واکنش سریع صورت به حالات احساسی صورت در کودکان برخوردار از رشدی عادی و کودکان با اختلال طیف اوتیسم

Abstract Typical adults mimic facial expressions within 1000 ms, but adults with autism spectrum disorder (ASD) do not. These rapid facial reactions (RFRs) are associated with the development of social–emotional abilities. Such interpersonal matching may be caused by motor mirroring or emotional responses. Using facial electromyography (EMG), this study evaluated mechanisms underlying RFRs during childhood and examined possible impairment in children with ASD. Experiment 1 found RFRs to happy and angry faces (not fear faces) in 15 typically developing children from 7 to 12 years of age. RFRs of fear (not anger) in response to angry faces indicated an emotional mechanism. In 11 children (8–13 years of age) with ASD, Experiment 2 found undifferentiated RFRs to fear expressions and no consistent RFRs to happy or angry faces. However, as children with ASD aged, matching RFRs to happy faces increased significantly, suggesting the development of processes underlying matching RFRs during this period in ASD.

Introduction Seeing a smiling face makes most people smile, and seeing an angry face can make them scowl (Bush et al., 1989, Dimberg, 1982, McIntosh, 2006 and McIntosh et al., 1994). The questions of why and how they do so have become increasingly important as our understanding of the role of interpersonal matching in development and social processes has expanded (Rogers & Williams, 2006). There is a wide variety of interpersonal matching behaviors, all of which include an observer engaging in behaviors similar to those of a model (Moody and McIntosh, 2006 and Williams et al., 2004). Some of the more complex behaviors, such as imitation, likely build on components of the most simple behaviors, such as automatic matching of emotional facial expressions (Moody and McIntosh, 2006 and Rogers, 1999). The current experiments examine these simple automatic facial responses in children. They are the first to demonstrate that facial electromyography (EMG) can be used to study these subtle and rapid responses in typically developing children and children with autism spectrum disorder (ASD). More important, Experiment 1 examines the mechanisms responsible for these rapid reactions, and Experiment 2 investigates these responses in children with ASD. Experiment 2 points toward the functional significance of these reactions and considers the development of matching in ASD. Rapid facial reactions Emotional facial mimicry is one type of rapid facial reaction (RFR). RFRs are commonly observed in adults after exposure to facial expressions. They occur very rapidly—within 1000 ms—and are often very subtle (Cacioppo et al., 1986 and Moody et al., 2007). Due to their speed and subtlety, investigators typically use EMG with surface electrodes placed over facial muscles to examine their occurrence. When an adult sees a picture of a happy facial expression, the muscles responsible for raising the cheek in a smile (zygomaticus major) typically show an increased level of activity; when an adult sees an angry expression, the muscles responsible for knitting the brows in a scowl (corrugator supercilii) may have greater activity (Dimberg, 1982, Dimberg, 1988 and Moody et al., 2007). These RFRs can occur even when people are exposed to facial expressions so quickly that they cannot consciously recognize the expressions (Dimberg et al., 2000 and Rotteveel et al., 2001). RFRs that match the observed expressions are associated with several important social and emotional abilities. In particular, matching of facial expressions has been theorized to be critical for social functioning, emotional contagion, empathy, and understanding of another person’s state of mind (Decéty and Chaminade, 2003, Hatfield et al., 1993, Hatfield et al., 1994, Iacoboni, 2005, Lakin and Chartrand, 2003, McIntosh, 2006, Scambler et al., 2007 and Sonnby-Borgstroem, 2002). In terms of evolution, expression matching may be adaptive because it helps humans to communicate and foster relationships (Lakin, Jefferis, Cheng, & Chartrand, 2003). Moreover, matching behaviors in general have important developmental functions such as facilitating social and emotional connectivity and understanding (Bavelas et al., 1987 and Masur and Rodemaker, 1999). Indeed, early RFRs may be important precursors to later, more complex imitative processes often studied in ASD. Therefore, it is important to understand RFRs and the role they play in interpersonal development and imitation. Although the presence of RFRs to emotional stimuli is well documented in adults (Dimberg, 1982, Dimberg, 1988 and McIntosh et al., 2006), there has been less work examining facial responses to facial expressions in children. Some studies suggest that newborns and infants less than 1 month of age match simple facial movements (Meltzoff & Moore, 1977) and emotional expressions (Field, Woodson, Greenberg, & Cohen, 1982), although the evidence is inconsistent (Anisfeld, 1996 and Kaitz et al., 1988). With development, there is more evidence of matching behaviors. Jones (2007) found that matching motor behaviors were not observed at 6 months of age but developed through the 2nd year of life. In addition, contagious yawning does not appear before 5 years of age, and the probability of occurrence continues to increase throughout childhood (Anderson & Meno, 2003). Evidence during toddlerhood for emotional responsiveness to others’ emotion displays was provided by Scambler and colleagues (2007). They studied emotional responsiveness to live adult displays of joy, fear, disgust, and pain among 2-year-olds with ASD, children with other developmental delays, and typically developing children. The children’s facial and behavioral responses were videotaped and coded for coordination in the valence of the emotion between child and experimenter. All groups showed some level of emotional responsivity, with children with ASD showing less. Facial responses to others’ emotions have also been demonstrated in preschoolers and second graders. Judges rated expressions on children’s faces to be highly congruent with the emotions displayed by children being viewed in films (Eisenberg et al., 1988). Despite the evidence indicating early matching and increases in matching with development, an important ambiguity remains. What causes the observed matching display? Among infants, the most consistently observed behavior (tongue protrusion) may be due not to motor matching or imitation but instead to arousal or exploration caused by the adult facial display (Anisfeld et al., 2001 and Jones, 1996). Moreover, there is also evidence for emotional contagion among infants. Newborns cry at the sound of other newborns crying (Martin and Clark, 1982 and Simner, 1971). At 10 to 14 months of age, infants orient to others’ distress, and some exhibit distress crying (Zahn-Waxler & Radke-Yarrow, 1982). Thus, any observed congruence of emotional facial responses may be due to shared emotion, not simple behavior matching. This analysis underscores the importance of careful examination of the mechanisms causing observed facial responses to others’ facial expressions. Among infants and older children, behaviors that match observed expressions might not be due to motor mimicry or simple imitation; instead, they might be due to other processes such as arousal, exploration, and emotional contagion. The specific mechanisms responsible for RFRs have only recently begun to be investigated (Moody et al., 2007). Indeed, recent investigations of the development of imitation during infancy suggest that the “origins of imitation” and the mechanisms producing mimicry and other matching behaviors “are almost entirely unknown and waiting to be described and explained” (Jones, 2007, p. 598). The current study advances the exploration of this category of behaviors by using EMG to examine mechanisms of children’s RFRs to others’ emotional facial expressions. This study builds on previous work that used visual coding of expressions (e.g., Eisenberg et al., 1988 and Scambler et al., 2007). By using EMG, which detects rapid and subtle expression changes, the current study facilitates examination of the initial responses to others’ facial displays and can track these changes over time. This allows us to establish the characteristics of rapid facial responses and explore the mechanisms that drive them. No work has used EMG to document whether the rapid reactions to emotional expressions seen in adults are evident in children or what mechanisms are responsible for RFRs from middle childhood through early adolescence. Such information is critical for understanding the development of RFRs and for understanding processes of typical and atypical social–emotional engagement during this phase of development. The current study specifically examines RFRs between 7 and 12 years of age because the development of the mechanisms underlying the response may be especially important during this time. This period is important in the development of perceiving and understanding other people’s emotions. During this time, children increasingly take others’ perspectives (Selman, 1976 and Selman and Byrne, 1974), increasingly respond empathically (Hoffman, 2000), and focus on peer interactions (Higgins & Parsons, 1983). The enhanced social focus of emotions in this age group suggests that mechanisms not available earlier in development may influence responses to others’ emotions. Examining the nature of RFRs during this age period is important because RFRs may play a role in fundamental interpersonal processes (Reed & McIntosh, 2008) and have significant functional consequences if disrupted (Moody & McIntosh, 2006). Possible underlying mechanisms of RFRs Although the presence of simple matching during infancy and of intentional