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DOI: 10.1007/s10803-020-04364-z

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Citation for published version (APA): Taylor, L. J., Charman, T., Howlin, P. A., Slonims, V., Green, J., The PACT-G Consortium, & Emsley, R. A. (2020). Brief Report: Associations between preverbal social communication skills, language and symptom severity in children with autism: An investigation using the Early Sociocognitive Battery. Journal of Autism and Developmental Disorders, 50(4), 1434-1442. https://doi.org/10.1007/s10803-020-04364-z

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Download date: 30. Sep. 2021 RUNNING HEAD: Social communication, language and autism symptoms

Brief Report: Associations between preverbal social communication skills, language and

symptom severity in children with autism: An investigation using the Early Sociocognitive

Battery

Lauren J. Taylor1, Tony Charman1,2, Patricia Howlin1, Vicky Slonims3, Jonathan Green4,5 &

The PACT-G Consortium*

1. Department of Psychology, King’s College London, Institute of Psychiatry, Psychology

and Neuroscience, London, UK

2. South London and Maudsley NHS Foundation Trust, London, UK

3. Guy’s & St. Thomas’ NHS Foundation Trust (Evelina Children’s Hospital), Newcomen

Centre at St. Thomas’, London, UK

4. Division of Neuroscience and Experimental Psychology, University of Manchester,

Manchester, UK

5. Royal Manchester Children’s Hospital, Manchester University NHS Foundation Trust,

Manchester, UK

* Listed in Acknowledgements

** Corresponding author:

Lauren Taylor

Department of Psychology, Henry Wellcome Building

Institute of Psychiatry, Psychology and Neuroscience

King’s College London

16 De Crespigny Park

London SE5 8AF E: [email protected] P: +44 (0)20 7848 0405

Disclosure of Conflicts of Interest The Paediatric Autism Communication Trial-Generalised (PACT-G) is funded by the National Institute of Health Research (NIHR) and Medical Research Council [Efficacy and Mechanism Evaluation Programme (13/119/18)]. The authors declare that they have no conflict of interest.

Social communication, language and autism symptoms 2

Abstract We investigated the Early Sociocognitive Battery (ESB), a novel measure of preverbal social communication skills, in children with autism participating in the Paediatric Autism

Communication Trial-Generalised (PACT-G). The associations between ESB scores, language and autism symptoms were assessed in 249 children aged 2-11 years. The results show that ESB subscale scores (social responsiveness, joint attention and symbolic comprehension) were significantly associated with concurrent autism symptoms and receptive and expressive language levels. The pattern of association between the ESB subscale scores differed between the ADOS-2 symptom domains and expressive and receptive language. These findings indicate the potential utility of the ESB as a measure of preverbal social communication in children with autism.

Key words: Autism; symptom severity; language; preverbal social communication

Social communication, language and autism symptoms 3

Brief Report: Associations between preverbal social communication skills, language and

symptom severity in children with autism: An investigation using the Early

Sociocognitive Battery

In typically developing children, language learning is a social process (e.g.

Tomasello, 2000). The early emergence of interpersonal skills, such as reacting to others’ emotional expressions, gaze following, responding to bids for joint attention, and understanding the meaning of symbols (i.e., words, gestures, images that convey meaning), play a key role in later communication development (Morales et al., 2000; Mundy, Sigman,

& Kasari, 1990; Tomasello, 1988) and underpins early word learning (Chiat, 2001; Chiat &

Roy, 2008). These pivotal skills are often impaired in young children with autism and delayed development in this area is associated with poor language outcomes (e.g. Bottema-

Beutel, 2016; Dawson et al., 2004; Murray et al., 2008) and more severe social communication difficulties in this population (e.g., Charman, 2003).

Extensive research has been dedicated to understanding early social communication skills and their association with language acquisition in autism (e.g. Charman, 2003; Mundy et al., 1990; Mundy, Sigman, & Kasari, 1994). These studies have often used experimental paradigms to measure early social communication in infants and young children (Charman et al., 1998; Sigman, Kasari, Kwon, & Yirmiya, 1992; Tomasello, Striano, & Rochat, 1999).

