RESEARCH ARTICLE An Evaluation of Imitation Recognition Abilities in Typically Developing Children and Young Children with Autism Spectrum Disorder Natalie I. Berger and Brooke Ingersoll Previous work has indicated that both typically developing children and children with Autism Spectrum Disorder (ASD) display a range of imitation recognition behaviors in response to a contingent adult imitator. However, it is unknown how the two groups perform comparatively on this construct. In this study, imitation recognition behaviors for children with ASD and typically developing children were observed during periods of contingent imitation imbedded in a naturalistic imitation task. Results from this study indicate that children with ASD are impaired in their ability to recognize being imitated relative to typically developing peers as demonstrated both by behaviors representing basic social attention and more mature imitation recognition. Display of imitation recognition behaviors was independent of length of contingent imitation period in typically developing children, but rate of engagement in imitation recognition behaviors was positively correlated with length of contingent imitation period in children with ASD. Exploratory findings also suggest a link between the ability to demonstrate recognition of being imitated and ASD symptom severity, language, and object imitation for young children with ASD. Autism Res 2015, 8: 442– C 2015 International Society for Autism Research, Wiley Periodicals, Inc. 453. V Keywords: autism; autism spectrum disorder; imitation; imitation recognition; social cognition

Background When faced with an imitative adult, typically developing infants between 2 and 8 months of age reliably demonstrate increases in social attention (e.g., look at what the experimenter is doing, increase eye contact, and smile more frequently) [Meltzoff & Moore, 1999; Nadel, 2002a; Nadel, Carchon, Kervella, Marcelli, & Reserbat-Plantey, 1999]. These behaviors have been conceptualized as early indicators of imitation recognition, in which the infant is implicitly conscious that she is being imitated but is not yet signaling explicit awareness of the intention behind the imitator’s behavior. Trevarthen and Hubley [1978] were one of the first to note this increase in social attention as a result of imitation in their examination of the use of imitation by mothers as a means for attracting and maintaining their infant’s attention. Similarly, Field [1977] reported increased infant gaze when the mother acted imitatively as opposed to engaging in other play behaviors. More recently, Nadel et al. [1999] has found that infants as young as 2 months old reliably respond to maternal imitation by increasing focal looks, smiles, and /or tonguing or vocalizing.

Similar behavior has been observed by multiple groups investigating imitation recognition outside of a natural maternal–child interaction [Agnetta & Rochat, 2004; Asendorpf, Warkentin, & Baudonnie`re, 1996; Eckerman & Stein, 1990; Meltzoff & Decety, 2003; Nadel, Revel, Andrey, & Gaussier, 2004]. These studies largely assess imitation recognition by having an infant sit opposite an adult who systematically imitates the infant’s actions and vocalizations. To control for the potential effects of watching an adult engaging in typical infant behavior and/or temporal contingency, some studies present the infant with two adults (live or via video monitors), one who imitates the child’s actions and vocalizations and one who either reacts contingently (but not imitatively) to the child’s actions or replicates the actions of a previously tested infant [e.g., Meltzoff, 1990]. In using both types of design with infants approximately 9–14 months of age, researchers have found that older infants also begin to engage in “testing behaviors” (i.e., systematically varying actions while closely watching their imitative partner) [Meltzoff, 1990; Nadel et al., 2004]. Infants engaging in this pattern of behavior are hypothesized to be checking whether the adult is intentionally imitating them, and

From the Department of Psychology, Michigan State University, Psychology Bldg., 316 Physics Rd. Room 69F, East Lansing, MI, 48824 (N.I.B, B.I) Received June 02, 2014; accepted for publication December 24, 2014 Address for correspondence and reprints: Natalie I. Berger, Department of Psychology, Michigan State University, 316 Physics Rd Room 69F, East Lansing, MI 48824. E-mail [email protected]. Published online 23 February 2015 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/aur.1462 C 2015 International Society for Autism Research, Wiley Periodicals, Inc. V

