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Oct 26, 2006 - Keywords Autism Ж ASD Ж Social communication Ж. Early identification ... Springer Science+Business Media, LLC 2006 ..... four trained examiners who were blind to the child's diagnosis ...... San Diego: Singular Publishing.
J Autism Dev Disord (2007) 37:960–975 DOI 10.1007/s10803-006-0237-4

ORIGINAL PAPER

Social Communication Profiles of Children with Autism Spectrum Disorders Late in the Second Year of Life Amy M. Wetherby Æ Nola Watt Æ Lindee Morgan Æ Stacy Shumway

Published online: 26 October 2006  Springer Science+Business Media, LLC 2006

Abstract This study examined social communication profiles from behavior samples videotaped between 18 and 24 months of age in three groups of children: 50 with autism spectrum disorders (ASD), 23 with developmental delays (DD), and 50 with typical development (TD). The ASD group scored significantly lower than the DD group on 5 social communication measures and the TD group on all 14 measures, indicating distinct profiles late in the second year. Understanding was the strongest predictor of developmental level and behavior regulation and inventory of gestures were the strongest predictors of autism symptoms at 3 years of age. The predictive relations suggest five pivotal skills late in the second year that have a cascading effect on outcomes of children with ASD. Keywords Autism Æ ASD Æ Social communication Æ Early identification Æ Joint attention

A. M. Wetherby (&) Æ N. Watt Æ L. Morgan Æ S. Shumway Department of Communication Disorders, Florida State University, RRC 107, Tallahassee, FL 32306-7814, USA e-mail: [email protected] Present Address: N. Watt Discipline of Speech Pathology and Audiology, School of Human and Community Development, University of the Witwatersrand, Johannesburg, South Africa Present Address: S. Shumway Pediatrics and Developmental Neuropsychiatry Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA

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Introduction Research has consistently documented social communication deficits as core features of autism spectrum disorders (ASD; Volkmar, Lord, Bailey, Schultz, & Klin, 2004). Social communication skills include a broad array of verbal and nonverbal behaviors used in reciprocal social interaction. Weaknesses in social communication are universal in children with ASD across ages and ability level, in spite of heterogeneity of language abilities (Tager-Flusberg, Joseph, & Folstein, 2001). Although impairments in social communication are a hallmark of ASD, relatively little is known about these deficits in very young children due to the usual age of diagnosis. While most children with ASD are not diagnosed until at least 3 years of age, a diagnosis can be made reliably by experienced clinicians at 2 years of age and this diagnosis has been found to persist a year later in 90% of children studied (Lord, 1995; Stone et al., 1999). Impairments in social communication were found to be prominent by 2 years of age but restricted and repetitive activities and interests were not evident in some children until closer to 3 years. Research on social communication deficits in children under 2 has important implications for improving early identification and informing genetic, biological, and intervention research. A deficit is considered to be core if it distinguishes children with ASD from children with other developmental delays (DD) and typical development (TD; Sigman, Dijamco, Gratier, & Rozga, 2004). A large body of research has identified core deficits in joint attention and symbolic aspects of communication and play in children with ASD from 2 to 5 years of age based on observational studies (Charman et al., 1997;

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Dawson et al., 2004; Lord, 1995; Mundy Sigman, & Kasari, 1990; Sigman, Mundy, Sherman, & Ungerer, 1986; Stone, Ousley, Yoder, Hogan, & Hepburn, 1997; Wetherby, Prizant, & Hutchinson, 1998). Many longitudinal studies have documented a relationship between responding to and/or initiating gestural joint attention in 2- to 3-year old children with ASD and language outcomes 6 months (McDuffie, Yoder, & Stone, 2005), 1 year (Mundy et al., 1990), and many years later (Sigman & Ruskin, 1999). It is possible that joint attention deficits underlie or contribute to symbolic deficits in children with ASD in that difficulties establishing a joint attentional focus may interfere with learning conventional meanings in language. Dawson et al. (2004) investigated social attention impairments in relation to language ability in 3- to 4-year old children with ASD, compared to mental age-matched children with DD and TD. They found that impairments in social orienting and joint attention best distinguished the children with ASD from the comparison groups. Joint attention was the best predictor of concurrent language ability but social orienting and attention to distress were correlated with joint attention, and therefore, may indirectly impact language ability through their relationship with joint attention. Research on core social communication deficits in younger children with ASD may help elucidate the nature of this relationship. Social Communication Deficits of Children with ASD in the Second Year of Life Preliminary research on the social communication deficits of children with ASD under 2 years of age is emerging from three different sources: (a) retrospective analyses of home videotapes of children later diagnosed with ASD; (b) parent report of social communication deficits; and (c) prospective systematic observational studies, and is briefly reviewed below. Retrospective Analysis of Home Videotapes The largest cohort of retrospective analyses is from home videotapes of first birthday parties of children later diagnosed with ASD. Osterling and Dawson (1994) found that at 12 months of age, 4 behaviors distinguished 11 children with ASD from typically developing children: lack of pointing, showing, looking at the face of another, and orienting to name. In a follow-up study, Osterling, Dawson, and Munson (2002) compared first birthday videotapes of 20 children with ASD, 14 with DD, and 20 with TD. They found that lack of looking at the face of another and

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orienting to name distinguished children with ASD from those with DD and TD. Pointing and showing were too infrequent in all three groups for meaningful analyses. Decreased use of gestures and increased use of repetitive behaviors distinguished children with ASD and TD but not children with ASD and DD. No significant group differences were found in use of vocalizations. Werner and Dawson (2005) recently compared first and second birthday videotapes of 36 children with ASD, 21 with early onset of symptoms and 15 with reported regression, and 18 with TD. The early-onset ASD group differed significantly from the groups with regression and TD at 12 months on measures of complex babble or words and declarative pointing but no differences were found on gaze to people, orienting to name, imperative pointing, affect, or repetitive motor behavior. By 24 months, both ASD groups differed from the TD group on complex babble, single words and phrases, declarative pointing, gaze to people, and orienting to name. No differences were found on imperative pointing, affect, appropriate toy play, or repetitive motor behavior. These findings suggest that the social communication deficits of children with ASD based on analysis of home videotapes at 12 and 24 months are not as prominent as those found in research of 2–5 year olds with ASD. The lack of a DD control group limits knowing whether these patterns are specific to ASD. These retrospective studies of home videotapes demonstrate that impairments in social communication are evident in children with ASD at 12 and 24 months and suggest that a broader array of deficits is evident at 24 months than 12 months; however, the findings are inconsistent across samples. For example, lack of looking at people and orienting to name distinguished ASD and TD at 12 months in the Osterling and colleagues (1994, 2002) samples but not the Werner and Dawson (2005) sample. Limited sample sizes may mask group differences. Furthermore, the sampling contexts of home videotapes may not have provided sufficient opportunity for social communicative behaviors, which also may mask group differences. Parent Report Most children with ASD are reported by their parents to demonstrate symptoms within the first 2 years of life, based on retrospective accounts (Werner, Dawson, Munson, & Osterling, 2005; Wimpory, Hobson, Williams & Nash, 2000). Furthermore, most families initially express concern to their pediatrician by the time their child is 18 months old (Howlin & Moore,