The experimental paradigms have been refined to create a range of standardised measures of early social communication, such as the Communication and Symbolic Behaviour Scales

(CSBS; Wetherby & Prizant, 2002), the Early Social Communication Scales (ESCS; Seibert,

Hogan, & Mundy, 1982) and Short Play and Communication Evaluation (SPACE; Shire,

Shih, Chang, & Kasari, 2018). While these assessments measure the expression of nonverbal social communication, i.e., observable behaviours that indicate social interaction, requesting, Social communication, language and autism symptoms 4 joint attention (both initiation of and response to joint attention) and symbolic play skills, the assessments do not measure social responsiveness or the child’s comprehension of symbols such as gesture. These latter skills are particularly important in the context of assessing children with autism, as delayed language development, at least in a sub-set of this population, may represent a fundamental impairment in complex symbolic function (Ricks &

Wing, 1975; Wing & Wing, 1971).

Furthermore, currently available social communication scales have been developed for infants and young children and are not standardised for older children with autism. While early social communication skills have rarely been measured in minimally verbal school-aged children with autism, there is an emerging body of research indicating that there may be a different pattern of association between early communication skills and language development in school-aged children with autism as compared to very young children (Bean

& Eigsti, 2012; Pecukonis, Plesa Skwerer, Eggleston, Meyer, & Tager-Flusberg, 2019). For example, the results of two recent studies of response to joint attention indicate that this skill was associated with receptive (Bean & Eigsti, 2012), but not expressive (Pecukonis et al.,

2019) language in school-aged children and adolescents with autism (aged 7-19 years). These findings indicate that associations between preverbal social communication skills and language may vary for subgroups of people with autism. Few studies have investigated early social communication skills in older children with autism, yet this work is important to understand possible barriers to language acquisition in these children.

To begin to address this gap in the literature, we included the Early Sociocognitive

Battery (ESB; Roy & Chiat, 2019) as a baseline measure of preverbal communication skills in the Paediatric Autism Communication Trial-Generalised (PACT-G; see Green et al., 2018;

Green et al., 2010 for details of the original trial). The ESB is a novel measure of the early emerging skills of social responsiveness, joint attention and symbolic comprehension and Social communication, language and autism symptoms 5 builds on experimental paradigms that have previously been used to measure early social communication in children with autism (e.g., Sigman et al., 1992; Tomasello et al., 1999).

The ESB has advantages over other measures of early social communication skills, as it is brief, can be administered nonverbally, requires no verbal response and includes subscales that measure social responsiveness and symbolic comprehension. The predictive validity of the ESB has been measured in a longitudinal study of children referred to clinical services for early language difficulties, but not autism. In that study, ESB scores at age 2 ½-4 (T1, N =

181) years were used to predict language and social communication outcomes 18-months later (at age 4-5, N = 163) years and again at age 9-11 years (N = 108) (Chiat & Roy, 2008,

2013; Roy & Chiat, 2019). The results indicated that ESB scores predicted language expression and comprehension (Preschool Language Scales scores) and social communication skills (Peer-Prosocial and Pragmatic composite scores from the Strengths and

Difficulties Questionnaire and Children’s Communication Checklist-2, respectively) at T2

(Chiat & Roy, 2008). ESB scores also predicted longer-term social communication outcomes

(Social Responsiveness Scale (SRS; Constantino & Gruber, 2005) scores) and parent- reported ‘late’ autism diagnoses at T3 for children with early language difficulties (Chiat &

Roy, 2013; Roy & Chiat, 2019). In community samples of typically developing children,

ESB scores were positively correlated with scores on the British Picture Vocabulary Scale-3rd

Edition (r = .35-.41, p < .001) (BPVS-3 Dunn, Dunn, & Styles, 2009), thus demonstrating concurrent validity. The measure has good test-retest (ICC = .95) and interrater (ICC = .90-

.95) reliability (Chiat & Roy, 2008; Roy & Chiat, 2019). Sensitivity and specificity have also been established for outcomes including contact with clinical services at T2 (sensitivity = .80, specificity = .86) and social communication problems (SRS scores)/parent-reported autism diagnosis at T3 (sensitivity = .89, specificity =.75) (Chiat & Roy, 2013; Roy & Chiat, 2019). Social communication, language and autism symptoms 6