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it is considered to be the earliest evidence for imitation recognition over and above changes in social attention. To date, there is no clear demonstration of this more mature imitation awareness before about 9 months of age [Nadel et al., 2004]. Most recently, examination of imitation recognition outside of the infant–mother dyad has focused on identifying the neural correlates of imitation recognition. Saby, Marshall, and Meltzoff [2012] investigated the time course of electroencephalography (EEG) activity over infants’ execution of two different actions and during their observation of matching or nonmatching action, and found a reliable neural signal associated with the recognition that another is imitating the self. Overall, there is substantial evidence indicating that infants recognize when an interactive partner engages in contingent imitation. While a general developmental trajectory for the emergence of imitation recognition skills has been detailed by Nadel et al. [2004], it is much less clear the role these behaviors play in development overall. Across the literature, imitation recognition has been hypothesized to be differentially related to intention, imitation, joint attention, communication, and/or social reciprocity [Nadel, 2002b; Toth, Munson, Meltzoff, & Dawson, 2006]. These are the same skills considered necessary for the development of theory of mind and more complex social communication abilities [Baron-Cohen, 2000; Tomasello, Carpenter, Call, Behne, & Moll, 2005; Tomasello, Kruger, & Ratner, 1993]. This potential overlap in skill sets has led some to postulate that imitation recognition itself may be a key factor in promoting development of both theory of mind and social communication more generally [Asendorpf et al., 1996; Meltzoff, 1990; Meltzoff and Gopnik, 1993; Nadel, 2002b; Nadel et al., 2004; Nielsen and Dissanayake, 2004]. Given that imitation recognition is hypothesized to underlie development of social communication and theory of mind, and that these both are considered core deficits in individuals with autism spectrum disorder (ASD) [Baron-Cohen, 2000; McEvoy, Rogers, & Pennington, 1993], it is important to develop a greater understanding of imitation recognition in this unique population. Paralleling studies with typically developing children, it is well established that children with ASD show increased social attention (i.e., eye contact, coordinated gaze shifting) and social signals (i.e., approach, touching) when they are imitated by an adult compared to when they are interacted with contingently, but not imitatively [e.g., Dawson & Adams, 1984; Escalona, Field, Nadel, & Lundy, 2002; Ezell et al., 2012; Field, Field, Sanders, & Nadel, 2001; Tiegerman & Primavera, 1984]. There is comparatively less work examining more mature imitation recognition (e.g., testing behaviors) in this population. Across a series of articles, Nadel

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and colleagues have presented observational accounts of these behaviors [Nadel, 2002a, 2004; Nadel et al., 2004], but only one study to date has directly examined this construct in ASD [Berger & Ingersoll, 2013]. Berger and Ingersoll’s [2013] recent study focused on demonstrating the ability of young children with ASD to engage in more mature imitation recognition behaviors (i.e., testing behaviors), and on elucidating the relationship between less mature (i.e., social attention) and more mature imitation recognition behaviors and hypothetically related social cognitive skills. This study found that some children with ASD indeed demonstrate advanced imitation recognition behavior such as testing behaviors. It also revealed a significant positive relationship between advanced imitation recognition behaviors and imitation skills and a significant negative relationship between advanced imitation recognition skills and impaired social reciprocity on the ADOS. However, Berger and Ingersoll’s [2013] study used a concurrent correlational design and no control group was used. As such, it is unknown how engagement in imitation recognition behaviors differs between children with ASD and their typically developing peers, although Nadel [2004] speculates that the development of imitation recognition skills in ASD parallels the developmental progression in typically developing infants, albeit at a delayed pace. Additionally, while results of the study indicated that rates of imitation recognition behavior were positively related to amount of contingent imitation, it remains unclear how contingent imitation influences expression of imitation recognition behaviors over time. This study aims to fill these gaps in the literature by directly assessing the degree to which children with ASD and a language- and cognitively-matched group of typically developing children engage in a variety of imitation recognition behaviors (e.g., looking at the experimenter and testing behaviors) during a period of contingent imitation by an adult. We expect that typically developing children will exhibit all types of imitation recognition behaviors at a higher rate than children with ASD. Based on findings indicating a positive relationship between prolonged periods of contingent imitation and imitation recognition [Berger & Ingersoll, 2013], we expect that both typically developing children and children with ASD will engage in greater amounts of all types of imitation recognition behaviors as the assessment progresses. We also explore the relationship between imitation recognition and behaviors that support social communication and development of theory of mind (i.e., imitation, communication, social reciprocity, and joint attention). Given the postulate that this skill set and imitation recognition are related, we expect that children who exhibit a higher frequency of engagement in imitation

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Table 1.

Participant Characteristics VMAb (mos.)

CA (mos.)

Autism Severitya

NVMAc (mos.)

Part. (n 5 30)

Mean

SD

Mean

SD

Mean

SD

Mean

SD

ASD TD

7.20 –

1.61 –

54.93 23.93

13.87 4.26

26.67 25.13

5.12 3.91

25.47 30.45

8.77 7.16

a

ADOS CSS. PLS-4/MSECL. c BSID-3/MSECL. b

recognition behaviors while being imitated will show more advanced skills across our standardized measures of imitation, communication, social reciprocity, and joint attention.