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1997; Siegel, Pliner, Eschler, & Elliot, 1988). Werner and colleagues (2005) administered an in-depth retrospective interview to parents of 72 children with ASD when the children were 3- to 4-years of age, and mental-age matched children with DD and TD, to examine variations in the course of development of ASD across the first 2 years of life. They found significant differences among all three groups in social symptoms at 13–15 months, repetitive behaviors at 16–18 months, and communication symptoms at 19– 21 months. Based on parent report with the ADI-R at 20 months of age, Cox et al. (1999) found three behaviors that distinguished 21 children with ASD from children with language delay—range of facial expression, use of conventional gesture, and pointing to indicate interest. These parent report studies support the findings from retrospective home videotape analyses that impairments in social communication skills may be the earliest indicators of ASD and are evident in the second year of life. In addition, findings from parent report suggest that parents of children with ASD may notice or recall impairments that are not as readily apparent on home videotapes. It is important to confirm and extend these findings with observational data. Prospective Systematic Observational Studies Prospective longitudinal designs with general population samples screened to identify very young children with ASD have been used to distinguish these children from matched samples of children with DD and TD. Studies of two cohorts identified in the second year of life have been published. The first cohort consists of children identified prospectively using the Checklist for Autism in Toddlers (CHAT; Baron-Cohen et al., 1996). Charman et al. (1997) found that 10 children who failed the CHAT and were diagnosed with ASD at 20 months used less social gaze in response to distress displayed by the adult, fewer gaze shifts in response to activation of mechanical toys, and less imitation of modeled actions than both the TD and DD groups. Swettenham et al. (1998) found that during free play these children with ASD spent less time looking at people and displayed fewer gaze shifts between people and objects than DD or TD controls. These findings indicate that deficits in aspects of joint attention are evident in children with ASD at 20 months of age. Charman et al. (2003) found that measures of joint attention of 18 children with ASD at 20 months of age predicted language at 42 months of age. In a group of 26 children with ASD with a mean age of 24.5 months, Charman et al. (2005) found that rate of communicating during a systematic sample was

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significantly associated with language, social, and communication outcome at 7 years of age, while standard measures of cognitive and language ability at age 2 did not predict outcome. The second major prospective cohort was identified from a general population screen using the Communication and Symbolic Behavior Scales Developmental Profile (CSBS; Wetherby & Prizant, 2002) and later diagnosed with ASD at age 3. Wetherby et al. (2004) conducted a prospective, longitudinal study to identify red flags for ASD from videotapes collected during the second year of life. Three groups of 18 children were identified, one with ASD with a mean age of 21.0 months, one with DD in which ASD was ruled out matched on developmental level and age, and one with TD matched on age. Children with ASD showed significant differences from both the DD and TD groups on nine red flags: (1) lack of appropriate gaze; (2) lack of warm, joyful expressions with gaze; (3) lack of sharing enjoyment or interest; (4) lack of response to name; (5) lack of coordination of gaze, facial expression, gesture, and sound; (6) lack of showing; (7) unusual prosody; (8) repetitive movements of the body; and (9) repetitive movements with objects. Children with ASD showed significant differences from the TD group but not the DD group on four additional red flags: (1) lack of response to contextual cues; (2) lack of pointing; (3) lack of vocalizations with consonants; and (4) lack of playing with toys conventionally. These differences correctly classified 94.4% of the sample. These findings indicate that children with ASD can be identified in the second year and distinguished from those with DD and TD based on a combination of lack of typical and presence of atypical behaviors, and underscore the importance of social communication along with repetitive behaviors in earlier identification of ASD. These observational studies suggest that by 20 months of age children with ASD have a distinct profile of social communication; however, they are based on small sample sizes. Further research utilizing systematic sampling is needed to provide more precise measures of core social communication deficits during the second year of life. This study is part of an ongoing longitudinal, prospective investigation of the FIRST WORDS Project to examine social communication profiles of children with ASD in the second year of life using systematic observational methods in relation to later outcomes. Although Wetherby et al. (2004) studied samples collected across the second year, the focus of this study was on the second half of the second year of life because the largest cohort of children participated in the Project at this age and social communication features are likely to be prominent at this

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age. Three groups of children were selected for this study, one group with communication delays who were later diagnosed with ASD, one group with communication delays in which ASD was ruled out, and one group with TD. The first objective of this study was to compare social communication measured late in the second year of life across groups. The second objective was to determine whether social communication measured late in the second year in the ASD group predicted nonverbal and verbal developmental level and severity of autism symptoms at 3 years of age.

Method Participant Recruitment There were 123 participants in this study, 50 with a clinical diagnosis of ASD, 23 with DD in which ASD had been ruled out, and 50 with TD. Children were recruited from the ongoing longitudinal, prospective study of the FIRST WORDS Project, which conducts screening on a general population sample recruited from healthcare and childcare agencies to identify children with communication delays under 24 months of age (see Wetherby et al., 2004 for details on the recruitment steps) using the CSBS (Wetherby & Prizant, 2002). The CSBS includes two measures: (a) a one-page, 24-item Infant-Toddler Checklist for screening that can be completed quickly by a parent at a physician’s office or childcare center, and (b) a Behavior Sample, which is a face-to-face evaluation of the child interacting with a parent and clinician that is videotaped for later analysis. Children participating in this study met the following selection criteria: (a) the CSBS Infant-Toddler Checklist was completed by the family when the child was under 24 months of age; (b) a CSBS Behavior Sample was videotaped when the child was over 18 months of age; and (c) the Mullen Scales of Early Learning (MSEL, Mullen, 1995) was completed when the child was over 2 years of age. These 123 participants included the 54 children reported by Wetherby et al. (2004) using samples collected over 18 months of age. Children in the ASD and DD groups were drawn from a pool of children with a communication delay during the second year of life based on performance in the bottom 10th percentile on one or more composites of the Behavior Sample. The children with a communication delay were divided into two groups, ASD and DD, based on a follow-up evaluation completed when the child was at least 30 months of age to make a best estimate diagnosis, described

