emotion, emotional development, facial expressions, infants, nonverbal commu-nication

SYSTEMS for deciphering the facial expres-sions of infants and young children were

developed in the 1980s. These systems rep-resent important and needed tools for pro-moting more accurate, empirical study ofearly emotional development. With them, re-searchers are beginning to understand wheninfants first express particular emotion sig-nals facially, the organization of these signals,and their relation to other aspects of moti-vated behavior. While many important ques-tions about the meaning and developmentalcourse of early expressions continue to be re-searched and debated, it is now recognizedthat most, if not all, of the facial componentsof the human expression repertoire can be ob-served shortly after birth (Camras, Holland,& Patterson, 1993; Izard & Malatesta, 1987;

From the Institute for the Study of ChildDevelopment, UMDNJ-Robert Wood Johnson MedicalSchool, New Brunswick, NJ.

Corresponding author: Margaret Wolan Sullivan, In-stitute for the Study of Child Development, UMDNJ-Robert Wood Johnson Medical School (e-mail: [email protected]).

Lewis & Michalson, 1983). Despite this find-ing, facial coding systems have only just be-gun to move out of the laboratory into clinicalsettings (Gilbert et al., 1999). This is unfor-tunate, because information about facial ex-pressions potentially has practical import forthose working with infants, older, nonverbalchildren, and their caregivers.

For practitioners, facial expressions are in-formative in 2 ways. First and foremost, theyare social signals to others. Crying, vocaliz-ing, and bodily movements combine with fa-cial expression to provide cues to an infant’sstatus. Savvy caregivers no doubt make useof all of these cues in interpreting infant be-havior. Although psychologists may be reluc-tant to assign a specific emotion value toinfant facial expressions, parents have noproblem doing so. In fact, they routinely usefacial expressions to attribute personality andintellectual characteristics to a young baby(Haviland, 1983). They also use facial expres-sions to gauge their own responses, thus help-ing to regulate their infants’ arousal and teach-ing them display rules (Malatesta & Haviland,1982). Parents’ reading and interpretation of

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the infant’s expressive cues in daily interac-tion are key to the child’s social development,emotion regulation, and early language learn-ing (Mundy & Willoughby, 1996; Walden &Knieps, 1996). Consequently, whether par-ents observe and are having difficulty inter-preting the expressive signals of their infantshould be an important screening question forthe practitioner.

Although some adults seem to have “nat-ural” skills at reading emotional expressions,others will need some training to recognizethe facial signals of young infants whose ex-pressions are often fleeting, subtle, and per-haps less well organized than those of olderchildren. This problem can be compoundedwhen there is neurological impairment ordevelopmental delay. Expressive behaviorsof infants and children with various formsof disability have been described as muted,hard-to-read, or excessively labile and incon-gruous, depending on the population un-der study (Mundy, Yirmiya, & Sigman, 1990;Kasari & Sigman, 1996; Sigman, Kasari, Kwon,& Yirmiya, 1992). When parents are un-able to recognize and interpret emotional sig-nals from their infants, they will be uncer-tain about their child’s needs and less ableto share positive affect. Consequently, par-ents may become less expressive themselves(Dawson, Hill, Spencer, Galpert, & Waton,1990), further degrading the quality of interac-tion. Learning to recognize facial expressionsand how they evolve is a worthwhile effortbecause these and other nonverbal cues ofemotion offer another channel of communi-cation when children’s behavior or vocal ut-terances are absent, or unclear. This channelsignals the infant’s arousal level, somethingabout the quality of the infant’s positive ornegative response to concurrent stimulation,and may help explain other aspects of motor,postural, and behavioral responses. In short,the ability to interpret infants’ expressive sig-nals is extremely important to parents person-ally and to promoting mutually satisfying inter-actions.

Another way expressions can be helpful topractitioners is that they offer clues to the

neurological and cognitive status of the child.Facial expressions are controlled through thefacial cranial nerves but are also intimatelylinked to cognitive development (Lewis &Michalson, 1983). Consequently, young chil-dren’s facial expressions have some clinicalsignificance. Although their initial appearanceis organized at the brain’s subcortical level,changes in their form or developmental pat-tern over time reveals that the child’s highercognitive and motivational systems are be-coming integrated as brain maturation pro-ceeds. Appropriate developmental changes infacial signals imply that certain cognitive func-tions are preserved in neurologically dam-aged children, for example. This fact haslong been recognized for smiling (McCall,1972), but is likely to be true for otherexpressions as well.

Data on individual differences in facial ex-pressions, their developmental trajectory innormally developing populations, and spe-cific information about facial expressions inatypical populations is growing. This articlesurveys the expressions of which infants andyoung children are capable as revealed by fa-cial coding systems such as MAX (MaximallyDiscriminative Facial Coding System), its com-panion, whole-face scoring system, AFFEX(Affective Expressions Scoring System; Izard,1982), and Baby FACS (Facial Action CodingSystem; Oster, 1978) and will cover typical ex-pressions. The article will not treat related andimportant topics such as arousal, physiologi-cal reactivity, or emotion regulation. Rather,the focus is a pragmatic one of how to rec-ognize expressions—whether they are mutedor intense, prototypic or idiosyncratic. Like-wise, we set aside the thorny theoretical ques-tion of whether the emotional experiences ofvery young children are similar to or differentfrom those of older children and adults. Sincethe discussion of expressions will make useof the movements described in MAX, AFFEX,and FACS, we briefly consider the nature ofthese tools.

Although some of the assumptions underly-ing MAX and AFFEX, as opposed to the BabyFACS coding systems, remain controversial,

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research using these systems shows that mostof the facial movements comprising adultemotion expressions are present and maponto positive and negative reactions to stim-ulation during the first months of life. MAX,AFFEX, and Baby FACS also share many fea-tures. For example, all observe movementsof the facial musculature in the forehead,eye/cheek, and mouth regions of the face.They also agree, for the most part, on thosefacial movements that constitute emotionsignals. The major differences between thesystems are their theoretical orientation andcomprehensiveness in scoring facial move-ments.