Methods Participants Children were recruited for the study by advertisements to local agencies serving children with autism, community events, and local preschools. Participants included 15 typically developing children (6 male) and 15 children with a community diagnosis of ASD (13 male), matched groupwise on nonverbal mental age and total language abilities (Nonverbal mental age: t(28) 5 20.92, n.s.; Total language: t(28) 5 1.71, n.s.; see Table 1 for participant characteristics). Typically developing children were screened for developmental concerns using the Communication and Symbolic Behavior ScalesDevelopmental Profile Infant-Toddler Checklist [CSBS-DP; Wetherby & Prizant, 2002]. No children were excluded from participation as no developmental concerns were reported by parents of typically developing children. ASD diagnoses were confirmed using the Autism Diagnostic Observation Schedule—2 [ADOS-2; Lord et al., 2000]. All children scored above the cutoff for either Autism or ASD on the revised ADOS algorithm [Gotham, Pickles, & Lord, 2009]. Design and Procedure Parents provided written consent for their child’s participation. Over a period of 3–4 days (approximately 3–4 hr in total), each child was tested individually in a quiet room either at their school or a University research laboratory. All behavioral testing was videotaped for later primary and inter-rater reliability scoring. Each child was provided a $20 gift card to a local toy store following their participation.

ages 1–42 months. Only the cognitive scale of the BSID-III was used here. Nonverbal mental age was operationalized in our analyses as age equivalent scores [Akshoomoff, 2006]. The Mullen Scales of Early Learning [MSEL; Mullen, 1995] was used to assess nonverbal mental age for six children with ASD in place of the BSID-III. The MSEL [Mullen, 1995] is a standardized developmental assessment for children up to 68 months of age. Average age equivalent across the Fine Motor and Visual Reception subscales acted as a proxy for nonverbal mental age for these children [e.g., Bishop, Guthrie, Coffing, & Lord, 2011; Green et al., 2010; Richler, Bishop, Kleinke, & Lord, 2007].

Language skills. The Preschool Language Scales, 4th Edition [PLS-4; Zimmerman, Steiner, & Pond, 2002] is a standardized assessment that measures language ability in children from 0 to 6 years, 11 months. Our measure of language ability was total language age equivalent (representing combined receptive and expressive skills). The language abilities of six children with ASD were assessed using the Mullen Scales of Early Learning [Mullen, 1995] in place of the PLS-4. Average age equivalent across the Receptive and Expressive subscales was used as a proxy for language abilities for these children.

ASD symptomatology. The Autism Diagnostic Observation Schedule-2 [ADOS-2; Lord et al., 2000], a standardized observational assessment, was used to examine autism symptomatology. The sample was characterized using calibrated severity scores derived from the ADOS2 algorithm (possible range 5 1–10) [Gotham, Pickles, & Lord, 2009]. Children were required to have a calibrated severity score of at least 5 to be included in our sample. The sum of the algorithm items for the Social Affective Domain (possible range 5 0–20) was used as a measure of Social Reciprocity [e.g., McDuffie et al., 2007].

Measures Nonverbal mental age. The Bayley Scales of Infant Development, 3rd Edition [BSID-III; Bayley, 2006] is a standardized developmental assessment for children

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Joint attention. The Early Social Communication Scales [ESCS; Seibert, Hogan, & Mundy, 1982] examines the child’s ability to engage in communication and

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Table 2.

Descriptions of Each Type of Imitation Recognition Behavior

Overall Category

Behavior

Abbreviation

Less mature imitation recognition

Looks at experimenter’s toy

EXP-T

Less mature imitation recognition More mature imitation recognition More mature imitation recognition

Looks at experimenter

EXP-F

Looks plus social signal

EXP-SS

Testing behavior

TEST

social interaction with an adult. Number of shows, points, and coordinated gaze shifts was used as a measure of Initiation of Joint Attention (IJA). Percent of correct responses to 6 proximal points and 8 distal points was used as a measure of Response to Joint Attention (RJA). Reliability was calculated by two independent raters, blinded to study aims, on 25% of observations using percent agreement, yielding agreement of 94.18% for IJA (65–100%) and 86.92% for RJA (68– 100%).

Imitation skills. A modified version of the Unstructured Imitation Assessment [UIA; Ingersoll & Meyer, 2011] was used here. The UIA is an imitation assessment examining a child’s ability to imitate spontaneously in a social-interactive context. The modified UIA used here included nine actions with objects, each associated with a specific toy. While the original UIA contains ten object actions [see Ingersoll & Meyer, 2011 Table 2 for descriptions of each action], our methodology (designed to maintain the integrity of the UIA while creating discrete periods of contingent imitation) required only nine objects. As such, we chose to exclude the item “feeding a stuffed bear” as a detailed analysis of item responses from all children who have completed the UIA in our laboratory indicated that children with ASD rarely imitated this target action. In the modified UIA, the child and experimenter were seated on the floor with three pairs of identical toys. To begin the task the examiner said, “I have some toys to play with. We can play together.” Then, the examiner imitated all of the child’s behavior and vocalizations for approximately 1 min. If the child engaged in toy play during this period, the experimenter imitated the child’s play with a duplicate toy. After the initial imitation period, the examiner began to model actions with toys. Before each trial, the examiner said “Watch me” and then modeled an action and a related verbal marker (e.g., “Bang, bang, bang,” when banging two cups together)

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Description Child shifts gaze away from own object to look at the object being manipulated by the experimenter. Child cannot be concurrently looking at own and experimenter’s toy; must shift from looking at own toy to direct gaze towards partner’s manipulation of object. Child directs gaze directly at experimenter’s face. Child directs gaze at experimenter’s face and uses a social signal (laugh, smile, reach, offer, etc.). Child changes his behavior to “test” whether the adult is mirroring him. Child visually references experimenter either immediately following or during the change in action.