While Chiat and Roy (2008) have previously investigated ESB scores in a community sample of typically developing 2-4-year-old children and a sample of children referred to clinical services for language difficulties, the ESB has not been used either to examine preverbal social communication in children with autism, or to explore these skills in middle childhood. Therefore, in this study, we investigated the associations between ESB scores, language, autism symptom severity and nonverbal ability in the PACT-G sample. Based on previous research that showing that low levels of early social communication skills are associated with later language and social communication outcomes (Chiat & Roy, 2013; Roy

& Chiat, 2019), we hypothesised that the ESB subscale scores for social responsiveness, joint attention and symbolic comprehension would predict expressive and receptive language levels and autism symptoms in our sample.

Method

Participants

Two hundred and forty nine (197 male, 52 female) children, aged between 2 and 11 years, were recruited to the Paediatric Autism Communication Trial-Generalised (see Green et al., 2018; Green et al., 2010, for the PACT-G trial protocol and a full description of PACT therapy, as described in our original study) between January 2017 and April 2018. PACT-G is a multisite, randomised controlled trial of a social communication intervention for children with autism, taking place in South London, Greater Manchester and the North-East of

England. At all sites, children who were younger than 5 years at baseline were recruited via referral from local paediatric, mental health and speech and language therapy services, and those who were 5 years or older either from special schools, or by referral from local clinical services. Children included in the trial met the following criteria:

• Confirmed diagnosis of autism, obtained from community-based clinical services; Social communication, language and autism symptoms 7

• Met the ‘Autism’ cut-off on the Autism Diagnostic Observation Schedule-2nd

Edition (ADOS-2; Lord et al., 2012) and scored ≥12 (children younger than 5

years) or ≥15 (children 5 years or older) on the Social Communication

Questionnaire (SCQ; Rutter, Bailey, & Lord, 2003);

• Nonverbal age equivalent scores of more than 12 months, measured using the Fine

Motor and Visual Reception subscales of the Mullen Scales of Early Learning

(MSEL; Mullen, 1995), or the Special Nonverbal Composite Score on the British

Ability Scales-School Age (BAS; Elliott & Smith, 2011);

• Children who were aged 5 years and older were between P3 and P8 on the English

curriculum1;

• The child’s nursery, school or education provider agreed to take part in the study.

While families spoke a range of additional languages, they were required to have enough

English to potentially participate in the intervention, and speak English to their child, at least some of the time. Children with epilepsy were included if this was controlled by medication.

Children and/or parents with significant hearing or visual impairments were excluded as were parents with severe learning disability or psychiatric disorder. Child characteristics are presented in Table 1. All parents provided informed, written consent before taking part in

PACT-G.

[Insert Table 1 about here]

Procedure and Measures

The data were collected at baseline, prior to randomisation and the delivery of any trial intervention. Assessments were administered over three or four sessions conducted at home, school and clinic or research lab. Child assessments (ADOS-2, MSEL, BAS, One

1 In England, the P scales supplement the national curriculum by describing targets for children aged 5-16 years with special educational needs. Children at P3 are beginning to communicate with intent and P8 represents a language age equivalent of approximately 4 years in a typically developing child. Social communication, language and autism symptoms 8

Word Picture Vocabulary Tests (Martin & Brownell, 2011a, 2011b), ESB), were usually administered in the clinic or research laboratory but could also be administered at home or school. Parent interviews (Vineland Adaptive Behavior Scales-2nd Edition; Sparrow,

Cicchetti, & Balla, 2005) were administered either at the home or research laboratory; parent questionnaires were usually completed between visits.

Autism Symptomatology. The Autism Diagnostic Observation Schedule-2nd Edition

(ADOS-2; Lord et al., 2012) is a semi-structured assessment of the social communication symptoms and restricted, repetitive and stereotyped behaviours that characterise autism.

Subscale total scores for Social Affect (SA) and Restricted and Repetitive Behaviour (RRB) can be used to calculate calibrated domain scores, which are standardised according to the child’s age and verbal ability (Hus, Gotham, & Lord, 2014) .