MAX and AFFEX focus on a theoret-ically limited set of “prototypic” expres-sions of adults. In contrast, Baby FACSdoes not, and is comprehensive in scor-ing all possible movement combinations. Be-cause MAX (Izard, 1983/1995) concentrateson those facial movements that are max-imally discriminative of 9 specific humanemotion expressions, it lends itself morereadily to applied situations. Besides the9 facially expressed emotions (ie, Interest,Surprise, Enjoyment, Anger, Sadness, Fear,Disgust, Contempt, and Shame), several con-trol or regulatory movements are also in-cluded in MAX. Blended expressions, describ-ing combinations of specific facial movementsin the face, also are deciphered (for example,Anger/Sad is a common expression blend ininfants). In MAX, single component expres-sions are thought to reflect a lower intensityof expression than are signals occurring in all3 facial regions (Abe & Izard, 1999). MAX, likeBaby FACS, is designed for use with videotapeor still photographs, but AFFEX can be usedas a live observational system. If you are inter-ested in what facial expression or expressionscan be “read” as emotional signals, MAX orAFFEX is the best application. We use it hereto present the facial expressions of infancy,describing specific expressions, their devel-opment, and what is currently known aboutthem in specific disabling conditions. The ex-pressions are described as related sets or fam-ilies because of the well-established finding

that infants’ expressions to any given contextvary across individuals. Even within individ-uals, multiple expressions seen in rapid suc-cession are common. Expressions are also sel-dom pure and may blend 2 emotion signals.Since blended expression may persist in somechildren (Yirmiya, Kasari, Sigman & Mundy,1989), the developmental course of andindividual differences in blends are of someinterest.

THE INTEREST FAMILY

Some do not consider interest is an emo-tional expression, but since it is a sign of pos-itive approach and receptivity to people andobjects, it is coded in MAX/AFFEX as a familyof expressions distinct from a neutral, awake,but nonexpressive face. Figure 1 illustrates3 varieties of interest occurring in young in-fants. Notice that in all of the photographs,the infants appear alert and attentive. How-ever, there are subtle differences in their ex-pressions, signaling differing qualities of thatattention.

Figure 1a has been characterized asthe “open” or relaxed interest expression(Sullivan & Lewis, 1989; Sullivan, Lewis,& Alessandri, 1992). The brows are raisedslightly, eyes wide open. The mouth is re-laxed and open, taking a bow-shape as shownhere. The mouth may be closed in somevariants, but the key is that there is no signof tension. This expression occurs in envi-ronments that offer the infant low intensity,nonthreatening stimulation. Also describedas “curious” and “wide-eyed wonder” in thenonscientific literature, open interest is byfar the most common expression of younginfants. Adults, on the other hand, typicallymaintain a neutral/awake expression as ourmodal expression. This is not the case forinfants, whose faces are rarely still and whoseexpressions change rapidly (Malatesta &Haviland, 1982). In fact, a “neutral” or soberface is rare in awake, attentive infants muchbefore about 9 months of age (Lewis &Sullivan, 1988). The common occurrence ofopen interest reflects the “positivity offset”

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Fig 1. Three forms of interest: (a) open interest, (b)knit brow interest, and (c) interest with lip roll.

of the central nervous system (Cacioppo& Gardner, 1999). That is, humans showa mild bias toward positive emotion and amotivation to approach novel objects, stimuli,or contexts. Very young infants showing the

relaxed, open interest expression are ready toexplore—if only visually—the environmentaround them.

Figure 1b shows a form of interest sug-gesting greater intensity. It is “excited” or“knit-brow” interest (Camras, 1992; Sullivan& Lewis, 1989). The major difference fromFig 1a is the upper face region. The browsstand out more prominently because the fore-head muscles have been contracted. Theyare pulled together, sometimes slightly asshown here, sometimes more strongly, mak-ing central bulges. The eyes appear slightlynarrowed, resulting in crinkling or furrowingof the outer eye muscles known as crow’s feet.Infants showing this expression appear to beintensely interested. They may vocalize whileshowing this expression or momentarily be-come still. They have a concentrated or evena quizzical look, as if they are actively study-ing what they are looking at. Knit brow in-terest is observed during young infants’ so-cial interactions, marking periods of gazingat mother or father (Malatesta & Haviland,1982; Oster, 1978). It persists as much as10 seconds, thereafter either resolving into asmile or, in some cases, fussing, if the inter-action has been overwhelming (Oster, 1978).This expression has a specific developmen-tal trajectory (Lewis, Sullivan, & Alessandri,1990; Malatesta & Haviland, 1982). Seen fre-quently in young infants, it decreases between2 and 8 months, appearing again regularly by10–12 months (Malatesta & Haviland, 1982;Malatesta, Culver, Tesman & Shipard, 1989;Sullivan and Lewis, 1988). Knit-brow interestat these ages typically occurs in situations thatchallenge infants or requires problem-solving.It has also been referred to as a wary facein studies of response to novel objects. Insuch contexts, this expression is coupled withthe inhibition of motor behavior (Bronson,1972; Lewis & Michalson, 1983). Warinesssuggests a state of heightened vigilance oruncertainty. Collectively, the findings sug-gest that knit brow interest is a form ofhighly focused, effortful attention associ-ated with active information processing. Theage change in its occurrence may mark a

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developmental shift in the type and qualityof stimulation that infants must “work” toassimilate.

Figure 1c shows an interest expression thatincludes one of MAX’s regulatory movements,a thinning and rolling inward of one or bothlips. This expression was seen widely someyears ago as the whimsical expression ofCabbage Patch@ baby dolls. This lip move-ment seems to be regulatory because it fre-quently suppresses smiling; however, its ex-act signal value in infants remains unclear. Inolder infants and children however, it tendsto be combined with or precede gaze aver-sion. After about 12 months, coordinationof this mouth expression with head and eyemovements signals the child’s awareness ofthe other’s unwanted attention in social situa-tions. Head lowering and gaze aversion func-tion to withdraw from or reduce undesiredsocial interaction, and when combined withthis lip movement may signal either embar-rassment or shyness toward a social part-ner, depending on the context and presenceof other bodily cues (Lewis & Brooks-Gunn,1979; Lewis, Sullivan, Stanger, & Weiss, 1989).After the onset of self-cognition at about 18months of age, this lip expression may oc-cur in evaluative settings. When coupled withbody collapse, mouth components suggest-ing sadness, and/or withdrawal from a task,it signals shame or evaluative embarrassment(Lewis, Alessandri, & Sullivan, 1992; Lewis,2000).

Infants with neurological impairment andvarious disabling conditions are frequentlyreported to have difficulties attending. Thesedifficulties are often noted during infancy orare detected as learning disabilities as chil-dren reach school age. Differences in the formor patterning of interest expressions mayappear as well and may offer early markers.Attention, unfortunately, has been studiedalmost exclusively as motor behavior, ie,visual, auditory, or even cardiac orienting tostimuli, not as facial expressions. Exceptionsare studies of emotion during joint attentionprimarily in children with autism and mentalretardation. In this work, children with thesedisabilities are compared to each other

and with an MA-matched group to observedifferences in MAX-coded positive, negative,interest (all forms) versus neutral expressions(e.g. Kasari et al, 1992; Yirmiya et al., 1992).This work finds that autistic children displayprimarily neutral and interest expressionsfor somewhat longer periods than do othergroups. Increased interest in autistic childrenappears at the expense of less enjoymentexpressions (Yirmiya et al., 1989). No pub-lished study has examined developmentaltrajectories or examined differences ininterest expressions in any atypical popula-tion. Knowledge about the range, distribu-tion, and pattern of these expressions maybe of some clinical use in identifying those inneed of further assessment.