followed by a 10-s response period. Each action was modeled three times regardless of the child’s subsequent behavior. After the third model, the examiner returned to imitating the child for approximately 1 min before presenting a new action. Contingent imitation by the examiner was done between actions to develop rapport and because we wanted to measure children’s ability to imitate in social-interactive context. Toys were presented in random order; however, the examiner refrained from modeling an action with the toy that the child was currently engaged with. After modeling an action with each toy in the set, the experiment engaged in a 3 min contingent imitation period. During this period of prolonged contingent imitation, the experimenter imitated all actions and vocalizations of the child. All toys in the set remained available to the child during this period, such that if the child engaged with a toy the experimenter was able to imitate the child’s play with a duplicate toy. This same procedure was repeated for the remaining two toy sets until all nine actions with objects were modelled. Toys were grouped together into sets based on average rate of action imitation in prior studies [i.e., Berger & Ingersoll, 2013; Ingersoll & Meyer, 2011] to ensure that each toy set contained target actions that were comparable in salience and difficulty. Participants received each toy set in a pseudo-randomized order (our sample size did not allow for complete counterbalancing). The child’s response to each of the nine target actions was scored as 0 5 no imitation, 1 5 partial imitation, or 2 5 complete imitation. For each participant, scores on the nine target actions were added together for a total possible score ranging from 0 to 18. Feedback was noncontingent on child performance, and included only verbal praise to encourage engagement with the toys (e.g., “Good playing”). Scoring was done by a trained research assistant blind to the study aims. Reliability was calculated by comparing scores of the primary coder with a blinded, independent observer on 25% of participants (j 5 0.86).

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Imitation recognition task. UIA videotapes were coded to assess child behavior during each of the 3-min contingent imitation periods. As previously described, the UIA requires that the experimenter engage in a brief period of contingent imitation between each play action being modelled. While it is possible to code imitation recognition during these brief periods [e.g., Berger & Ingersoll, 2013], we wanted to maximize the saliency of the contingent imitation period and ensure that each child received the same amount of contingent imitation. Thus the modified UIA used here also contained distinct periods of contingent imitation that were consistent across children; each child received a total of 9 min of contingent imitation. This design allowed us to control for the possibility that longer lengths of contingent imitation may influence imitation recognition behaviors. Operational definitions for less mature and more mature imitation recognition behaviors were identical to those used by Berger and Ingersoll [2013]. These definitions are based on Meltzoff’s [1990] and Nadel’s [2002a] descriptions (Table 2). Rate of engagement in these behaviors (i.e., percent of intervals spent engaging in each behavior) represented our primary outcome measures. Videos were scored using 10-s interval coding by a trained research assistant blind to study aims. To assess interobserver reliability, 33% of children were chosen at random from each group and an independent coder scored their engagement in imitation recognition behaviors. Cohen’s kappa was 0.84 for looks at experimenter’s toy (EXP-T), .90 for looks at experimenter’s face (EXP-F), 0.86 for looks plus social signal (EXP-SS), and 0.95 for testing behavior (TEST). These values represent substantial to almost perfect agreement [Landis & Koch, 1977]. Data Analysis Data collected did not violate assumptions of independence or sphericity, and was not significantly skewed, platykurtic, or leptokurtic. As such, all analyses conducted were parametric (except those involving rankordered variables). A two-factor multivariate analysis of variance (MANOVA) with group as a between-subjects factor and imitation recognition behaviors as withinsubjects factors was conducted. Univariate F tests for each variable were conducted to explore significant MANOVA results. To address Nadel’s [2004] hypothesis that these skills emerge in a developmental sequence, two repeated measures ANOVAs were conducted (one for each group) to compare rates of engagement in each imitation recognition behavior. To evaluate the influence of length of contingent imitation on imitation recognition, we assessed engagement in these skills across and within the 3-min blocks using a series of repeated measures ANOVAs and paired t-tests. Pearson

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Figure 1. Rate of engagement in each type of imitation recognition behavior across groups. EXP-T 5 Looks at experimenter’s toy; EXP-F 5 Looks at experimenter’s face; EXP-SS 5 Looks plus social signal; TEST 5 Testing behavior. product-moment correlations were also conducted to explore the relationship between imitation recognition abilities and other social-cognitive skills for each group. As our social reciprocity measure was ordinal, Spearman’s rank-order correlation coefficients were used to examine the relationship between imitation recognition skills and this construct.