Nonverbal Ability. The visual reception and fine motor subscales from the MSEL, and the nonverbal composite score from the BAS were used as measures of nonverbal ability. As our sample included children older than 5 years, who were thus outside the age range to derive standard scores, we used the age equivalent scores from the MSEL to create a nonverbal developmental quotient (NVDQ; nonverbal mental age equivalent/chronological age * 100).

Language Skills. Language was assessed using a range of parent-report and researcher- administered assessments. The Expressive and Receptive One Word Vocabulary Tests

(Martin & Brownell, 2011a, 2011b) provided a direct measure of the child’s vocabulary.

Parent-reported receptive and expressive vocabulary scores were obtained from the Words and Gestures and Words and Sentences forms from the MacArthur-Bates Communicative

Development Inventories (MCDI; Fenson et al., 1994). We also used the Receptive and

Expressive Communication subdomain scores from the Vineland Adaptive Behavior Scales-

2nd Edition-Survey Interview Form (VABS-II; Sparrow et al., 2005) to measure the child’s adaptive communication skills. Social communication, language and autism symptoms 9

Early Sociocognitive Battery (ESB; Roy & Chiat, 2019). The ESB measures three sets of socio-cognitive skills:

1. Social Responsiveness: The researcher demonstrates a series of scenarios, e.g.,

banging her finger with a hammer, during which she expresses facial expressions that

represent six different emotions (hurt, surprise, frustration/anger, fear, distraction,

achievement). The child’s response to the emotional expression is measured by the

duration of looks to the face, either fleeting (1 point), or for at least two seconds (2

points), (maximum total score 12).

2. Joint attention: The researcher has six plastic eggs, which she opens, one at a time, to

show the child a small object. Larger versions of these objects are placed behind and

around the child and the researcher directs the child’s attention to these objects using

either eye gaze or pointing paired with the verbal cue, “I brought my [object] today.”

The child’s responses are scored based on whether they alternate gaze between the

small object and the researcher’s face (1 point), and whether they follow the

researcher’s direction of gaze (2 points) or point (1 point) to the larger object

(maximum total score 18).

3. Symbolic Comprehension: This task comprises three symbolic conditions that

measure the child’s understanding of gesture, miniature objects and substitute objects.

For each activity, the researcher uses a form of symbolic representation to indicate

which one of six objects the child should find. The child then selects the

corresponding object, scoring one point for each correct object selected (total score

18).

The ESB was administered and scored live by postdoctoral research associates and research assistants who had been trained in the measure by the test developers. Training consisted of a one-day workshop after which, research staff were expected to video-record one Social communication, language and autism symptoms 10 administration of the ESB and return the tape to the trainers, for feedback on the fidelity of administration and reliability of coding.

Statistical Analysis

Data were prepared and analysed using Stata 15 (StataCorp, 2017). Since many of the children were either at basal on the expressive and receptive language measures, or outside the normative age range of the measure (e.g., the MCDI), raw scores were used for all

2 analyses . There were strong correlations between scores on the receptive (.65 < rs < .69, p <

.01) and expressive (.82 < rs < .87, p < .001) language measures, so we created receptive and expressive language composite scores from the Vineland, MCDI and OWPVT prior to any analysis. These composites were created by first transforming the raw scores for each measure into z-scores to ensure that they were measured on a comparable scale, then taking the mean of the standardised scores to derive the composites.

Several of the variables did not follow a normal distribution (see Supplementary

Figures F1-F3 for distributions of the ESB subscale scores), so we used nonparametric tests

(Spearman’s rank correlations) to examine the associations between age, nonverbal ability, language and ADOS-2 SA and RRB domain scores. We calculated the ADOS-2 calibrated domain scores based on Hus et al. (2014) and examined the SA and RRB subscales separately as previous studies have shown differential associations between joint attention and empathic responding and the social and repetitive behaviour domains of autism (e.g. Charman, 2003;

Mundy et al., 1994). We subsequently ran a series of multiple linear regression analyses to investigate whether ESB subscale scores predicted concurrent receptive and expressive language levels and autism symptom severity. Due to the strong positive associations between nonverbal ability and ESB subscale scores (see Supplementary Table S1 for full correlation matrix), NVDQ was entered as a predictor into the regression analyses. In

2 The raw scores provide an indication of language level, rather than language ability relative to chronological age. Social communication, language and autism symptoms 11 checking that the data met the assumptions for linear regression, we found that chronological age and nonverbal ability did not meet the assumption of linearity (i.e. the relationship between these variables and the outcome variables was not linear). Thus, these two variables were log transformed and the resulting variables entered into each of the regression models.