SURPRISE

The Surprise expression is rarely seen inyoung infants, especially in the full formshown in Fig 2. In surprise expressions, thebrows are raised and prominently arched. Theeyes are widened so that the white of thesclera is more evident than in relaxed inter-est. The mouth gapes with jaw slackened,

Fig 2. Surprise in a 5-month-old.

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assuming an “o” shape, and may be ac-companied by abrupt, momentary stillingof other ongoing behavior. The expressionin Fig 2 occurred when a 5-month-old ac-cidentally turned on slides and taped mu-sic by tugging on a ribbon attached to herwrist (Sullivan & Lewis, in press). Surpriseis an appropriate expression in this contextof sudden, unexpected exposure to an au-diovisual event. Yet, investigators have beenstymied in their study of surprise becauseit does not consistently occur in situationsthat adults imagine would surprise babies.A jack-in-the-box does not produce surpriseexpressions in a majority of babies, for ex-ample. Occasionally, surprise occurs in situ-ations where the experimenter did not an-ticipate observing it (Bennett, Bendersky, &Lewis, 2002; Camras, 1992). When surprisedoes occur, it appears briefly before resolv-ing into some other expression—either inter-est, smiling, or a negative expression. Mostresearchers accept that infants show at leastmild surprise expressions to novel events by 6months, and some may do so sooner (Bennettet al., 2002; Charlesworth & Kreutzer, 1973).But, there are wide individual differences inwhether babies display this expression evenwithin the standard laboratory situations, sug-gesting that surprise may occur only in themost emotionally reactive infants. Besides thesuddenness of the stimulus onset and its in-tensity, a key factor in surprise seems to bewhether the stimulus event was expected. Forinstance, infants who learned that pulling astring turned on a slide with music expressedsurprise at this contingent event only whenfirst learning this response. Once learninghad occurred, surprise expressions were nolonger observed, suggesting that the infantsnow expected something when they pulled(Sullivan & Lewis, 1989). Surprise expressionsin very young infants also appear to growmore intense across the first several repeated,sudden stimulus presentations. This is lesscharacteristic of surprise in adults, who if sur-prised by a stimulus more than once, rapidlyshow an attenuated response.

Like interest expressions, informationabout surprise expressions is lacking for

various populations of infants and childrenlikely to be seen in clinical practice. Given itsrelation to arousal modulation in response tounexpected events and its tendency to habit-uate with familiarization, information aboutsurprise expressions in various groups is ofconsiderable interest in assessing children’semotion regulation and emerging cognitiveskills.

ENJOYMENT

Because they are so readily recognized andsuch widely acknowledged milestones of so-cial behavior, smiling and laughter, the 2major facial expressions of enjoyment, havebeen the most intensely studied expressionsin infants. Their developmental trajectoryand links to cognitive processing in infantshave been extremely well documented infull-term and preterm infants, as well as ininfants with Down Syndrome, autism, andblindness (Calhoun & Kuczera, 1996; Carvajal& Iglesias, 1997; Cicchetti & Sroufe, 1978;Kasari, Mundy, et al, 1990; Kasari, Sigman,et al., 1992; McCall, 1972; Sroufe & Waters,1976; Sroufe & Wunsch, 1972; Vine, 1973).While smiling appears universally, culturaland environmental differences also have beendescribed (Camras et al., 1998; Gerwirtz,1965; Kisilevsky, et al., 1998). Some have ar-gued that additional enjoyment forms are de-tectable in older infants (Fogel et al., 2000;Scanlon-Jones et al., 1990). In fact, the de-velopmental course of enjoyment provides amodel for comparison with the developmentof other expressions, although not all expres-sions will follow enjoyment’s pattern.

Smiling, like interest, is present from theopening days of life and is state-dependentduring the neonatal period. Unlike the inter-est expressions, which presume an awake,alert infant, the first signals of enjoyment ap-pear during the newborn’s sleep. Even at thisearly stage, newborn smiles include the 2most recognizable components of this expres-sion: narrowed eyes, widened mouth, withcorners raised. These same features consis-tently appear in the smiles of older infants(see Fig 3a–c), although later smiles are more

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Fig 3. Four examples of enjoyment from 2- to 9-month-olds in various contexts. (a) Response to tactileteasing at 8 weeks, (b) response to audiovisual contingency at 4.5 months, (c) response to play in an olderinfant, and (d) response to audiovisual contingency in an older infant with Down syndrome.

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intense and may include other components.Originally thought to be related to digestion(older literature may refer to them as “vegeta-tive”or “gas” smiles), sleepy smiles are proba-bly related to the discharge of pleasant stimu-lation of some kind by the infant’s immaturecentral nervous system (CNS) during rapideye movement sleep. The source of this stim-ulation need not be internal, but can be linkedto the external environment through what-ever attention and perceptual processing sys-tems are functional at birth. For example, oneof the author’s newborn daughter slept in aroom with a musical, chiming clock on herfirst day at home from the hospital. Two dayslater, when she was again sleeping nearby, theclock chimes elicited smiling. This incidentin a healthy newborn shows that the CNS isprimed to recognize familiar external auditoryinformation and to signal this recognition toothers. Repetition alone may be enough topromote positive emotional responses to non-threatening stimulation through simple asso-ciative learning (Zajonc, 2001).

Between 6 and 8 weeks, smiles of en-joyment can be observed during waking toboth visual and auditory stimulation. Visualstimuli alone elicit smiling in young infantsbut must have a face-like quality. For ex-ample, a gently bobbing oval with 2 smallblack circles, suggesting the eyes of a hu-man face, are sufficient to make a 2- to 3-

Table 1. Variants of enjoyment

MAX/AFFEXFacial actions codes Context

Closed-mouth, simple smile 0-0-52 CL Social and Toy play (Scalon-Jones, Raag,(ie, grin) & Collins, 1990)

Enjoyment Readiness to engage, peekaboo game (Fogel,Nelson-Jones, & Hsu, 2002)

“Duchenne” smile (with 0-33-52 Social interactiona (Fogel et al., 2000;cheek raise/eye crinkle) Scalon-Jones et al., 1990)

Enjoyment Play with mother, tickle game (Fogel et al., 2002)Bared-teeth play or 0-0-52/50∗ Social and Toy play (Scalon-Jones et al., 1990)

open-mouth Enjoyment Social Play (Scalon-Jones et al., 1990)Duplay (play + cheek 0-33-52/50 Game resolution, peek-a-boo and

raise/eye crinkle) Enjoyment tickle (Fogel et al., 2000)

∗The combination of codes 52/50 can be used to designate a smile with jaw drop.

month-old smile (Ambrose, 1963; Vine, 1973).Figure 3a shows that gentle tactile stimula-tion also successfully elicits enjoyment in an8-week-old. Such demonstrations show thatexpressions of enjoyment in early life areclosely tied to the physical quality of stimula-tion, which can be auditory, tactile, or visual,but is usually multisensory in quality. Verysoon, however, enjoyment begins to occur tosocial events.