imitation during toddlerhood suggests that matching behaviors are established by 7 years of age, their existence leaves open the question of the specific nature or mechanism of any matching observed. For example, when a 10-year-old sees a happy face, it seems likely (although not yet demonstrated) that he or she will automatically respond with happy RFRs. The underlying mechanism of such rapid responses has often been described as motor mimicry, but here we investigate whether there is another underlying mechanism. In fact, there are two theorized reasons or underlying mechanisms for these rapid responses: motor mimicry (the 10-year-old automatically matches the observed expression via a nonemotional process) and an emotional response (the observed smile evokes a happy emotion, so he or she displays a smile) (Moody et al., 2007). RFRs are often described as a direct, nonaffective motor matching reaction (Chartrand & Bargh, 1999), typically termed mimicry. This direct perception–action neural link may be viewed as bypassing emotional systems and being mediated by the mirror–neuron system ( Buccino et al., 2004, Niedenthal et al., 2005 and Williams et al., 2001). Such motor matching is one method through which people come to share others’ emotions ( Bavelas et al., 1987, Hatfield et al., 1993, Hatfield et al., 1994 and McIntosh et al., 1994). The second mechanism that may be involved in producing matching facial displays is an affective one. In contrast to motor mimicry generating emotion through facial feedback processes (McIntosh, 1996), a person’s initial response to the face may be an affective response. If the observer “catches” the emotion of the face, then a matching emotional display would be produced (Cacioppo et al., 1988, Dimberg, 1997 and Winkielman and Cacioppo, 2001). Emotional responses to others’ emotions are a plausible cause for matching RFRs because such emotional responsiveness occurs quite early in development (for a review, see Hatfield et al., 1994). Although emotional responses are often a catching or matching of the other’s emotion, the affective mechanisms might not always produce a matching response. An observer may respond with a nonmatching emotion. If this response occurred, then the RFRs would be complementary instead of matching. In support of the latter hypothesis that RFRs are tied to an emotional state stemming from the stimuli, recent work has found that RFRs do not always directly match the observed facial expression. Sometimes adults react to an angry face not by drawing their brows together in a matching scowl but instead by raising their eyebrows and expressing fear (Moody et al., 2007). This work underscores the point that the matching behaviors seen may be more than motor mimetic; they may reflect emotional responses that can be complementary to the observed emotional face. Because RFRs are likely critical to social–emotional development, it is important to understand what underlying processes are reflected by RFRs and whether they are the same in younger samples as in adults. The current study In Experiment 1, we examined RFRs to emotional facial expressions in typically developing children from 7 to 12 years of age. First, we investigated whether children show RFRs to such stimuli. The occurrence of RFRs in adults is robust; however, although we predict their existence during this age period, RFRs have not been documented or described in children of any age. If RFRs are building blocks to more complex imitation and other social–emotional skills evident in children and adults, then RFRs should be evident during childhood. Second, we investigated possible mechanisms responsible for RFRs. Specifically, we investigated whether the patterns of RFRs in children indicate that responses to the emotional facial expressions are consistent solely with motor mimicry or show emotional influences on the responses. To help delineate the two processes, we focused on RFRs to angry expressions because muscle activation representing fear to an angry face (i.e., increased medial frontalis activation) would suggest an emotional response. Finding emotional responses would support the interpretation that emotional influences (and not merely motor matching) on RFRs occur during this age period. Matching responses (increased corrugator activation) would be consistent with both motor matching and emotional responses. Experiment 2 builds on Experiment 1 by examining the existence, patterns, and mechanisms of RFRs in a sample of children with ASD. Examining RFRs in children with social–emotional deficits can help to uncover the extent to which RFRs are associated with typical development and social–emotional functioning. Together, the experiments involving typically developing children and children with ASD provide an examination of the presence of RFRs in development and the mechanisms underlying them.

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