ESB subscale total scores for social responsiveness, joint attention and symbolic comprehension were entered as predictor variables along with the transformed variables for age and NVDQ. Outcome variables were ADOS-2 SA and RRB calibrated domain scores and the receptive and expressive language composite scores. All ESB subscales were completed for 231 children and these data were included in the regression analysis.

Results

Descriptive statistics for all measures are presented in Table 2.

[Insert Table 2 about here]

The results of the regression analyses showed that, while the models for both autism SA,

(F(5, 225) = 6.09, p <.001, R2 = .119) and RRB (F (2, 225) = 3.79, p = .0026, R2 = .078) scores were significant, the pattern of association between the variables differed across symptom domains (See Table 4). While joint attention was significantly associated with concurrent ADOS SA scores, only symbolic comprehension showed an association with

ADOS RRB scores (Table 3). Lower ESB subscale scores were associated with higher

ADOS-2 scores (i.e., more symptoms), for both SA and RRB domains. The regression models for receptive, (F(2, 225) = 73.97, p < .001, R2 = .62), and expressive, (F(2, 225) =

64.94, p < .001, R2 = .59), language were also significant (See Table 4). Chronological age, nonverbal ability and social responsiveness showed significant associations with both receptive and expressive language. While ESB joint attention was significantly associated with receptive, but not expressive language, symbolic comprehension showed the opposite pattern, showing a significant association with expressive, but not receptive language. Higher Social communication, language and autism symptoms 12

ESB subscale scores were associated with higher language levels for both receptive and expressive language.

[Insert Tables 3 and 4 about here]

Discussion

We investigated autism symptom severity and language in relation to preverbal social communication skills in children with autism participating in the PACT-G study. Consistent with our hypothesis, ESB subscale scores were associated with current language levels and autism symptoms. However, the pattern of associations between each of the ESB subscales and the outcome variables differed. Overall, the findings converge with a large body of previous research showing that preverbal social communication skills are related to autism symptom severity and delayed receptive and expressive language development in young and minimally verbal school-age children with autism (e.g. Baron-Cohen, Baldwin, & Crowson,

1997; Bigham & Bourchier-Sutton, 2007; Charman, 2003; Dawson et al., 2004; Murray et al.,

2008; Pecukonis et al., 2019; Sigman et al., 1992; Thurm, Lord, Lee, & Newschaffer, 2007;

Ungerer & Sigman, 1981).

Regarding the associations between ESB subscale scores and autism symptoms, we found that only joint attention was related to the ADOS-2 SA domain, and only symbolic comprehension to ADOS-2 RRB domain scores. There is longstanding evidence indicating that joint attention is associated with the social communication symptoms, but not the repetitive behaviours characteristic of autism (e.g. Charman, 2003; Delinicolas & Young,

2007; Mundy et al., 1994). This suggests that the core difficulties with joint attention drive some of the social communication symptoms of autism. Our findings also indicate that poor symbolic comprehension could contribute to the repetitive and stereotyped behaviours observed in autism. These behaviours have consistently been linked to difficulties with symbolic skills (e.g. Watt, Wetherby, Barber, & Morgan, 2008), suggesting that, rather than Social communication, language and autism symptoms 13 demonstrating pretence, children with poor symbolic comprehension tend to use objects in a repetitive or stereotyped way. Overall, the differential pattern of association between ESB subscale scores and social and repetitive symptoms of autism may suggest that distinct mechanisms underlie the social communication and repetitive behaviour domains and that these two symptom domains follow different developmental trajectories (e.g. Charman,

2003).

Our results indicate that the preverbal social communication skills of social responsiveness, joint attention and symbolic comprehension are differentially associated with receptive and expressive language in children with autism. For example, scores on the social responsiveness scale were associated with both receptive and expressive language levels.