Expressions of enjoyment to social stimula-tion increase dramatically by 16 weeks. Socialsmiling peaks between 12–14 weeks of agein home-reared infants in Western culture. In-fants at this age clearly seem to enjoy peopleand will smile readily at most adults who in-teract pleasantly with them. After 16 weeks,however, many infants become more discrim-inating about whom they will smile for. Thefamiliarity and the behavioral style of the in-teractive partner become important factors.In this way, an emotional signal provides anindex of the infant’s growing social-cognitivedevelopment.

In 12- to 17- month-old infants, variantsof social smiling have been described (Fogelet al., 2000; Scanlon-Jones et al., 1990). Theseappear to signal somewhat different quali-ties of enjoyment within social situations butmore work is needed to determine if theyare actually different expressions or just dif-fering intensities of enjoyment (see Table 1).

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None are treated as unique emotions inMAX/AFFEX, but are simply coded as enjoy-ment. All of these expressions were more fre-quent during interaction with mother thanwith toys. The play face, however, has specialmeaning.

The laughing or play face

Wide-open mouthed, gaping enjoyment ex-pressions occur with characteristic vocaliza-tions known as laughter. In intense forms ofthis expression, the lips may be rolled in-ward as the jaw gapes. Either form signalshigh excitement and positive arousal. Such ex-pressions haven been called “play face” be-cause they appear to be the human equiv-alent of a primate expression of the samequality (Blurton-Jones, 1972; Preuschoft & vanHoof, 1997). The play face makes its appear-ance by 5 months of age in normally devel-oping infants (Sroufe & Waters, 1976). It oc-curs at first to vigorous, auditory, and tactilestimulation, ie, tickling as did smiling a fewweeks previously. After 7 months, visual stim-ulation becomes more effective in elicitingthis expression. By about 12 months, incon-gruity and novelty, especially if it involves theinfant’s own participation, will elicit laugh-ter and the play face, immediately or in an-ticipation of game-like interaction with a so-cial partner, such as peek-a-boo (Fogel et al.,2000).

Enjoyment of mastery

During the second half of the first year, in-fants continue to smile and laugh at nonsocialevents but infrequently compared to socialsituations. Smiling occurs in nonsocial con-texts especially when infants learn that inter-esting, familiar, and therefore, nonthreaten-ing stimulation is under their own control.Figure 3b shows a 4-month-old expressing en-joyment of a slide and music that she haslearned to expect when she tugs a ribbonattached to her wrist (Lewis et al., 1990;Sullivan & Lewis, 1989). This is the beginningof playful enjoyment of mastery of the physi-cal environment that will continue to developas infants learn to play and explore. Compar-

ing this expression to one of the 9-month-oldat play with something novel (Fig 3c), one cansee that the crinkled eyes, widened mouth,and raised, dimpled cheeks are very similar,despite the fact that motor and cognitive skillshave grown considerably in the intervening5 months. Thus, it seems that the form ofthe enjoyment expression does not change,only the contexts and qualities of stimula-tion required to elicit it. Enjoyment of mas-tery of an object or task becomes especiallycommon after 12 months and has been stud-ied as one measure of “mastery motivation”(Busch-Rossnagel, 1997). Once the infant iscapable of self-referential and self-evaluativebehavior, the integration of enjoyment ofmastery and postural and gestural signalswill lead to more elaborated expressions ofpride.

Because of the connection of enjoymentwith management of arousal and emergingcognitive competencies, smiling and laughterhave been the most studied expressions of in-fants and children with disabilities. Much isknown, for example, about the emergence ofenjoyment in infants with Down syndrome(DS) (DS; Cicchetti & Sroufe, 1978; Sroufe &Wunsch, 1972). As can be seen in Fig 3d, thecharacteristic expressive components of mas-tery enjoyment are present in this 8-month-old child. Research shows that the generalcourse of both smiling and the play face isthe same in infants with DS, although delayedcompared to infants without this syndrome.For example, social smiling peaks at thesame mental age (ie, 4–5 months) and smilesare directed appropriately to social partners(Carvajal & Iglesias, 1997). The intensity ofenjoyment is less, however, and infants withDS may not sustain social enjoyment in spon-taneous interaction to the same degree as doinfants without the syndrome and may be lesslikely to initiate smiling (Carvajal & Iglesias,2000; Kasari & Sigman, 1996). Such differ-ences can have important effects on socialinteraction. Smiling to auditory stimulationalso may be more limited in some childrenwith DS, but can be increased with interven-tion (Calhoun & Kuczera, 1996). In fact, by

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preschool age, children with DS are usuallyreported to be highly positive in their socialinteractions. One study finds however thatthey are uniformly high in expression enjoy-ment across situations whereas MA-matchedpeers displayed more enjoyment only in thosesituations involving joint attention and affectsharing (Kasari, Mundy, et al., 1990; Kasari,Sigman, et al., 1992). Thus the child withDS seems to display enjoyment more indis-criminately, suggesting a need to focus onemotion regulation in some contexts. Finally,enjoyment of mastery may be affected insome children with DS because motor lim-itations restrict early forms of object play,but this also can be improved by interven-tion (Brinker & Lewis, 1982; Sullivan & Lewis,1990).

In severe cerebral palsy (CP), enjoyment ex-pressions, especially in the mouth region, maybe less well modulated or appear asymmetri-cal. If motor impairment is severe, the playface may be the only form of smiling availableto these children because subcortical centersmodulating enjoyment are activated.

The course of smiling in blind children alsohas been studied to understand the degreeof visual input that is necessary to producerecognizable expressions of happiness. Visualinput does not appear to be necessary forblind children to produce recognizable, spon-taneous expressions of enjoyment. Instead, itis their negative expressions that are moredifficult to recognize compared to those ofsighted children (Galati, Sini, Tinit, & Miceli,2001). However, blind children may be lessskillful at management of social expressions,contributing to the social inhibition that is fre-quently reported in these children (Castanho& Otta, 1999). Lower rates and poorer qual-ity of enjoyment expressions may prompt theperception of inhibition in children with dis-abilities generally.