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below. Children in the TD group were drawn from a pool of children who displayed performance above the 25th percentile on all three composites of the Behavior Sample during the second year and within normal limits on the MSEL. Additionally, none of the TD children were suspected of having ASD by the parent or clinician when the MSEL was completed. The DD group was matched group-wise to the ASD group on the symbolic composite of the CSBS in the second year. Thus, the DD group formed a comparison group at the same age and developmental level as the children with ASD. It is important to note that the DD group included a mixture of children with global developmental delay and with specific language, speech, and/or motor delay, in order to match the variation in cognitive level of the ASD group. The TD group was matched individually to the ASD group on sex and chronological age at the time of the Behavior Sample. Best Estimate Diagnosis A diagnostic evaluation was completed for all children with a communication delay when they were at least 30 months of age by an interdisciplinary team consisting of a licensed speech–language pathologist and psychologist. A clinical diagnosis by an experienced clinician is the most stable and reliable method for diagnosis of ASD in children under 4 years of age, based on consideration of the child’s history, developmental level, adaptive functioning, verbal and nonverbal communication, and level of social engagement and imagination (Chawarska & Volkmar, 2005). The team made a best estimate diagnosis based on the following measures: (a) the MSEL to determine nonverbal and verbal developmental level; (b) the Vineland Adaptive Behavior Scales (VABS; Survey Interview Form; Sparrow, Balla, & Cicchetti, 1984) to provide an index of adaptive behavior; (c) a developmental history; (d) the Autism Diagnostic Observation Schedule (ADOS; Lord, Rutter, DiLavore, & Risi, 1999) to provide a standardized assessment of communication, social interaction, and play or imaginative use of materials for the diagnosis of ASD; and (e) the Social Communication Questionnaire (SCQ; Lifetime Version; Rutter, Bailey, Berument, Lord, & Pickles, 2001) to provide parent report of symptoms of ASD. The team made a best estimate diagnosis of Autistic Disorder, Pervasive Developmental Disorder-Not Otherwise Specified (PDD-NOS), or non-spectrum based on the DSM-IV diagnostic criteria (APA, 1994). The term best estimate diagnosis is used because the

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clinicians were allowed to make a judgment using the information gathered from the diagnostic evaluation to make a diagnosis. A diagnosis of Asperger Disorder was not made or ruled out due to the young age of these children. Children were assigned to the ASD group if they received a diagnosis of Autistic Disorder or PDD-NOS and their communication and social interaction total on the ADOS fell at or above the cutoff for autism spectrum; otherwise they were assigned to the DD group. There was only one child whose ADOS scores fell above the autism spectrum cut-off but did not receive a PDD-NOS diagnosis because the team felt that his heightened scores were due to the severity of his developmental delay. The ADOS could not be completed for two children because they lived at a distance and families could not return for the evaluation. Both of these children received a diagnosis of ASD at 30 months of age or older by a pediatric neurologist, and therefore, were assigned to the ASD group. Of the 73 children with a communication delay, 50 were assigned to the ASD group and 23 to the DD group. In an effort to rule out ASD, families in the TD group were mailed the SCQ (Rutter et al., 2001), which is a 40-item parent report tool for diagnostic screening of ASD appropriate for young children (Corsello, Cook, & Leventhal, 2003). The SCQ total score of 0 indicates no risk for ASD and 15 or higher indicates risk for ASD. If the families did not return the SCQ within 3 weeks, they were sent another copy of the questionnaire. The SCQ was returned by 26 families, which is 52% of the children in the TD group. These children received an average score of 6.1, with a range

from 0 to 12, and all had scores below the cutoff for ASD. Participant Demographic and Developmental Characteristics A summary of participant demographics is presented in Table 1. Mervis and Klein-Tasman (2004) recommended a p-value > .50 on tests of group differences to indicate that groups are well-matched on a variable and a p-value < .20 to indicate that groups are not matched on the variable. Using these criteria, all three groups were well-matched on mother’s and father’s education and mother’s age, suggesting that the groups were comparable on socioeconomic status. The ASD group had slightly more children who were Hispanic and Asian than the TD group and the DD group had slightly more children who were African American than both the ASD and TD groups. Thus, the groups were fairly similar with regard to most aspects of demographics. A summary of participant developmental characteristics for the CSBS Behavior Sample gathered in the second year and the follow-up diagnostic evaluation for the three groups is presented in Table 2. The children ranged in age from 18.24 to 26.86 months at the Behavior Sample. The ASD group was well-matched on age with the TD group using the Mervis and KleinTasman (2004) criterion and minimally-matched with the DD group. The ASD group was significantly different than the TD group on all three CSBS composites and the total. The ASD group was well-matched with the DD group on the symbolic composite only,

Table 1 Summary of participant demographics Demographic

ASD (n = 50)

Parent’s education in years completed Mother (M, SD) 15.48a Father (M, SD) 15.73a Parent’s age at child’s birth in years Mother (M, SD) 31.19a Father (M, SD) 32.99a Males (%) 86.0 First born (%) 39.5 Ethnicity (%) Caucasian 70.0 African American 16.0 Hispanic 10.0 Asian 4.0

DD (n = 23)

TD (n = 50)

F-value

Pairwise p-value DD-ASD

TD-ASD

2.08 2.52

15.36a 15.40a

2.42 2.42

15.15a 15.44a

2.29 2.69

0.27 0.21

.996 .938

.841 .923

4.93 6.82

32.15a 35.72a 82.6 39.1

6.32 5.66

31.60a 34.18a 86.0 37.5

5.83 6.45

0.22 1.53

.892 .232

.973 .766

65.2 21.7 8.7 4.3

86.0 12.0 2.0 0.0

Note: Means in the same row with different subscripts differ significantly at p < .05 on the post-hoc Dunnet T3 comparison F-values are Welch corrected when necessary for violation of homogeneity of variance as assessed by Levene’s test

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Table 2 Summary of developmental characteristics Characteristic

ASD (n = 50)

DD (n = 23)

TD (n = 50)