While this finding is consistent with several previous studies, it has been suggested that social responsiveness is indirectly associated with language via its association with joint attention

(e.g. Dawson et al., 2004). We did not test this hypothesis, but we did find that response to joint attention was significantly associated with receptive, but not expressive language. It is well established that response to joint attention is a necessary precursor to receptive language, as children need to understand others’ intentions and use the direction of a speaker’s gaze to correctly map novel words onto novel objects (Baron-Cohen et al., 1997; Tomasello, 2000).

Children with autism have been shown to use alternative, less effective strategies to learn new words (Baron-Cohen et al., 1997), so it is unsurprising that, in our sample, those with low scores on the ESB joint attention subscale also had low receptive language. This finding is also consistent with recent cross-sectional results reported by Pecukonis et al. (2019), who found that joint attention was not significantly associated with concurrent expressive language in a sample of minimally verbal children and adolescents (aged 5-19 years) with autism. However, Pecukonis et al. (2019) did not examine the associations between joint attention and receptive language and we are unable to establish whether our finding of joint Social communication, language and autism symptoms 14 attention as a significant predictor of receptive language levels is consistent with this recent work. Interestingly, there was evidence of poor symbolic comprehension in our sample, which converges with several early studies that showed poor understanding of gesture in children with autism. This difficulty appears to be particularly pronounced in those with no speech (e.g. Bartak, Rutter, & Cox, 1975; Wing & Wing, 1971). In our sample, symbolic comprehension predicted expressive language, suggesting that this may be a core deficit associated with delayed language development, at least in a subset of children with autism

(Ricks & Wing, 1975). Overall, our findings highlight the multi-faceted nature of language development in autism, where a range of social communication and developmental factors may interact to contribute to language delays in this population.

Our results suggest that there is at least a subgroup of children with autism who have difficulties with preverbal social communication skills in middle childhood. One explanation for this finding is that these difficulties are driven by low nonverbal ability or global developmental delays. The results of previous studies of joint attention in children aged less than four years, show differential patterns of joint attention difficulties based on developmental level and IQ. For example, Mundy et al. (1994) showed that while children with autism and a developmental age of less than 20 months had difficulties using eye contact, following eye gaze and pointing, these difficulties were not present in children with autism who had a developmental age beyond 20 months. In contrast, the results of recent studies that have investigated associations between cognitive ability and joint attention in minimally-verbal school aged children with autism have been mixed, with some findings showing no associations (Bean & Eigsti, 2012) and others indicating that joint attention is related to verbal- and nonverbal ability (Johnson Harrison, Lu, McLean, & Sheinkopf, 2016).

We also found that nonverbal ability was significantly associated with all the ESB subscale scores, thus our results are consistent with these latter findings and suggest that low preverbal Social communication, language and autism symptoms 15 social communication skills in the PACT-G sample may reflect global developmental delays.

Nevertheless, measuring preverbal social communication skills in these children may provide insight into the persistent nature of language impairments in older children with autism.

The results of our study could reflect limitations of the ESB as a measure of preverbal skills in children with autism. The ESB has not previously been validated for typically developing children who are older than four, or for children with autism, thus we are unable to compare the scores for our sample to any published norms. The measure was developed for young children, and, while a good proportion of our sample was developmentally at the age for which the assessment has been developed and normed, it is possible that the materials were not interesting or engaging for our older children. In addition, some of the children in our sample were quite active and had limited attention, which at times interfered with the administration of the assessment. Thus, low scores on the ESB could reflect difficulties with the children’s attention and engagement, rather than low preverbal social communication skills. Furthermore, evidence from previous studies indicates that the social context can influence social responsiveness and joint attention in children with autism (Dawson &

Adams, 1984; Dawson & Galpert, 1990; Lewy & Dawson, 1992). Hence the ESB may have failed to capture the early social communicative behaviours of some PACT-G children in the assessment context even though these skills may have been present in naturalistic social interactions.