Enjoyment expressions in autistic childrenhave been studied around the issue of sharedaffect between child and adult partners. Lessenjoyment is expressed by these childrenwhen compared with MA-matched controlsin semistructured interactions. Autistic chil-

dren also fail to share enjoyment with socialpartners by coordinating their enjoymentexpressions with eye contact (Dawsonet al., 1990; Sigman et al., 1992). During toyplay, autistic children are as likely to expressenjoyment, a finding that underscores thenonsocial nature of their expressions (Sigmanet al, 1992). Finally, autistic childrenare likely to display incongruous blendsexpressions that combine positive and nega-tive facial elements (Yirmiya et al., 1989). Itis unclear if this occurs because of problemsin regulating expressions themselves, or be-cause of ambivalent or competing emotionalarousal in these children. However, incongru-ous expressions provide unclear, conflictingsignals to caregivers who rely much oncontext or trial and error in responding tothem.

PHYSICAL PAIN

Some argue that pain is not an emotion.Yet, painful stimulation clearly causes a strongnegative emotional response and promotesother negative expressions. The developmen-tal course of pain expression has been stud-ied in some detail because of its theoreticalinterest and the very practical need for as-sessment and management of pain in pedi-atric procedures (Grunau, Oberlander, Holsti,& Whitfield, 1998; Oberlander, 2001). Painexpressions can be also observed in situa-tions of distress that are not physically painful(Oster, Hegley, & Nagel, 1992). Thus, the painexpression and those that follow it provideclues to emotional and regulatory responsesto all forms of aversive stimulation.

Acute pain in response to tissue damageduring standard pediatric procedures (eg, cir-cumcision, heel lance, or inoculation) pro-vides a naturalistic and ethical way to observehow facially and behaviorally expressed painresponses change with the developmentaland neurological status of the infant. Pain inresponse to such procedures is signaled bydistinctive and intense facial actions includ-ing the drawing together and lowering of thebrows to create a midbrow bulge, a deepened

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Fig 4. Pain in response to DPT inoculation in 4-month-olds showing (a) cupped tongue and (b) lateralretraction of the mouth.

nasolabial furrow, and tight squeezing ofthe eye orbit muscles, resulting in a strongsquint. From the newborn period through 18months, few changes occur in the pain ex-pression’s appearance or components (Craig,1992; Craig & Grunau, 1993; Izard, Hem-bree, Dougherty, & Spizziri, 1983; Johnston,Stevens, Craig, & Granan, 1993; Lilley, Craig,& Grunau,1997). Throughout this time, the fa-cial response to acute pain reliably includesall of the upper face movements listed. Mouthmovements are more variable but include lat-eral stretching of lips, especially in older in-fants and children. In young infants, one oftwo common mouth variations can be ob-served. Prominent especially in newborns isa dropped jaw with taut or ”cupped” tonguewithin an angular, wide mouth (see Fig 4a;Lilley et al., 1997). From 1 to 5 years, thesefacial movements cohere to form pain expres-sions in pediatric patients. A greater numberof components shown is related to higherpain ratings by clinicians (Gilbert et al., 1999).The laterally stretched mouth also occurs

commonly at these ages (see Fig 4b). Sincefew longitudinal investigations of pain havefollowed infants’ pain expressions from thenewborn period, the meaning of these vari-ations and age changes in the mouth compo-nents of pain are unknown. We do not know ifthey reflect individual differences in pain sen-sitivity or in regulatory responses to pain.

Surprisingly, increased crying in pretermsand newborns is not a reliable marker forpain in response to a heel lance (Grunau& Craig, 1987). Young babies vary in theirirritability and many will cry in responseto handling prior to the actual procedure(Grunau, Johnston, & Craig, 1990; Owens& Todt, 1985). Very low birth weight pre-mature infants between 26–31 weeks gesta-tional age, show the upper face pain actionswhen their heels are lanced to obtain blood.The upper facial response is specific to thepiercing of the skin, rather than other po-tentially stressful aspects of handling that oc-cur as part of the medical procedure, and isaccompanied by the maximum increase in

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heart rate. Noxious stimulation and the highnegative arousal they produce appear to si-multaneously activate many different nega-tively toned neurological systems in the youngbaby. Pain expressions are associated with arise in cortisol levels in newborns, also sug-gesting that heel lancing is a highly stressfulprocedure for the young baby (Oberlander,Gilbert, Chambers, O’Donnell, & Craig, 1999;Owens & Todt, 1985; Ramsay & Lewis, 1994).The pain expression and its accompanyingphysiological response are related to the de-velopmental age of the preterms, appearingmore consistent and robust in older babies(Johnston, Stevens, Yang, & Horton, 1995).It is unclear if this age change reflects bet-ter neurological regulation of the pain re-sponse, or the gradual recovery from illnessand trauma experienced by many of these sickbabies.

Although the expression of pain appearsrelatively invariant over the first 2 years oflife, a number of important changes occurthat possibly reflect a combination of neuro-physiological maturation, life experience, anda growing ability to remember prior painfulexperiences. In contrast to newborns, in2-month-olds, the expressive components ofpain occur at low frequency during a preinoc-ulation or baseline period. This observationsuggests that pain expressions, occurring asnonspecific generalized distress reactions tohandling, decrease with age. However, be-cause a significant and dramatic increase inall pain components is observed in responseto inoculation, infants’ pain response showssome specificity to skin trauma at every agestudied (Lilley et al., 1997). Healthy term in-fants between 2 and 4 months of age havethe most robust response to pain (Lewis &Thomas, 1990; Maikler, 1991). By 4 months,pain expressions are highly specific to in-oculation, with very few pain signals occur-ring during the baseline period. Likewise,4 month-olds have quicker recovery frompain (Lilley et al., 1997; Lewis & Thomas,1990; Ramsay & Lewis, 1994), suggestingthat CNS mechanisms inhibiting the trans-

mission of pain become functional at thisage. Following this important transition point,6-month-olds show a shorter duration of painresponse and less of a rise in cortisol in re-sponse to immunizations, suggesting betterinternal physiological regulation in responseto pain (Lewis & Thomas, 1990; Ramsay &Lewis, 1994).

Although the appearance of the pain ex-pression may change little with age, older in-fants have more complex responses to pain.Typically, they display facial pain for a smallerproportion of time prior to quieting, dis-playing anger and blended expressions in-stead (Izard et al., 1983; Izard, Hembree,& Heubner, 1987). By 18 months, pain-specific expressions comprised only 10% ofthe postinoculation distress (Izard et al.,1987). Thus, anger and other negative ex-pressions become rapid after-reactions to theinitial pain response. This pain after-reactionis most likely to influence the appropri-ate soothing strategy and might also be sta-ble across individuals. For example, thesepostpain facial signals likely reflect somecombination of differences in pain sensitiv-ity and social experience among individuals.For, example, Japanese infants seem to haveless pain sensitivity and qualitatively differentemotional responses to inoculation than doAmerican infants; pain expressions are lessintense and are not typically followed byanger and crying, but by surprise (Lewis,Ramsay, & Kawakami, 1993). Differences be-tween Chinese infants and other groups areeven more pronounced for a variety of expres-sions (Camras et al., 1998).