M

SD

M

SD

M

SD

1.90 2.37 2.63 3.07 12.63

20.71a 7.83b 7.30a 6.48a 81.78a

1.58 3.33 2.75 2.39 12.05

21.14a 11.34c 10.38b 11.30b 103.50b

1.72 2.39 2.48 2.58 11.43

9.61 25.19 31.12

36.37a 86.16a 79.43a

6.01 21.41 21.84

35.98a 115.25b 109.88b

5.11 16.90 16.78

13.41 17.50 13.28 16.20 14.09 13.67

44.58a 81.30a 81.48a 85.70b 76.43a 78.04a

10.93 16.52 20.28 17.97 24.36 19.95

CSBS DP behavior sampled Age in months 21.36a Social composite 4.96a Speech composite 5.84a Symbolic composite 5.84a Total 73.86a Mullen scales of early learninge Age in months 37.74a Nonverbal DQ 76.73a Verbal DQ 67.38a Vineland adaptive behavior scalesf Age in months 42.13a Communication 74.60a Daily living 72.84a Social 74.16a Motor 78.56a Adaptive behavior 70.27a

F-value

Pairwise p-value DD-ASD

TD-ASD

1.17 88.82*** 40.08*** 55.74*** 79.39***

.342 .002 .109 .707 .040

.896 .000 .000 .000 .000

0.64 45.51*** 43.83***

.843 .282 .177

.593 .000 .000

0.66 2.41 3.42 6.70* 0.15 2.82

.422 .128 .074 .013 .702 .103

Note: Means in the same row with different subscripts differ significantly at p < .05 on the post-hoc Dunnet T3 comparison F-values are Welch corrected when necessary for violation of homogeneity of variance as assessed by Levene’s test d

Standard Scores based on a M of 10 and SD of 3 for the Composite and M of 100 and SD of 15 for the Total

e

Developmental Quotients (DQ) based on age equivalent divided by chronological age multiplied by 100

f

Standard Scores based on a M of 100 and SD of 15

* p < .05, ** p < .01, *** p < .001

indicating they were matched on development level in the second year. A DQ based on age equivalent divided by chronological age multiplied by 100, was used to more fully characterize individual variation. A nonverbal DQ was calculated from the average of the fine motor and visual reception scales, and a verbal DQ was calculated from the average of the receptive and expressive language scales. The MSEL scores presented in Table 2 indicate that the ASD and DD groups show a wide range of cognitive functioning. As expected, the ASD group was significantly different than the TD group on nonverbal and verbal DQ. The ASD group was not significantly different than the DD group on nonverbal DQ. The mean verbal DQ for the ASD group was slightly but not significantly lower than that for the DD group, however, the large variance for the ASD group may limit the ability to detect group differences. On the VABS, also presented in Table 2, the ASD group was not significantly different than the DD group on only the motor domain, with small non-significant differences on the communication and daily living domains and significant differences on the social domain. This sample represents the diversity of verbal and nonverbal skills found in this population, with more than half of the sample being relatively higher functioning (nonverbal DQ > 70); 38%

had a nonverbal DQ below 70. The DD group was comprised of 39% who had a nonverbal DQ below 70, 26% with specific language delay, and 35% with speech and/or fine motor delay. The mean age at the time of the ADOS was 44.18 months (SD = 14.09) for the ASD group and 44.76 months (SD = 10.11) for the DD group, which was not significantly different, F = 0.04, p = .845. There were 27 children in the ASD group (54%) who received a best estimate diagnosis of autistic disorder and 23 (46%) who received a diagnosis of PDD-NOS. The mean ADOS communication and social total algorithm score was 13.94 (SD = 4.25) for the ASD group and 3.91 (SD = 3.29) for the DD group, which was significantly different, F = 114.59, p = .000. Based on performance at the time of the diagnostic evaluation, 40 children in the ASD group (80%) and 21 in the DD group (91%) used at least five words regularly with communicative intent; 25 children in the ASD group (50%) and 17 in the DD group (74%) used flexible word combinations. Social Communication Measures from the Second Year of Life The CSBS Behavior Sample was collected using the standard sampling procedures and materials

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(Wetherby & Prizant, 2002). A child’s caregiver was present and instructed to respond naturally, but not to direct the child’s behavior, in order to encourage spontaneous communication and play. The evaluation session began with a warm-up of about 10 min and lasted 30–40 min. The Behavior Sample uses a standard set of systematic procedures designed to encourage spontaneous behavior that range in degree of structure. The child is first presented with communicative temptations to entice spontaneous communication using a windup toy, balloon, bubbles, jar with food, bag with toys, and picture books, and then presented with a feeding toy set and stuffed animal to play symbolically and blocks to play constructively. The sample is divided into six activities during which the child’s social communication skills are rated and includes probes of gaze/point follow and comprehension of object names, person names, and body parts. The Behavior Sample was videotaped and scored using the standard procedures by one of four trained examiners who were blind to the child’s diagnosis. Information about the reliability and validity of the CSBS has been reported in Wetherby, Allen, Cleary, Kublin, and Goldstein (2002), Wetherby, Goldstein, Cleary, Allen, and Kublin (2003), and Wetherby and Prizant (2002). The CSBS was found to have high internal consistency (a coefficients ranging from .86 to .92) and good test–retest reliability over a 4-month interval. Construct and concurrent validity have been supported by the developmental progression of scores from 12 to 24 months of age, inter-correlations among cluster and composite scores, and correlations between the parent report measures and the Behavior Sample. The three composites of the Checklist and Behavior Sample were a significant predictor of receptive and expressive language outcomes at 2 and 3 years of age and the Behavior Sample explained a significant amount of unique variance in language outcomes beyond the Checklist. Thus, the CSBS Checklist and Behavior Sample are appropriate evaluation tools for children with developmental delays from 12 to 24 months of age. For this study, the raw scores were used for 14 items of the CSBS Behavior Sample that form the social, speech, and symbolic composites. Following are descriptions of each. Gaze Shifts The number of activities out of 6 during which the child displays a gaze shift to measure social referencing of

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objects with alternating gaze and must be a 3-point gaze shift (i.e., person–object–person or object– person–object). Shared Positive Affect The number of activities out of 6 during which the child displays shared positive affect to measure social referencing of positive affect defined as a clear facial expression of pleasure or excitement that is directed with gaze to another person. Gaze/Point Follow The number of times that the child looks where the clinician is pointing and looking out of 2 trials, one to the side of the child and one behind the child, to measure the ability to follow the regard of another person’s gaze and point at a distance and is also referred to as responding to joint attention. Rate of Communicating The number of communicative acts used with a maximum of 3 per activity out of 18 to measure the rate of vocal or gestural communicative signals that serve a communicative function. Acts for Behavior Regulation The number of activities out of 6 during which the child communicates for behavior regulation to measure the use of vocal or gestural communicative acts to regulate the behavior of another person to request or protest an object or action. Acts for Social Interaction The number of activities out of 6 during which the child communicates for social interaction to measure the use of vocal or gestural communicative acts to draw attention to oneself to get the other person to look at, notice, or comfort him/her. Acts for Joint Attention The number of activities out of 6 during which the child communicates for joint attention to measure the use of vocal or gestural communicative acts to direct attention to an object to get the other person to look at or notice something of interest.