This study is the first to investigate preverbal social communication in children with autism using the ESB and the findings provide insight into the potential utility of the measure for understanding early social communication problems in children with autism. The ESB offers advantages over other measures of early social communication skills, such as the

CSBS (Wetherby & Prizant, 2002), and the ESCS (Mundy et al., 2003) as it is a brief, largely nonverbal assessment, requiring minimal verbal comprehension and no verbal response. The Social communication, language and autism symptoms 16

ESB also covers a wider age range than these other measures, which have been developed and standardised for use in typically developing infants up to the age of 30-months. Thus, they may produce ceiling effects in preschool-aged children with autism who have language skills above the 30-month level. In addition, while these measures include tasks that assess elicited or spontaneous symbolic play acts, they do not include tasks that assess the child’s understanding of symbols such as gesture. Impaired symbolic skills are considered to be a core area of difficulty in autism that makes an important contribution to language acquisition or impairment in this population (Ricks & Wing, 1975). Thus, further investigation of symbolic comprehension, using measures such as the ESB, may enhance our understanding of expressive language development in children with autism.

In sum, our findings suggest that preverbal social communication skills may be important intervention targets in children with autism through to middle childhood. And, while we do not yet know whether the ESB is sensitive to change in preverbal social communication skills over time, it is possible that, in the future, this assessment could be used to detect changes in early emerging skills that are not typically captured in direct assessments of language. Future intervention studies could include the ESB as an outcome measure to examine whether this assessment is both sensitive to change and a predictor of differential response to therapies that aim to improve preverbal social communication and expressive language in children with autism.

Social communication, language and autism symptoms 17

Ethical approval

All procedures performed in this study involving human participants were in accordance with the ethical standards of the North West – Greater Manchester Central Research Ethics

Committee (REF: 15/NW/0912) and the study complies with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Social communication, language and autism symptoms 18

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Table 1. Demographic characteristics of PACT-G sample (N = 249)

N (%) Mean SD Min Max Age (Years; Months) 5; 9 1; 5 2; 9 10; 11 Ethnicity White-British 136 (55) White non-British 13 (5) Mixed/Multiple ethnic backgroundsa 23 (9) Asian/Asian-British 31 (12) Black/African/Caribbean/Black British 40 (16) Other ethnic groupb 6 (2) Parent Marital Status Single 40 (16) Married/Cohabiting 190 (76) Separated/Divorced 18 (7) Parent Education At least one parent with post-16 education 105 (42) Family Size Number of Children 2.04 .89 1 6 Number of Adults 2.0 .86 1 7 Socioeconomic Status† 35 (14%) NVDQc 249 (100%) 48.53 18.68 12.52 111.98 ADOS-2 CSS 7.39 1.26 6 10 VABS-II Receptive Language (Years; Months) 1; 6 0; 10 0; 0 7; 6 VABS-II Expressive Language (Years; Months) 1; 6 0; 11 0; 2 5; 10 Note: a. Includes mixed white and black Caribbean, white and black African, white and Asian, and any other mixed backgrounds. b. Includes Arab. c. NVDQ was based on Mullen scores for n = 247 and the BAS for n = 2.

NVDQ Nonverbal Developmental Quotient; ADOS CSS Autism Diagnostic Observation Schedule-2nd Edition

Calibrated Severity Score; VABS-II Vineland Adaptive Behavior Scales, Second Edition. † Dichotomised as at least one parent in professional or administrative occupations (NS-SEC classes 1-3) versus all others.

Social communication, language and autism symptoms 25

Table 2. Number of participants (total N = 249), mean, SD, minimum and maximum raw scores for the Early Socio-cognitive Battery, ADOS-2 SA and RRB calibrated domain scores and language measures.

N Mean SD Min Max

Early Socio-cognitive Battery Subscale Total Scores

Social Responsiveness 241 2.69 3.34 0 12

Joint Attention 240 6.22 5.27 0 18

Symbolic Comprehension 232 4.62 4.68 0 18

ADOS-2 Social Affect Calibrated Domain Score

Module 1 (Few/no words) 110 7.29 1.43 4 10

Module 1 (Some words) 77 7.54 1.47 4 10

Module 2 (Phrase speech) 62 7.77 1.48 4 10

ADOS Restricted and Repetitive Behaviour Calibrated Domain Score

Module 1 (Few/no words) 110 7.69 1.22 5 10

Module 1 (Some words) 77 7.30 1.43 1 10

Module 2 (Phrase speech) 62 7.45 1.49 1 10

Language Measures (Raw Total Scores)