Greater behavioral coordination and mat-uration of motor skills also lead to elabora-tion of responses to pain in older infants.Infants over 12 months of age are morelikely to show goal-focused behaviors fol-lowing immunizations (withdrawing, avoid-ing), compared to younger infants who dis-play more unorganized distress responses(Craig & Grunau, 1993). Between 12 and 18months, pain responses become anticipatory.Lilley et al (1997) reported that baseline

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pain expressions were low between 4 and12 months, but rose again between 12 and18 months to a level similar to that of 2-month-olds! These differences in the baseline or pre-inoculation period suggest that the older in-fants anticipated the painful procedures instore for them. If so, pediatricians may be-gin to encounter anticipatory emotional re-sponses to pain, cued by the environmentand salient memories of prior procedures by12 months, perhaps even earlier. Collectively,these changes suggest that the pain expres-sion is stable over the first 2 years of life andthere is a close link between facially signaledpain and neurophysiological development.

Significant neurological impairment ap-pears to dampen the pain response, but thebasis for dampened or atypical pain responsesis unclear (Oberlander et al., 1999). Signif-icant neurological, motor, and/or cognitiveimpairment can produce a decreased painresponse for any number of reasons, lead-ing to underrecognition and poor manage-ment of pain in children with disabilities orneurological impairment. The developmentof expression-based pain scales for pediatricpractice is a relatively recent application di-rected toward addressing this problem anddiscovering methods to assess pain based onfacial responses (Oberlander, 2001). Hope-fully, better quantification of pain will lead tobetter recognition and effective management.

DISGUST AND ITS VARIANTS

The disgust expression is another that hasbeen studied in some detail in newborns. Thenewborn’s response to bitter and sour sub-stances is distinct from responses to waterand sweet solutions (Granchow, Steiner, &Daher, 1983; Rosenstein & Oster, 1988;Steiner, 1979). Saltiness does not trigger dis-gust expressions, with less than half of in-fants showing any negative response to it(Rosenstein & Oster, 1988). However, quinineand other bitter tastes are potent and rapidelicitors of disgust responses regardless of in-fant state. The intensity of the disgust expres-sions as well as the pattern of components

expressed appear to index increasing concen-trations of the solutions presented (Granchowet al., 1983; Rosenstein & Oster, 1988; Steiner,1979). The response to a bitter taste typicallyinvolves turning away from the source of thestimulus and gaping of the mouth and lowerlip, as shown in Fig 5a. Sometimes, the gagreflex is observed (Steiner, 1979). Nose wrin-kling and upper lip raising are components ofthe full disgust reaction, but occur alone asobserved in about half of the newborns as aless intense form of the reaction (Rosenstein& Oster, 1988). A flattened tongue and drool-ing may also be visible, depending on the stateof the child and the concentration of the fluid(Steiner, 1979). These responses signal strongdistaste on the part of the infant. They are adefensive reflex helping the infant to rid itselfof the unappealing taste. Similar responses areobserved to odors that most adults would findobjectionable, such as fishy and “rotten egg”smells (Steiner, 1979).

Responses to a sour taste, such as citricacid solution, are more variable, seem to bemilder, and evolve over several seconds incontrast to disgust. Lip pursing is the com-monly observed initial response, accompa-nied by nose wrinkling, narrowed eyes, andblinking (Rosenstein & Oster, 1988; Steiner,1979). Figure 5b shows this response in a 4-month-old. A closed mouth, either with cor-ners down or retracted lips, is a feature as-sociated with milder aversive reactions. This“sour grimace,” signaling dislike, occurs as theresponse develops (Granchow et al., 1983;Steiner, 1979).

The variability of sour expressions in re-sponse to sour tastes is even more pro-nounced in 4-month-olds than in newborns.The most common response to a naturalsour taste (lemon juice) at this age is in-terest, following the initial puckering andrapid lip movements associated with tastingor mouthing of the flavor. In some infants,however, negative expressions indicating dis-like (sad frown or lip retraction movements)appear, as observed in newborns (see Fig 5c).However, a few infants actually smile, the nextmost common response to this taste (Bennett,

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Fig 5. Disgust (a) and sour (b, c) responses of 4-month-old infants elicited by a lemon juice swab.

et al, 2000). This finding shows that early in-dividual differences in taste preferences andrapid resolution of initial mild disgust reac-tions into either enjoyment or dislike emergeearly in life.

The developmental course of the disgustfamily of expressions has not been tracedfurther, but it appears that the disgust re-sponse is so well-developed in infants andspecific to both the quality of olfactory andgustatory stimulation, that its form changeslittle. Steiner (1979) undertook extensivestudy of disgust and enjoyment taste re-actions in various populations of infantsand children with various forms of disabil-ity, including newborns with hydrocephaly,

anencephaly, the congenitally blind, childrenwith craniofacial malformations, and mentallyretarded adults. Disgust and sour grimace ex-pressions were recognizable in all popula-tions studied, despite the considerable vari-ation in the cognitive and motor control(Steiner, 1979). He argued that the preser-vation of disgust responses across this widerange of cognitive and motor functioningmeans that disgust expressions are controlledby the brainstem and so undergoes little mor-phological change. However, the emergenceof the positive or negative reactions to souralso points to 4 months as an importantdevelopmental milestone in organization ofexpressions.

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Perhaps the most interesting aspect of dis-gust expressions, and the one about whichlittle is known, is how the subtle variationsin responsiveness observed even in newbornsare related to individual differences in ner-vous system functioning or other factors, suchas temperament. A second unanswered ques-tion is when these expressions begin to occurin response to non-taste stimuli, and espe-cially social stimulation. Like smiling, dis-gust expressions are elicited initially to phys-ical rather than social-psychological elicitors.Non-taste stimuli that might be sufficient toproduce disgust in infants have not yet beenreported, but can be imagined. Disgust sig-nals stimulus rejection. Therefore, too rapidor sudden occurrence of a stimulus mightelicit disgust expressions if the stimulus over-whelms infants’ ability to process it. We haveobserved this on some occasions in the infantlearning lab: sometimes an infant pulls suffi-ciently rapidly that the slide and music ap-pears within a second of its previous appear-ance and before the infant’s reaction to thefirst appearance has subsided. When this oc-curs, the infant may display nose wrinkling, orasymmetrical mouth and lip movements in re-sponse, suggesting a kind of recoil reaction tothe overwhelming, too rapid reoccurrence ofthe stimulus. While clearly not yet an instanceof “psychological disgust,” such observationssuggest that prior to 6 months of age, compo-nents of disgust may occur in response to vi-sual and auditory stimulation, setting the stagefor their later function in social situations.But, the forms of disgust observed in this casedo not involve the intense, gaping reactionsobserved in response to bitter tastes.