Results Engagement in Imitation Recognition Behaviors Across Groups A one-way MANOVA revealed a significant main effect for group, such that overall typically developing children engaged significantly more in imitation recognition behaviors than children with ASD [Wilks’ k 5 0.22, F(4, 25) 5 22.72, P < 0.001]. Follow-up ANOVAs indicated significant univariate main effects for group across all imitation recognition behaviors [Look at experimenter’s toy: F(1, 28) 5 35.28, P < 0.001; Look at experimenter’s face: F(1, 28) 5 40.98, P < 0.001; Looks plus social signal: F(1, 28) 5 24.64, P < 0.001; Testing behavior: F(1, 28) 5 17.56, P < 0.001] suggesting that children with ASD are impaired in their imitation recognition abilities relative to typically developing controls (Figure 1).1 We further examined the proportion of children in each group who engaged in each of the imitation recognition 1 There is some research suggesting gender differences in social cognitive skills of young children [e.g., Walker, 2005]. To investigate the potential influence of gender on our results, we conducted additional analyses comparing imitation recognition performance of typically developing girls to typically developing boys in our sample. No gender differences were identified across any type of imitation recognition behavior. While the differential ratio in boys to girls across our samples of children with ASD and typically developing children represents a limitation to our study, it is unlikely that gender contributed to the differential imitation recognition abilities between children with ASD and their typically developing peers observed here.

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Table 3.

Means and Standard Deviations for Percent of Intervals Engaging in Each Imitation Recognition Behavior EXP-T

Part. (n 5 30) Mean SD

EXP-F

Test

ASD

TD

ASD

TD

ASD

TD

ASD

TD

37.37 15.26

71.48 16.10

26.46 17.11

64.44 15.33

8.52 12.12

37.90 19.46

9.14 16.09

34.69 17.29

behaviors at least once. All children (from both groups) engaged in EXP-T and EXP-F. However, more typically developing children (100%) engaged in EXP-SS imitation recognition than children with ASD (60%; v2 5 4.67, P < 0.05). The same pattern is evident when examining testing behaviors (TD: 100%, ASD: 53%; v2 5 9.13, P < 0.005). Rates of Engagement in Imitation Recognition Behaviors Within Groups Two repeated measures ANOVAs were conducted (one for each group). The first repeated measures ANOVA indicated a significant difference between the rate of the different imitation recognition behaviors for typically developing children, F(3, 42) 5 29.28, P < 0.001. Follow-up paired t-tests, adjusted for multiple tests using Bonferroni correction, indicated that typically developing children were significantly more likely to engage in EXP-T than either EXP-SS (t(14) 5 7.13, P < 0.001) or TEST (t(14) 5 6.75, P < 0.001). Typically developing participants were also significantly more likely to engage in EXP-F than EXP-SS, t(14) 5 6.17, P < 0.001 or TEST behaviors, t(14) 5 7.94, P < 0.001. There were no significant differences in rates of either EXP-T and EXP-F (t(14) 5 1.14, n.s.), or EXP-SS and TEST, (t(14) 5 0.79, n.s). The second repeated measures ANOVA indicated a significant difference between the rate of the different imitation recognition behaviors for children with ASD, F(3, 42) 5 21.78, P < 0.001. Results from follow-up paired ttests, again adjusted for multiple tests using Bonferroni correction, paralleled that of typically developing children. Results indicated that children with ASD were significantly more likely to engage in EXP-T than either EXP-SS (t(14) 5 5.65, P < 0.001) or TEST (t(14) 5 5.53, P < 0.001). Participants with ASD were also significantly more likely to engage in EXP-F than EXP-SS, t(14) 5 7.23, P < 0.001 or TEST behaviors, t(14) 5 7.38, P < 0.001. There were no significant differences in rates of either EXP-T and EXP-F (t(14) 5 1.81, n.s.), or EXP-SS and TEST, (t(14) 5 0.21, n.s). See Table 3 for mean imitation recognition behavioral frequencies for both children with ASD and typically developing children. Relationship Between Contingent Imitation Period and Imitation Recognition Behaviors To assess how contingent imitation influenced expression of imitation recognition behaviors over time, we

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EXP-SS

evaluated engagement in these skills both across and within the 3-min blocks using a series of repeated measures ANOVAs (to compare rate of imitation recognition behaviors across the three blocks) and paired t-tests (to compare rate of imitation between the first and second half of each period). In conducting these analyses, we collapsed EXP-T and EXP-F together into a single variable “less mature imitation recognition” and EXP-SS and TEST into a second variable “more mature imitation recognition.” This was done given our current findings that frequency of engagement in EXP-T and EXP-SS do not differ from EXP-F and TEST, respectively, and prior research indicating that these behaviors meaningfully group together into two distinct constructs [Berger & Ingersoll, 2013].

ASD participants. The first set of repeated measures ANOVAs included only ASD participants, and indicated no significant difference in engagement in either less mature imitation recognition (F(2, 26) 5 1.84, n.s.) or more mature imitation recognition (F(2, 26) 5 1.75, n.s.) across the three blocks of contingent imitation (Figure 2). This suggests that our method indeed assessed children’s underlying imitation recognition abilities, rather than acting as a “mini-intervention.” Further, examination of the individual data indicated that no child expressed more mature imitation

Figure 2. Rate of engagement in imitation recognition behaviors across each block of contingent imitation, by group. LM 5 less mature imitation recognition; MM 5 more mature imitation recognition.