VABS-II Receptive Communication 249 17.24 7.28 1 36

VABS-II Expressive Communication 249 31.63 20.06 2 90

MCDI Receptive Vocabulary 239 207.25 132.05 0 396

MCDI Expressive Vocabulary 239 146.33 142.73 0 396

Receptive OWPVT 248 17.98 21.86 0 80

Expressive OWPVT 244 15.58 19.58 0 85

ADOS-2 Autism Diagnostic Observation Schedule-2nd Edition; SA Social Affect; RRB Rigid, Repetitive and Stereotyped Behaviour; VABS- II Vineland Adaptive Behaviour Scale-2nd Edition; MCDI MacArthur Bates Communicative Development Inventory; OWPVT One Word Picture Vocabulary Test.

Social communication, language and autism symptoms 26

Table 3. Regression models for NVDQ, chronological age and ESB subscale raw total scores as predictors of ADOS-2 SA and RRB calibrated domain scores

ADOS SA ADOS RRB B SE B t p ß B SE B t p ß NVDQ -.321 .405 -.79 .429 -.089 .240 .369 .65 .516 .075 Chronological Age -.583 .418 -1.39 .165 -.135 .540 .381 1.42 .157 .141 ESB Social -.019 .031 -.62 .538 -.045 .024 .028 .84 .404 .062 Responsiveness ESB Joint Attention -.070 .022 -3.16 .002 -.253 -.037 .020 -1.84 .067 -.151 ESB Symbolic -.006 .027 -.23 .820 -.020 -.060 .025 -2.40 .017 -.217 Comprehension Note: For the SA and RRB subscales of the ADOS-2, lower scores indicate fewer of the social communication difficulties and repetitive behaviours that characterise autism.

Social communication, language and autism symptoms 27

Table 4. Regression models for NVDQ, chronological age and ESB subscale raw total scores as predictors of receptive and expressive language composite scores

Receptive Language Expressive Language B SE B t p ß B SE B t p ß NVDQ 1.62 .16 10.32 <.001 .76 1.62 .18 9.07 <.001 .70 Chronological Age 1.27 .16 7.82 <.001 .50 1.25 .18 6.80 <.001 .45 ESB Social .03 .012 2.73 .007 .13 .03 .01 2.72 .007 .13 Responsiveness ESB Joint Attention .20 .009 2.22 .028 .12 .01 .010 1.20 .231 .07 ESB Symbolic .013 .01 1.20 .23 .07 .03 .01 2.50 .013 .15 Comprehension

Social communication, language and autism symptoms 28

Supplementary Information

Supplementary Table S1. Spearman’s rank correlations between ESB subscale raw total scores and measures of nonverbal ability, age, autism symptoms and language.

1. 2. 3. 4. 5. 6. 7. 8. 9.

1. Chronological Age (Months)† -

2. NVDQ -.564* -

3. ESB Social Responsiveness .157 .267* -

4. ESB Joint Attention .051 .438* .448* -

5. ESB Symbolic Comprehension .059 .478* .444* .565* -

6. ADOS-2 SA Calibrated Domain Score -.117 -.118 -.235 -.337* -.219 -

7. ADOS-2 RRB Calibrated Domain Score .060 -.155 -.069 -.206 -.200 .071 -

8. Receptive Language Composite .079 .560* .447* .542* .588* -.099 -.083 -

9. Expressive Language Composite .069 .528* .430* .489* .561* -.020 -.058 .901 -

† N = 231 *p < .01. Note: Coefficients are reported with Bonferroni-adjusted significance levels of 0.01 or less.

Social communication, language and autism symptoms 29

Supplementary Figure F1. Histogram depicting the distribution of total scores on the ESB social responsiveness subscale.

0 8

)

( 6

r d

r e

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0 0 5 10 ESB Social Responsiveness Subscale Total Score

Supplementary Figure F2. Histogram depicting the distribution of total scores on the ESB joint attention subscale.

)

(

m 0

N 0 0 5 10 15 20 ESB Joint Attention Subscale Total Score Social communication, language and autism symptoms 30

Supplementary Figure F3. Histogram depicting the distribution of total scores on the ESB symbolic comprehension subscale.

0 1

0 8

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(

p i

t r

e b

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0 0 5 10 15 20 ESB Symbolic Comprehension Subscale Total Score