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Inventory of Gestures The number of different conventional gestures displayed with a maximum of 8 (i.e., give, push away, reach, show, point, wave, head shake, head nod). Inventory of Consonants The number of different consonants produced with a maximum of 10 (e.g., b, d, g, m, n). Inventory of Words The number of different words (i.e., forms that are used referentially and that approximate conventional words, spoken or signed) produced with a maximum of 16. Understanding The sum of the number of object names out of 3 possible, person names out of 2 possible, plus body parts out of 3 possible with a maximum of 8 to measure understanding single words without gestural cues. Inventory of Actions The number of different functional actions used with objects during play with a maximum of 12. Pretend Play Actions The number of pretend actions with objects toward other (i.e., adult or stuffed animal) used during play with a maximum of 6. Stacking Blocks The number of blocks stacked to measure the ability to use one object in combination with another to construct in play with a maximum of 5. Inter-rater Reliability Inter-rater reliability for the CSBS Behavior Sample was calculated using generalizability (g) coefficients for pairs of four independent raters on randomly selected videotapes for at least 20% of the samples scored by each rater. G coefficients that are at least .60 are considered acceptable for demonstrating inter-rater reliability (Mitchell, 1979). Rater one scored the largest number of samples and therefore was considered the expert to which the other raters were compared.

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The g coefficients for the social communication measures ranged from .76 to 1.00, with an average of .91, indicating that the raters exhibited high inter-rater reliability.

Results Group Differences in Social Communication Measures The mean scores on each of the social communication measures from the CSBS Behavior Sample are presented in Table 3. A series of one-way analyses of variance (ANOVA) were conducted to evaluate group differences using a Welch correction for lack of homogeneous variances. Significant group differences were found for all 14 social communication measures. Post-hoc tests were conducted using Dunnet T3 method to evaluate pairwise differences among means. There were significant differences between the ASD and TD groups with large effect sizes on all 14 measures. There were significant differences between the ASD and DD groups with large effect sizes on gaze shifts, gaze/point follow, rate of communicating, and acts for joint attention and a significant difference with a medium effect size on inventory of conventional gestures. There were non-significant differences between the ASD and DD groups with medium effect sizes on shared positive affect, acts for social interaction, and pretend play actions and with small or minimal effect sizes on acts for behavior regulation, inventory of consonants, inventory of words, understanding, inventory of play actions, and stacking blocks. Intercorrelations among the Social Communication Measures for the ASD Group To examine concurrent relations among the social communication measures, Pearson product-moment correlation coefficients controlling for the effects of age were computed for the ASD group and are presented in Table 4. As expected, moderate to large correlations were observed among most of the social communication measures. Large correlations were observed between gaze shifts and shared positive affect but small correlations were found between each of these measures and measures in the speech and symbolic composite. Small to moderate correlations were observed between acts for social interaction and all other measures, except understanding, for which a large correlation was found. Additionally, small

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Table 3 Group differences in social communication measures Social communication measures

Social composite Gaze shifts Shared positive affect Gaze/point follow Rate of communicating Acts for behavior regulation Acts for social interaction Acts for joint attention Inventory of gestures Speech composite Inventory of consonants Inventory of words Symbolic composite Understanding Inventory of play actions Pretend play actions Stacking blocks

ASD (n = 50)

DD (n = 23)

TD (n = 50)

F-value

Pairwise group differences DD-ASD

TD-ASD p value

Effect sized

1.00 0.50 0.91 0.83 0.29 0.66 1.05 0.67

.000 .000 .000 .000 .000 .000 .000 .000

1.56 1.21 2.31 2.00 1.09 1.18 2.08 1.98

.363 .681

0.39 0.24

.000 .000

1.57 1.36

.950 .243 .138 .546

0.12 0.42 0.51 –0.29

.000 .000 .000 .000

1.65 1.61 1.66 0.98

M

SD

M

SD

M

SD

p value

4.02a 2.24a 0.66a 10.60a 4.50a 0.86a 1.30a 2.64a

2.06 1.73 0.82 5.34 1.58 1.31 1.73 1.47

5.48b 3.13ab 1.39b 14.65b 4.91a 1.83ab 3.35b 3.70b

0.85 1.82 0.78 4.42 1.20 1.64 2.17 1.71

5.88b 4.20b 1.92c 17.46c 5.68b 2.70b 4.52b 5.24c

0.33 1.51 0.27 1.52 0.59 1.81 1.36 1.15

21.55*** 18.10*** 54.81*** 40.58*** 14.86*** 17.16*** 52.95*** 48.99***

.000 .154 .002 .004 .529 .052 .001 .044

1.84a 1.42a

2.17 3.25

2.74a 2.13a

2.47 2.58

5.30b 7.50b

2.23 5.69

31.47*** 21.99***

1.68a 4.30a 1.24a 3.10a

2.49 2.59 1.52 1.80

1.96a 5.30a 2.00a 2.61a

2.21 2.16 1.48 1.53

5.76b 7.42b 3.44b 4.54b

2.48 1.28 1.13 1.15

39.01*** 33.67*** 35.32*** 20.68***

Effect size

d

Note: Means in the same row with different subscripts differ significantly at p < .05 on the post-hoc Dunnet T3 corrected comparison F-values are Welch corrected when necessary for violation of homogeneity of variance as assessed by Levene’s test d

Effect size based on Cohen’s d ‡ .20 is small, .50 is medium, and .80 is large

* p < .05, ** p < .01, *** p < .001 Table 4 Intercorrelations among the social communication measures for the ASD group (n = 50) Social communication measures 1 Social composite 1. Gaze shifts 2. Shared positive affect 3. Gaze/point follow 4. Rate of communicating 5. Acts for behavior regulation 6. Acts for social interaction 7. Acts for joint attention 8. Inventory of gestures Speech composite 9. Inventory of consonants 10. Inventory of words Symbolic composite 11. Understanding 12. Inventory of play actions 13. Pretend play actions 14. Stacking blocks