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ognition behaviors extensively across all three periods, with levels of engagement similar across contingent imitation periods. No significant results emerged when comparing rate of imitation recognition behaviors within time blocks (Less Mature imitation recognition: t(14) 5 0.79, n.s.; More Mature imitation recognition: t(14) 5 20.39, n.s.; see Figure 3), suggesting that typically developing children display their imitation recognition skills readily when being contingently imitated by an adult.

Figure 3. Rate of engagement in imitation recognition behaviors within each block of contingent imitation, by group. LM 5 less mature imitation recognition; MM 5 more mature imitation recognition. recognition abilities in the third block who did not also express these abilities in either the first or second blocks. To investigate display of imitation recognition behaviors within the 3-min time blocks, each block was divided in half. Engagement in imitation recognition behaviors within the first 1.5-min segment of each block were averaged together, as was engagement in imitation recognition behaviors within the second half of each block. Paired t-tests allowed us to examine whether increased length of contingent imitation period facilitates display of imitation recognition behaviors. This did not appear to be the case for less mature imitation recognition abilities (t(14) 5 0.72, n.s.). While results of the paired t-test for more mature imitation recognition were also nonsignificant (t(14) 5 21.86, P 5 0.08, Cohen’s d 5 0.48), the data indicated a trend toward greater expression of more mature imitation recognition behaviors in the second half of the contingent imitation periods. The effect size for this comparison indicates that this is bordering on a medium sized effect [Cohen, 1988]. This suggests that for children with ASD, display of more mature imitation recognition behaviors may require a sustained period of contingent imitation by an adult (Figure 3).

Typically developing participants. Paralleling our results with ASD participants, our second set of repeated measures ANOVAs indicated no significant difference in engagement in either less mature imitation recognition (F(2, 28) 5 0.66, n.s.) or more mature imitation recognition (F(2, 28) 5 1.08, n.s.) across the three blocks of contingent imitation (Figure 2). Our typically developing children naturally engaged in imitation rec-

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Association between imitation recognition and other social-cognitive skills. Finally, we examined the associations between imitation recognition behaviors and other social-cognitive skills. An immediate issue of consideration here is our small sample size for each group. Correlations with only 15 individuals are highly susceptible to differences in individual data, and thus these findings should be considered exploratory. The collapsed variables of less mature imitation recognition and more mature imitation recognition were used here to compare results with previous research. Results from this analysis are presented in Table 4. For children with ASD, engagement in less and more mature imitation recognition was related to low social reciprocity and object imitation whereas more mature imitation recognition was also related to language. No significant relationships emerged when examining imitation recognition behaviors and social-cognitive skills for children with typical development.

Discussion The purpose of this study was to directly compare how children with ASD and typically developing children respond to being imitated during a naturalistic imitation task. Previous empirical research has demonstrated that children with autism do indeed engage in a variety Table 4. Bivariate Correlations Between IR Behaviors and Standardized Assessments

Total lang. Low social reciproc.a Object imitation RJA IJA

Less Mature IR

More Mature IR

ASD

TD

ASD

TD

0.30 20.55* 0.58* 0.36 0.16

0.28

0.66** 20.49* 0.57** 0.45 0.08

0.27

0.06 0.16 0.28

0.32 0.17 0.06

* P < 0.05, ** P < 0.01. Note. As our hypotheses predicted specific directional relationships, all bivariate correlations are one-tailed. a Spearman’s rho reported for low social reciprocity analyses. Social Reciprocity was measured by the Social Affective scale on the ADOS-2.

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of imitation recognition behaviors [Berger & Ingersoll, 2013; see Nadel, 2002a, 2004; Nadel et al., 2004 for descriptive studies]; however, to our knowledge, this is the first empirical study to directly compare imitation recognition abilities in young children with ASD and typically developing children. Our finding that children with ASD engage in less mature imitation recognition behaviors (i.e., increased social attention) when contingently imitated is consistent with other work in this area [Dawson & Adams, 1984; Escalona et al., 2002; Ezell et al., 2012; Field et al., 2001; Tiegerman & Primavera, 1984]. In line with results from our previous study [Berger & Ingersoll, 2013], we also found here that children with ASD engage in more mature forms of imitation recognition (i.e., testing behaviors). However, we also found that children with ASD engage in all forms of imitation recognition behaviors with less frequency than their typically developing peers. Interestingly, both groups displayed the same pattern of engagement in imitation recognition behaviors, such that they engaged more frequently in less mature than more mature imitation recognition behaviors. This study provides additional empirical support for Nadel’s [2004] hypothesis that imitation recognition skills unfold in a consistent, albeit delayed, developmental sequence in children with ASD. However, it remains unclear whether children with ASD ever “catch up” with their typically developing peers such that they eventually engage in similar frequencies of imitation recognition behaviors. The striking difference in proportion of children exhibiting testing behavior in response to contingent imitation across groups suggests that more mature imitation recognition behaviors may act to distinguish children with ASD from those with typical development. Importantly, imitation recognition appears to be an early emerging skill, with typically developing children reliably exhibiting testing behaviors by 9–15 months [Meltzoff, 1990; Nadel et al., 2004]. Our results are consistent with this, such that all typically developing children in our sample (minimum chronological age of 16 months) engaged in the highest level of imitation recognition behavior (i.e., testing behavior) at least once. Despite our ASD sample being well-beyond both the chronological age and the developmental level at which testing behavior is typically observed (mean nonverbal mental age was 26.67 months; minimum chronological age of 35 months), only 53% of the sample engaged in this behavior at all. Given the developmental sequence in which these skills appear to unfold, it is likely than even fewer children with ASD would have exhibited this behavior at a younger age. This finding may suggest that testing behavior in response to contingent imitation may aid in the differential diagnosis of ASD in very young children.