Toilet training and introduction of solidfoods when the child is able to eat inde-pendently are thought to be important con-texts for parent-child socialization of disgust(Rozen, Hadt, & McCauley, 2000). It is alsopossible that disgust, signaling stimulus rejec-tion, is more common in neurologically dam-aged infants and children in whom inhibitorycontrol is slow to develop or absent. This re-sponse would be an important clue to care-givers to reduce the intensity or pacing ofstimulation.

ANGER OR ‘‘CRY FACE” EXPRESSIONS

The prototypic anger or cry face appearsin Fig 6a. It is characterized by brows drawntogether and lowered, sometimes strongly asseen in this view. Deep nasolabial folds framea wide-opened square mouth. Anger expres-sions of this intensity are almost always ac-companied by a rolling cry in infants, butmilder versions are observed without any vo-calization. This expression is the infant’s mostcommon negative expression.

A major quandary for theorists is that theanger/cry face rarely occurs in young infantswithout the co-occurrence of other negativeexpressions or blends. Blended anger and sad-ness, as seen in Fig 5b, is commonly seen. Inthis expression, knit, lowered brows and nar-rowed eyes of the upper face region are ac-companied by a sad ”pout” in the lower face.This particular blend (upper face anger withlower face sadness) is often observed duringsocial interaction with the mother and it tendsto decrease with age in this setting (Izardet al., 1995). This might not be so in all situa-tions that recruit anger expressions, but moreinformation is needed. The co-occurrence ofmultiple negative and blended expressionswith the anger/cry face has led some to arguethat these negative expressions collectively re-flect general distress or unhappiness insteadof a specific facial signal of anger or othernegative emotions (Camras, 1992). However,the co-occurrence of multiple negative ex-pressions in the early months can also beexplained by the well-known quality of theCNS to respond more intensely to negativethan to positive stimuli (Peters & Czapinski,1990). Although the CNS idles in a mildly pos-itive mode (positivity offset), when a threaten-ing stimulus is encountered, a vigorous nega-tive response is observed. This phenomenon,known as the negativity bias, may be espe-cially evident in young infants, in whom in-hibitory control is still limited and arousal ispoorly regulated. The negativity bias couldresult in an initially unmodulated negativeresponse that simultaneously activates severalcompeting systems when an aversive eventis initially perceived. It is not that there is

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Fig 6. Anger (a) and upper face anger blended with sad (b) expressions in 5-month-olds.

one “undifferentiated” distress state, but thatall negative emotion systems are primed. Thestrongest response tendency is an energiz-ing response to action in order to resist orovercome the aversive stimulus. It is signaledby increased motor activity and crying aswell as by the prototypical anger or cry faceexpressions.

Although anger expressions may not ap-pear exclusively when infants encounter cer-tain types of negative events, by 3–4 monthsof age, a number of situations seem to re-sult in anger expressions predominantly. Re-straining an infant’s arms, for example, pro-duces a variety of facial expressions, notall of them negative. Anger, however, is thepredominant negative expression (Bennettet al., 2002; Braungart-Reiker & Stifter, 1996;Stenberg, Campos, & Emde, 1983; but seeCamras et al., 1998, regarding ethnic differ-ences). An even more powerful example isthe response of infants to loss of a contingentevent (Lewis et al, 1990; Sullivan, Lewis, &Alessandri, 1992). Infants who learn to con-trol a pleasant event by pulling a ribbon showanger expressions and increase pulling when

that action abruptly fails to produce the event.Anger expressions increase, but other nega-tive expressions do not. The increase is there-fore specific to infants’ having learned a re-lation between action and outcome (Lewiset al., 1990; Sullivan & Lewis, in press). Situa-tions that produce anger expressions before6 months of age are those in which ac-cess to desired objects or goals is blockedor thwarted in some way (Bennett et al.,2002; Lewis et al., 1990; Stenberg et al., 1983;Sullivan et al, 1992) or, those causing pain af-ter about 4 months (Izard et al., 1983). Thereis stability in individuals’ expressions of angerin these contexts as well (Izard et al., 1995;Sullivan et al, 1992).

Crying and fussing are widely recognizedvocal signals of negative emotion in infants,but no any one quality of crying appearsto be specific to the “cry face” or to anyother negative expression. Negative facialexpressions can precede negative vocal be-havior, suggesting that greater or increas-ing arousal is needed for vocal crying. Criescan be differentiated by frequency and tonalquality but it is difficult for observers to

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discriminate these features reliably and expe-rience is an important factor when differen-tiating vocal crying in the mild to moderaterange (Papousek, 1989). Facial expressionsprobably provide more graded informationabout the onset, quality, and intensity of neg-ative reactivity, making such discriminationspossible.

The form, development, and regulation ofanger expressions and their relation to vo-cal crying in atypical development has notbeen addressed in any significant detail. Likesmiling, negative vocalizations undergo an im-portant developmental transition in the first4 months (Hopkins, 2001). Presumably thischange parallels changes in the patterningof anger and other negative expressions, al-though this has not been studied. Much avail-able work has focused on the clinical utilityof vocal cry behavior and unexplained infantirritability (Barr, Hopkins, & Green, 2000). Be-cause adults rely on vocal and facial informa-tion before correctly identifying that infantsare indeed upset (Greene & Gustafson, 2001),the lack of information about the coordinationof expression and voice in the development oftypical and atypical children is frustrating. Dis-

Fig 7. Sad expressions without (a) and with (b) lower lip protrusion in infants under 6 months of age.

abling conditions significantly affect adult per-ceptions of young children. For example, in-fants and children with DS are reportedly lessirritable than the norm and those with CP andauditory and visual handicaps even more so(Field, 1996). Autistic children are also some-times found to be more negative (Yirmiyaet al., 1989). Greater attention to the quality ofexpressive behavior of children with disabil-ities might provide more clinically useful in-formation and suggest possible interventions.Given their physical limitations, it is reason-able to expect greater frustration on the partof these children. Whether it is expressed asanger, other negative expressions, or undiffer-entiated distress is not known

SAD OR ‘‘POUT FACE” EXPRESSIONS

Figure 7a shows the sad frown or “poutface” expression. The brows are raised and an-gular in appearance over narrowed eyes. Thenasolabial folds appear prominent, as theydo in all negative expressions. The mouthcorners are down-turned in a “horseshoe”shape (Oster, 1978). The chin is raised, some-times prominently as in Fig 7b. The latter

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movement, especially when combined withforward projection of the lower lip, as inFig 7b, gives it the pouting quality. In bothexamples of this expression, the mouth isclosed, although open-mouthed sad pouts arealso possible. Sad pouts are equally likely toappear as an upper face signal or as a full ex-pression in young infants (Izard et al., 1995;Sullivan & Lewis, in press). When blendedwith another expression, sad brows are espe-cially likely to combine with anger or, less of-ten, with interest in the lower face. In eithercase, such blends are interpreted as a signal ofdislike or unhappiness.