2

3

4

.71*** .29* .47** .37** .28 .51*** .45**

.18 .51*** .35* .28* .45** .37**

.36* .36* .21 .37** .50***

.87*** .45** .18 .74*** .58*** .44** .66*** .66*** .32*

.34* .16

.28* .11

.48*** .65*** .54*** .42** .48** .48** .32* .46**

.60*** .61*** .54*** .46** .86***

.13 .26 .29* .18

.18 .32* .34* .21

.61*** .52*** .40** .21

.61*** .55*** .71*** .35*

.54*** .68*** .69** .44**

5

6

.38** .68*** .58*** .45**

.55*** .28* .33* .09

7

8

9

10

11

12

13

.67***

.58*** .62*** .64*** .41**

.52*** .60*** .60*** .46*

.59*** .44** .51*** .54*** .60*** .75*** .21 .28* .45** .38**

Note: Intercorrelations are Pearson partial correlation coefficients controlling for age * p < .05, ** p < .01, *** p < .001

correlations were observed between stacking blocks and gaze/point follow, inventory of words, and understanding. Predictive Relations with Developmental Outcome To examine predictive relations between early social communication measures and developmental outcome

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at 3 years, bivariate correlations between the social communication measures gathered in the second year of life and nonverbal and verbal DQ were computed for children in the ASD group who had a MSEL completed at 36 months of age or older (n = 42). Pearson correlation coefficients controlling for the effects of age are presented in the left two columns of Table 5. Individual variation on all of the social

J Autism Dev Disord (2007) 37:960–975 Table 5 Correlations among the social communication measures in the second year and nonverbal and verbal DQ at 3 years of age for children with autism spectrum disorder (n = 42)

Note: Nonverbal and Verbal Developmental Quotients (DQ) are based on age equivalent divided by chronological age multiplied by 100 on the Mullen Scales of Early Learning * p < .05, ** p < .01, *** p < .001

Social communication measures

Social composite Gaze shifts Shared positive affect Gaze/point follow Rate of communicating Acts for behavior regulation Acts for social interaction Acts for joint attention Inventory of gestures Speech composite Inventory of consonants Inventory of words Symbolic composite Understanding Inventory of play actions Pretend play actions Stacking blocks

communication measures except gaze shifts, shared positive affect, and acts for social interaction was found to correlate significantly with nonverbal DQ at 3 years of age. Similar patterns of effect size and level of significance were found for verbal DQ except that a moderate significant relation was observed between verbal DQ and acts for social interaction. Additionally, inventory of conventional gestures showed a larger correlation with nonverbal DQ and inventory of words with verbal DQ. The large, significant correlation observed between understanding and both nonverbal and verbal DQ suggests that this is the best indicator of developmental level measured in the second year. Therefore, the relationship between the other social communication measures and DQ while controlling for understanding and age was explored and the partial correlations are presented in the right two columns of Table 5. When controlling for age and understanding, nonverbal DQ was predicted by rate of communicating, acts for behavior regulation, inventory of gestures, inventory of consonants, inventory of play actions, and stacking blocks; verbal DQ was predicted by acts for behavior regulation and inventory of consonants. Predictive Relations with Severity of Autism Symptoms To examine predictive relations between early social communication abilities and autism symptoms at 3 years, bivariate correlations between the social

969 Controlling for age

Controlling for age and understanding

Nonverbal DQ

Verbal DQ

Nonverbal DQ

Verbal DQ

.10 .03 .41* .56** .56*** .29 .48** .62***

.08 .01 .40* .53*** .44** .39* .48** .42**

.11 –.00 .15 .37* .50** –.13 .19 .46**

.08 –.03 .09 .31 .35* –.02 .17 .14

.58*** .44**

.57*** .53***

.39* .08

.35* .18

.62*** .52** .45** .51**

.67*** .45** .51** .32*

.36* .18 .45**

.24 .25 .20

communication measures gathered in the second year of life and severity of autism symptoms based on the ADOS algorithm totals for the communication and social interaction domains were examined. It should be noted that higher ADOS scores indicate more severe symptoms of autism. Correlations were computed for the ASD (n = 48) and DD (n = 22) groups combined to examine the relations between early social communication measures in children with communication delays and severity of autism symptoms at 3 years of age and are presented in the left two columns of Table 6. Significant negative correlations were observed between all of the early social communication measures and the communication and/or social interaction ADOS algorithm totals at 3 years of age with the exceptions of inventory of words, understanding, and stacking blocks. Correlations were also computed for the ASD group only and are presented in the right two columns of Table 6. Significant negative correlations were observed between the following six early social communication measures and the communication total on the ADOS—rate of communicating, acts for behavior regulation, inventory of gestures, inventory of consonants, inventory of play actions, and pretend play actions. Only acts for behavior regulation and inventory of gestures were significantly related to the social interaction total on the ADOS. The smaller correlations with the ASD group only are expected given the more limited variance both in the early social communication measures and the ADOS scores within this group than the combined groups.

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970 Table 6 Correlations among the social communication measures in the second year and autism symptoms at 3 years of age for children with ASD (n = 42) and DD (n = 22)

* p < .05, ** p < .01, *** p < .001

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CSBS DP

Social communication measures Social composite Gaze shifts Shared positive affect Gaze/point follow Rate of communicating Acts for behavior regulation Acts for social interaction Acts for joint attention Inventory of gestures Speech composite Inventory of consonants Inventory of words Symbolic composite Understanding Inventory of play actions Pretend play actions Stacking blocks

Discussion This prospective, longitudinal study examined social communication measures of children with ASD late in the second year of life with a mean age of 21.36 months (SD = 1.90) in comparison to children with DD and TD and in relation to outcomes at 3 years of age. This discussion highlights the core social communication deficits in these children with ASD and predictive relations of social communication in the second year with developmental level and severity of autism symptoms at 3 years of age. Implications for improving early identification and understanding early social communication development in ASD are discussed.