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Response to contingent imitation might also be useful as a brief, cost effective screening tool to refer toddlers for more comprehensive assessment or early intervention. However, it would be critical to better understand the specificity of imitation recognition deficits to ASD populations before exploring these clinical possibilities. Further research using a developmentally delayed control group is thus recommended, and lack of this comparison group represents a limitation to this study design. Our original hypothesis around length of contingent imitation period and expression of imitation recognition behaviors was only partially supported. In line with our hypothesis, results demonstrate that children with ASD respond to sustained periods of contingent imitation by increasing their more mature imitation recognition behaviors. This indicates that treatments using contingent imitation as a key intervention strategy are likely to positively influence more mature imitation recognition behaviors. This is a novel finding, as previous work with this population has focused primarily on changes in social attention (i.e., less mature imitation recognition) in response to contingent imitation [Dawson & Adams, 1984; Escalona et al., 2002; Field et al., 2001; Tiegerman & Primavera, 1984]. The relationship between sustained contingent imitation and engagement in more mature imitation recognition is particularly important given data suggesting that more mature imitation recognition behaviors (and not less mature imitation recognition behaviors) are positively related to language in children with ASD. Notably, our finding that imitation recognition behaviors improved within a three minute block, but did not change across multiple blocks, for children with ASD suggests that interventions using this technique should emphasize prolonged periods of sustained contingent imitation rather than brief, repeated, bouts of contingent imitation. However, we did not include a control condition in which the experimenter responded contingently but did not imitate the children’s behavior. Research indicates that contingent imitation (as opposed to contingent responding) increases social attention in children with ASD [e.g., Tiegerman & Primavera, 1984], and thus one might expect the same pattern of behaviors for more mature imitation recognition behaviors. Nevertheless, it is important for future research to compare more mature imitation recognition behaviors during both contingent imitation and contingent responding. In contrast to our hypothesis, typically developing children’s rates of imitation recognition behaviors did not change as a function of length of contingent imitation period. These children immediately recognized that the adult was imitating them, and responded accordingly. The finding that typically developing children and children with ASD differed in their rate of

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imitation recognition behaviors as a function of length of contingent imitation period suggests that the underlying mechanism for imitation recognition may be underdeveloped in this population. However, motivation as a key factor influencing development of social cognitive skills has recently emerged as a potential explanation for core impairments observed in those with ASD (Chevallier, Kohls, Troiani, Brodkin, & Schultz, 2012]. According to Chevallier et al.’s [2012] account of social motivation models of ASD, early deficits in social attention provide a foundation for developmental processes that limit the child’s exposure to adequate opportunities for social learning. This creates an imbalance in the child’s attention to social and nonsocial stimuli, which then evokes additional disruption in the development of social skills and social cognition. Support for this hypothesis comes from behavioral studies examining infant orienting behaviors to different types of environmental stimuli. For example, Dawson, Meltzoff, Osterling, Rinaldi, and Brown [1998] found that young children with ASD, compared to typically developing peers and children with Down’s Syndrome, more frequently fail to orient to stimuli in their environment. Of key interest here, however, is their finding that this failure to orient was much more extreme for social stimuli compared to nonsocial stimuli [Dawson et al., 1998]. More recent work supporting the social motivation hypothesis has used EEG to investigate the neural correlates of reward processing in typically developing children and children with ASD. Stavropoulos and Carver [2014] found that children with autism have reward anticipation and processing deficits for social stimuli, but not for nonsocial stimuli, compared to their typically developing peers. The authors interpret their findings as indicating that typically developing children find social stimuli more salient than nonsocial stimuli, while children with ASD appear to have the opposite preference. Our research provides additional support for the social motivation hypothesis [Chevallier et al., 2012]. The failure of children with ASD to engage in less mature imitation recognition (i.e., basic social attention) as frequently as their typically developing peers could have downstream consequences, including, but not limited to, difficulty with more mature imitation recognition. For example, previous research with typically developing infants and children indicates that being imitated prompts continuation of play interactions [Grusec & Abramovitch, 1982; Lubin & Field, 1981], further imitation between peers [Eckerman, 1993], promotes helping behaviors [Carpenter, Uebel, & Tomasello, 2013], increases trust [Over, Carpenter, Spears, & Gattis, 2013], and is related to the initiation of subsequent play interactions [Fawcett & Liszkowski, 2012]. Failure to recognize the imitation of others