Sad pouts have never been observed tobe specific to any stimulus or context. Forthis reason, little is known about them. Theyare not a dominant negative expression inany context that has been studied, except forpouts associated with the after-sour response(Bennett et al., 2002). Sad pouts occur at rela-tively low but stable levels during both socialinteraction and learning/frustration episodes(Izard et al., 1995; Sullivan et al., 1992).Some have suggested that this expressionoccurs as an infant or young child eitherarouses to an anger expression or as a reg-ulatory movement inhibiting anger (Camras,1992; Oster, 1978). It is possible that sadexpressions are never completely indepen-dent of anger expressions even in adults(Barr-Zisowitz, 2000). Caregiver interventionin response to sad expressions may forestallor more effectively help dampen more in-tense negative response, but this has not beendemonstrated.

FEAR EXPRESSIONS

Fear expressions are notoriously difficultto observe in infants. In adults and children,this expression involves raised and straight-ened brows, widened eyes with tense lowereyelids, and horizontally retracted lips. Lessintense versions feature brow movementsalone, possibly blended with interest or otherfacial movements in the lower face, such asanger or sadness. Situations that could con-ceivably frighten infants (eg, a visual cliff, the

approach of a stranger, highly novel masks,and startling mechanical toys) do not elicitfear expressions (Bennett et al., 2002; Camras,1992; Izard et al., 1995; Lewis & Michalson,1983). Therefore, some suggest that infantsmay not be able to display fear until some-time after 7–12 months because greater expe-rience and cognitive abilities are needed forappraisal of strange and dangerous environ-mental events (Izard & Malatesta, 1987). Bothindependent locomotion and ability to inhibitbehavior may also be prerequisites of fear. Forexample, wariness of strangers, a mild form offear, is not observed in a majority of childrenuntil after 7 months of age (Bronson, 1972).By 11 months, the brow components of feardo occur to a variety of aversive stimuli, butare not specific to fear-inducing toys, such asa growling mechanical gorilla (Camras et al.,1998). Fear systems in the brain do have ahigh degree of plasticity (LeDoux & Phelps,2000), supporting the view that learning andexperience are very important to this emo-tion. The question remains how little experi-ence is needed for fear expressions to occur.Figure 8a shows the response of a 6-month-old infant to the return of a nurse for thesecond of 2 inoculations administered at thiswell-child visit. This observation suggests thata single salient experience may be suffi-cient. By 2 years of age, fear can be rapidlylearned, resulting in phobic reactions thatmay spread readily to previously nonfearedobjects through learning (Watson & Rayner,1920).

Even in young infants, fear blends are ob-served on occasion in situations that are aver-sive. For example, fear blends occurred in8% of infants in response to arm restraint(Camras, Oster, Campos, Miyake, & Bradshaw,1997). This raises the possibility that moststimulus situations studied thus far are notadequate to elicit fear expressions and thatblends are observed because milder stimula-tion results in less intense reactions. As withdisgust, very specific and intense stimulationmay be necessary to elicit fear expressions.Looming objects, very loud sounds, and theloss of support are good candidates. However,

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Fig 8. A fear expression in response to approach of a nurse following inoculation (a) and a fear blend inresponse to the sudden appearance of a stimulus (b).

some of these are impossible to study exper-imentally because of ethical considerations.Alternatively, aversive situations may producefear only in the most temperamentally fearfulchildren. In our studies of infant condition-ing, fear blends appear as negatively toned sur-prise expressions (see Fig 7b). These surprise-fear blends appear early in the conditioningsession, before infants realize that their ownmovements cause the sudden onset of slidesand music. While most infants are surprisedand interested in these first appearances ofslides and music, others show surprise reac-tions that grow more extreme across severalpresentations, ultimately developing a nega-tive quality including fear components (browstraightening, tensed lower eyelid, and/or lat-eral movement of the mouth corners). In mostcases, fear-surprise responses subside quicklyas infants learn the relation between theirown movements and the slide’s appearance(Lewis, Sullivan, & Michalson, 1984; Sullivan& Lewis, 1989). But, some infants begin to

fuss and are unable to complete the proce-dure. These infants are reported by mothersto have more fearful temperaments (Sullivan,Ramsay, & Lewis, 1992). It seems reasonableto infer that infants with fearful temperamentsmay be expressing fear.

Because so few negative situations elicitfear and the percentage of children for whomfear expressions have been observed is solow (Bennett et al., 2002), the developmen-tal course of fear expressions has not beenstudied extensively. The dependence of fearon cognitive skills and appraisal of dangerin the environment may mean that mostinfants must learn to fear. Hence, fear ex-pressions will vary greatly across individ-uals. Some infants may express excessiveamounts of fear, either because neurologi-cal damage has interfered with the normalbuffering of the fear expression, or becauseprolonged experience with invasive medicalprocedures have resulted in conditioning offearfulness.

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SUMMARY

Despite differing approaches to measure-ment, considerable evidence shows thatcontext-appropriate emotion expressions oc-cur in infants and young children from birthor shortly thereafter. No matter what sys-tem is used, interest, enjoyment, anger, pain,and disgust have been shown to signal be-havioral dispositions congruent with theseemotions in young infants. This is also truefor fear and sad expressions in older infants.Pain, enjoyment, interest, and possibly angerand disgust show little change over the first2 years. Instead, the contexts that elicitthese emotions shift at several major transi-tions in cognitive development and cerebralmaturation, ie, 4 months, 7–9 months, and18–24 months. At these developmental ages,expressions can be particularly informativeabout the developmental status of children.At all ages, individual differences in expres-sive behavior can provide clues to children’spreferences and style of response. Althougha number of interesting and important ques-tions remain about expressive development,

it seems clear that facial expressions provideimportant information to caregivers and prac-titioners alike. Expressions, especially whencombined with vocal and postural behaviors,provide important clues to the motivationalstate of infants who cannot otherwise re-port what they feel. Ability to read the facialbehavior of children with disabilities givesparents an important tool for promoting posi-tive emotion, better management of their chil-dren’s negative behavior, and preventing frus-tration or helpless withdrawal of the parents.It is also clear that social environments havesubstantial influence on the emotional be-haviors of children with disabilities as well(Field, 1996), suggesting that well-designedinterventions may help parents who have dif-ficulty in understanding their children’s ex-pression become better attuned to subtle, in-congruous, or ambiguous signals. Awarenessof these expressions and their developmen-tal trajectories by the practitioner can as-sist in assigning meaning to infant behavior,skills that parents are especially concernedabout in day to day commerce with theirchildren.

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