Core Social Communication Deficits in Children with ASD Late in the Second Year The children with ASD scored significantly lower than the age-matched children in the TD group on all social communication measures. These results are based on a larger sample than previous research and confirm previous findings that social communication deficits are evident in children with ASD between 18 and 24 months of age. These findings demonstrate that deficits in social communication in children with ASD under 2 years of age can be detected on standardized measures of social communication using systematic observation, such as the CSBS, which has important implications for improving early identification. This is a particularly

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ADOS algorithm totals ASD and DD groups

ASD group only

Communication

Social interaction

Communication

Social interaction

–.32** –.28* –.35** –.45*** –.34** –.29* –.39** –.39**

–.32** –.17 –.41*** –.39** –.28* –.21 –.39** –.39**

–.17 –.19 –.11 –.35* –.40** –.02 –.14 –.36*

–.08 .03 –.12 –.22 –.34* .12 –.05 –.32*

–.40** –.20

–.30* –.19

–.34* –.10

–.18 –.10

–.08 –.42*** –.43*** –.02

–.08 –.32** –.34** –.04

–.02 –.38* –.38* –.05

–.09 –.26 –.26 .03

important finding given that more than half of the ASD group in this study was high functioning. Compared to children with DD matched on age and developmental level, children with ASD performed significantly lower on five social communication measures—gaze shifts, gaze/point follow, rate of communicating, acts for joint attention, and inventory of conventional gestures. All of these skills have been found to distinguish older preschool children with ASD from children with DD and TD (Mundy et al., 1990; Stone et al., 1997; Wetherby et al., 1998; Dawson et al., 2004). These findings suggest that these five social communication skills are core deficits of ASD in the second year of life and should be evident by 18– 24 months of age. The findings of Wetherby et al. (2004) and Werner et al. (2005) suggest that repetitive behaviors and restricted interests are also likely to be evident at this age or earlier. Future research should examine more precise measures of social communication and repetitive behaviors and restricted interests in the second year to better understand the ontogeny of core deficits across domains. It is important to consider limitations of this study in interpreting findings. One limitation is that this sample was heterogeneous in developmental level and the social communication profile identified may not be the same in subgroups. It would be informative to examine social communication profiles in children with low versus high developmental levels separately. Second, the sampling procedures of the CSBS provide support to structure interactions that may limit group

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differences. The children with ASD may have used more or higher-level social communication skills during the sample than in unstructured natural environments. Additionally, the CSBS sampling opportunities and restricted range of scores may limit group differences. For example, children in all three groups used more acts for behavior regulation and joint attention than social interaction, and therefore, there may have been insufficient opportunities to detect differences between the ASD and DD groups on acts for social interaction. Finally, matching the ASD and DD groups on the symbolic composite may have limited group differences on items within this composite. Wetherby et al. (1998) matched groups on expressive language and found significant differences in symbolic play between slightly older children with ASD and DD, in addition to the core deficits identified in the present study. These findings support the use of a multilevel screening and evaluation process to sift out children with ASD from a general pediatric population. It can be very challenging to inform a family that their young child has ASD, whether they recognize that their child is delayed or not. The CSBS maximizes the role of the family by having parents complete the Infant-Toddler Checklist and participate in the Behavior Sample. The CSBS can be used with a general pediatric population to inform the family that their child has a social communication delay, which puts their child at risk for ASD. For children who show the collection of core deficits identified in this study, the next step should be a systematic rating of red flags of ASD (see Wetherby et al., 2004) and/or referral for a diagnostic evaluation. It may be the combination of social communication deficits with repetitive behaviors and restricted interests that should alert professionals to consider a diagnosis of ASD. Building consensus with the family on the child’s social communication profile may be an important initial step to get a family ready to consider a diagnosis of ASD and enter early intervention. Predicting Outcomes at 3 Years from Social Communication Late in the Second Year The heterogeneity of developmental functioning in children with ASD was reflected in this sample at outcome and found to be related to individual variation in many social communication skills in the second year of life. Understanding was the strongest predictor of both nonverbal and verbal developmental outcome; however, the other social communication measures showed moderate to large correlations with developmental outcome with only two exceptions. Gaze shifts and shared positive affect were not related to devel-

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opmental outcome. For the children with ASD between 18 and 24 months, the best predictors of nonverbal skills at 3 years were understanding, rate of communicating, acts for behavior regulation, inventory of conventional gestures, inventory of consonants, inventory of conventional actions in play, and stacking blocks. The best predictors of verbal skills at 3 years were understanding, acts for behavior regulation, and inventory of consonants. For the combined group of children with communication delays (i.e., ASD and DD groups combined), all of the social communication measures from the second year predicted severity of autism symptoms at 3 years with three exceptions. Inventory of words, understanding, and stacking blocks in the second year were not related to the ADOS totals at 3 years. For the children with ASD between 18 and 24 months, the best predictors of autism symptoms in the social interaction domain at 3 years were acts for behavior regulation and inventory of conventional gestures. There was a larger set of significant predictors of autism symptoms in the communication domain which included acts for behavior regulation and inventory of conventional gestures, but also rate of communicating, inventory of consonants, inventory of conventional actions in play, and pretend play actions. The Social Communication Phenotype of ASD Late in the Second Year These findings contribute to a better understanding of the social communication phenotype of children with ASD late in the second year of life and relationships with developmental level and severity of autism symptoms at 3 years. The results suggest that social communication deficits of young children with ASD are multifaceted, with some components shared with children with DD and others unique to ASD. We will examine the following components of social communication and suggest that these are pivotal skills that through a transactional process have a cascading effect on outcomes: communicative intentions, conventional behaviors, representation, social referencing, and rate of communicating. Communicative Intentions Typical children communicate for behavior regulation, social interaction, and joint attention by the end of the first year before the emergence of words (Bruner, 1981; Wetherby & Prizant, 1993). Wetherby (1986) suggested that the easiest and first emerging communicative intention for children with autism is behavior