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would functionally limit children with autism’s ability to use mimicry “as a tool to establish social connectedness with others” [Fawcett & Liszkowski, 2012, p. 689] and interfere with the development of typical peer relationships and potentially other, more advanced, social cognitive skills. Typically developing children do not experience this deficit in social motivation, and thus immediately attend (i.e., less mature imitation recognition) and respond (i.e., more mature imitation recognition) to the adult’s imitative behaviors. Previous work has proposed a relationship between imitation recognition and the emergence of more advanced social cognitive skills [Asendorpf et al., 1996; Berger & Ingersoll, 2013; Meltzoff, 1990; Meltzoff & Decety, 2003; Meltzoff & Gopnik, 1993; Nadel 2002a, b; Nadel et al., 2004]. Notably, according to Meltzoff’s [2007] “Like-me” developmental theory, the recognition of being imitated by others is a manifestation of nonverbal self-other understanding and a building block for social-cognitive development. Meltzoff [2007] holds that it is the recognition of self-other equivalences in action that facilitates the understanding that others have parallel psychological states, and goes as far as to hypothesize that impairment in the “like-me” mechanism can help explain the characteristic deficits associated with ASD. While Meltzoff’s [2007] framework is based largely on work with typically developing children, our finding that children with ASD are uniquely impaired in their imitation recognition abilities provides support for his theory. Furthermore, as would be predicted by Meltzoff, we have identified a relationship between imitation recognition abilities and other social cognitive skills (although our correlational results must be considered exploratory given the small sample size). Our correlational analyses indicated that both less mature and more mature imitation recognition skills are significantly related to language, spontaneous imitation production, and social reciprocity. However, it is important to note that while the correlational results reported here are generally in line with our previous work [Berger & Ingersoll, 2013], some differences did emerge. Specifically, the observed negative relationship between less mature imitation recognition and low social reciprocity (i.e., children with better social reciprocity exhibited more social attention behaviors) is in contrast to previous results that identified a relationship with social reciprocity only for more mature imitation recognition. This is likely driven by the different operational definitions of social reciprocity across the two studies. While the initial study used the Social Reciprocity score from the ADOS-G, the current results reflect the Social Affective score from the ADOS2. These differ in that the Social Affective domain of the ADOS-2 contains several communication items (e.g., gestures and spontaneous vocalizations directed at

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others) and the Social Reciprocity score from the ADOSG does not. As such, the child’s basic communication abilities may be contributing to the significant negative relationship identified in this study between low social reciprocity and less mature intention understanding. A significant relationship between measures of joint attention and less mature or more mature imitation recognition was not found, and we cannot draw clear conclusions from this null finding given our small sample size and the correlational design of the study. Given the magnitude of the relationships between response to joint attention and less mature and more mature imitation recognition, it seems likely that the lack of significant results was driven by our sample size. In contrast, the relationships between our imitation recognition constructs and initiation of joint attention were close to zero. This parallels results from our prior work [Berger & Ingersoll, 2013]. As we have previously speculated, this may indicate that recognizing and understanding the intentional behavior of an imitative partner is distinct from mechanisms involved in sharing an experience with that partner. Our exploratory correlational analyses also did not identify any significant relationships between imitation recognition and social cognitive skills in typically developing children. The lack of significant relationships likely reflects the lack of variability in skill set within this sample (i.e., typically developing children were essentially at ceiling across tasks). It may also be that the relationship between imitation recognition and social cognitive skills is observed primarily during the preverbal stage in typical development. For example, Nadel [2006] has observed that typically developing children no longer use communicative imitation once they acquire language. Given the delays in communication skills observed in children with ASD, the relationship between imitation recognition and social cognitive skills may last for a longer period. It should be noted that while we are unable to discern the directionality of the observed relationships in this study, the findings reported here, coupled with the relative impairment observed in children with ASD, indicate that imitation recognition may be another foundational skill to be included in early interventions for this population. However, additional work using longitudinal designs is called for to further clarify the role imitation recognition plays in the development of more advanced socialcognitive skills. In conclusion, this study indicates that children with ASD are impaired in their ability to recognize being imitated compared to typically developing peers as indicated both by behaviors representing basic social attention and more mature imitation recognition. Exploratory findings also suggest a link between the ability to demonstrate recognition of

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being imitated and social reciprocity, language, and object imitation. Further research characterizing the role imitation recognition plays in the development of social communication and the specificity of the impairment in more mature imitation recognition to ASD is needed.

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