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regulation and the most difficult is joint attention, presumably because of the differing social underpinnings. This ontogeny has been supported by Stone and Caro-Martinez (1990) in children with ASD ranging from 4 to 13 years of age and by Wetherby et al. (1998) in 2–4 year old children. The present study extends those findings down to 18–24 months. Compared to the children with DD, these children with ASD were comparable on acts for behavior regulation, slightly lower on acts for social interaction, and significantly lower on acts for joint attention. The predictive relations between acts for behavior regulation and both nonverbal and verbal developmental outcomes as well as severity of autism symptoms in both the communication and social interaction domains suggest that this is a pivotal skill that has a cascading effect on cognitive, social, and language development in very young children with ASD. The relative strengths that children with ASD may have in communicating for behavior regulation at 18–24 months may be used to bootstrap other skills. Furthermore, communicating for social interaction to draw attention to self may be inherently easier than communicating for joint attention for children with ASD because it does not require the triadic coordination of attention between another person and an object. Dyadic coordination of shared attention may be the next step after children with ASD can communicate for behavior regulation and may be another bootstrapping mechanism to learn social contingencies. As suggested by Dawson et al. (2004), engaging more in early successful exchanges, even if only to meet environmental needs, could help children attend to the social cues of their caregivers and learn the inherent value of communicating with people, thus enhancing communication for other intentions later. Conventional Behaviors The capacity to acquire conventional behaviors is triggered by children using active learning strategies that involve exploring objects, observing others, and learning in social exchange through imitation (Bates, 1979; McLean & Snyder-McLean, 1999; Meltzoff, 2004). For both inventory of conventional gestures and play actions, the ASD group had large deficits compared to the TD group and moderate deficits compared to the DD group. The predictive relations between these early conventional behaviors and both nonverbal DQ and autism symptoms suggest that these are pivotal skills that may impact cognitive and social

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development in young children with ASD. This may reflect a transactional process in that caregivers are better able to be responsive to children who initiate with conventional behaviors. Group differences in inventory of conventional gestures were greater than group differences in inventory of play actions. This is consistent with studies of imitation in children with ASD that have documented greater difficulty imitating actions without objects than with objects (McDuffie, Yoder, & Stone, 2005; Williams, Whiten, & Singh, 2004). Thus, difficulty imitating actions without objects may hinder learning conventional gestures and objects may provide a scaffold for learning conventional actions in play. Representation Like children with DD, children with ASD are delayed at 18–24 months in symbolic skills or the capacity for representation across domains. The combination of understanding, inventory of play actions, and stacking blocks was the best predictor of nonverbal representation, which suggests that boosting these early representational skills would have a positive impact on developmental outcome. However, it is noteworthy that understanding, stacking blocks, and inventory of words were independent of autism symptoms. Thus, it appears that the conventional aspect of play, not the representational aspect, is a significant predictor of autism symptoms. Both gaze/point follow and initiating joint attention were core deficits in these children with ASD at 18– 24 months and showed moderate relations with nonverbal and verbal DQ at 3 years, consistent with previous research. However, after controlling for understanding, gaze/point follow and acts for joint attention were no longer significant predictors, suggesting that it is the representational aspect of these skills that is predictive of developmental outcome. This is noteworthy considering the important role of gaze/ point follow as a predictor of later joint attention and language outcome for older children with ASD (Sigman & Ruskin, 1999) and as a potential moderator of the effects of intervention on language outcomes (Bono, Daley, & Sigman, 2004). Joint attention deficits may not have been unique predictors of outcome at this young age because so many of the children with ASD were so deficient on these skills in the second year of life. It is not until children with ASD are a little older that individual variation in joint attention skills is a unique predictor of language and other developmental outcomes.

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The ASD group was comparable to the DD group on inventory of consonants and words, suggesting that these deficits are not specific to ASD. Although a very large correlation was observed between inventory of consonants and inventory of words, only inventory of consonants was a significant predictor of nonverbal and verbal DQ, after controlling for understanding. Inventory of words was not related to developmental level or autism severity. Thus, the capacity to produce well-formed canonical syllables is another pivotal skill for these young children with ASD. While it may seem surprising that inventory of consonants would be related to representational skills and predict nonverbal DQ, caregivers are more likely to model language in response to their children’s use of canonical vocalizations; therefore, children with a larger inventory of consonants in communicative acts will likely be exposed to more words within a meaningful interaction (Yoder & Warren, 1999). Social Referencing Children with ASD in this sample showed a collection of core deficits that reflect difficulty with social referencing. By 9 months of age, typical children actively observe and shift gaze between people and objects to see if their caregiver is attending to their focus of interest (Bakeman & Adamson, 1984) and are able to coordinate gaze with the expression of emotional states to share affect. In this study, a very large correlation was found between gaze shifts and shared positive affect in the children with ASD (r = .71). These skills showed relatively small or negligible correlations with representational skills and were not significant predictors of either developmental outcome or autism symptoms. Thus, the core deficit in gaze shifts through its relationship with shared affect, communicative intentions, and conventional behavior may have a cascading effect on developmental outcome and autism symptoms. These findings are consistent with those of Dawson et al. (2004) on 3- and 4-year olds with ASD that impairments in social attention were related to joint attention but not concurrent measures of language. Rate of Communicating Rate of communicating was a core deficit of ASD at 18–24 months that reflects the combined repertoire of social communicative skills. Moderate to large intercorrelations were found between rate of communicating and all of the other social communication measures, which suggests that it is a useful index of

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initiating and responding to social bids. Rate of communicating showed moderate correlations with nonverbal and verbal DQ when controlling for understanding and with autism symptoms in the communication domain, consistent with the predictive relations reported by Charman et al. (2005) between rate of communicating and outcome at 7 years. These predictive relations may reflect a transactional process in that children with higher rates of communicating are more likely to impact their social environment by creating more opportunities for interacting and engagement. Building on previous work of Mundy and colleagues, Mundy and Burnette (2005) have eloquently presented a neurodevelopmental model of ASD. They suggested that an initial neurological deficit in infants with autism leads to an early impairment in social orienting and joint attention, which contributes to subsequent neurodevelopmental pathology by an attenuation of social input. This transactional process can lead to a cumulative spiraling that may compromise subsequent neurological and behavioral development or possibly be ameliorated through early intervention. The findings of the present study suggest that by 18–24 months of age there are five core social communication deficits of ASD—gaze shifts, gaze/ point follow, rate of communicating, acts for joint attention, and inventory of gestures. These core deficits may attenuate the quality of the social input that children with ASD are exposed to very early in life. Future research should examine social communication skills in even younger children with ASD and the relation between social communication skills and repetitive behavior and restricted interests in the second year of life to elucidate the ontogeny of autism symptoms. We have proposed that these core social communication deficits are related to a set of pivotal component skills in the second year that impacts the quality of the social environment and through a transactional process has a cascading effect on developmental outcome and autism symptoms at 3 years of age. These pivotal skills may be critical targets to consider in early intervention to enhance social communication skills that are likely to impact the social environment, and thus, lead to better outcomes for children with ASD. Acknowledgments This research was supported in part by two grants from the U.S. Department of Education, Office of Special Education and Rehabilitation Services (H324M010071 and H324C030112) and a grant from the U.S. Department of Education, Institute of Education Sciences (R305T010262). The authors would like to thank the families who gave their time to participate in this project.

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