Mothers of children with autism spectrum disorders: Play behaviors with infant siblings and social responsiveness

Abstract

Mother–infant interactions are a proximal process in early development and may be especially salient for children who are at risk for social difficulties (i.e. infant siblings of children with autism spectrum disorder). To inform how indices of maternal behaviors may improve parent-mediated interventions designed to mitigate autism spectrum disorder risk, the present study explored maternal social responsiveness ratings and social behaviors during dyadic play interactions. Dyads were recruited from families with at least one older child with autism spectrum disorder (high-risk group, n = 90) or families with no history of autism spectrum disorder (low-risk group, n = 62). As part of a prospective study, interactions were coded when infant siblings were 6, 9, and 12 months of age, for gaze, affect, vocalizations, and multimodal bids or responses (i.e. social smiles). Maternal social responsiveness was indexed via the Social Responsiveness Scale. Mothers in both risk groups had comparable Social Responsiveness Scale scores and social behaviors during play. Two maternal behaviors emerged as positive correlates of infant social behaviors and are thus of high relevance to parent-mediated interventions. Specifically, more maternal positive affect and the use of multimodal bids or responses were associated with more infant positive affect, vocalizations, gaze to face, and multimodal bids or responses.

Keywords

autism spectrum disorder infant sibling mother–infant interaction parent-mediated intervention social responsiveness

Families serve as the primary context for infant development and daily dyadic interactions are the proximal processes of early social development. These “building blocks” often occur within play and other daily caregiving activities. For children developing at elevated risk for social communication difficulties (i.e. infant siblings of children with autism spectrum disorder (ASD)), this context may be especially salient during the first year. In addition, in families raising children with ASD, marked difficulties in social responsiveness and communication have been documented in parents (e.g. Page et al., 2017; Parr et al., 2015). These parental difficulties create a potential barrier to care because parent-mediated interventions are now common practice when supporting children with or at risk for ASD (Green et al., 2013, 2015, 2017; Jones et al., 2017; Kasari et al., 2014b; Pickles et al., 2016; Rogers et al., 2014). Social responsiveness and communication strengths or weaknesses among mothers (or other primary caregivers) can have a direct impact on the efficacy of parent-mediated interventions (Parr et al., 2015). However, intervention studies rarely index maternal social responsiveness or communicative competencies (e.g. Kasari et al., 2014a).

To inform parent-mediated interventions, this study addressed three aims. The first aim assessed if questionnaire-based ratings of social responsivness or coded social behaviors in context are distinctly different for mothers raising infants at risk for ASD. The second aim focused on maternal behaviors and assessed if these codes were associated with social responsiveness ratings or coded infant social behaviors in context at 6, 9, or 12 months of age. The final aim of this study assessed how maternal and infant behaviors may be distinct across infant diagnostic outcome groups at 36 months of age. These aims were informed by two lines of research including: (1) indices of social responsiveness in families raising children with ASD and (2) previous coding schemes used to index social behaviors in parents raising children with and at risk for ASD.

Maternal social responsiveness

Social responsiveness is a key element of positive dyadic interactions and is a known difficulty among family members raising children with ASD. These subclinical social difficulties are often described as elements of the broader autism phenotype (BAP). Validated questionnaires like the Social Responsiveness Scale (SRS) or the Broad Autism Phenotype Questionnaire (BAPQ) are commonly used in family-based ASD research to index the full continuum of social competence (Constantino et al., 2010; Constantino and Todd, 2003; Feczko et al., 2016; Schwichtenberg et al., 2010). Elevated scores indicate difficulties with social responsiveness, rigidity, and contextual awareness across a variety of situations. Several studies have demonstrated that families raising children with ASD present with a shifted distribution or more difficulties with social responsiveness and communication (Page et al., 2017; Virkud et al., 2008). However, these findings are less common in mothers and relatively little is known about how high or low scores on these questionnaires relate to behaviors in context. To our knowledge, currently only two ASD-focused studies address how social responsiveness or competence ratings are associated with observed interactive behaviors. First, a study by Jones et al. (2017) assessed child social responsiveness (SRS scores) and child gaze behaviors across two contexts (play and conversations). Children with higher SRS scores (more social and communication difficulties) exhibited fewer gaze shifts to the examiner within a conversation context. Second, Parr et al. (2015) provided a parent-mediated intervention to mothers of children with ASD exhibiting high (n = 5) and low (n = 9) levels of the BAP. Mothers presenting with more BAP features, or more social and communication difficulties, exhibited less change in their play behaviors (e.g. praise, turn-taking, imitation) in response to the parent-mediated intervention. These preliminary studies highlight the potential utility of indexing social responsiveness and communication competencies. For example, if a mother receives an elevated SRS score, are her interactions with her infant markedly different than that of a mother with a lower score? If such a connection could be demonstrated, then interventionists or clinicians could use questionnaires to identify those who may need more support when implementing a parent-mediated intervention.

Maternal social behaviors in context

When considering maternal behaviors and infant development, an extensive body of research exists that highlights the imperative role of maternal behaviors in language and social development (Bang and Nadig, 2015; Bottema-Beutel et al., 2014; Brian et al., 2016; Chiang et al., 2016; Green et al., 2017; Gulsrud et al., 2016; Kasari et al., 2015; Kim and Mahoney, 2004; Pickles et al., 2016; Shire et al., 2016; Siller et al., 2014; Siller and Sigman, 2002; Tager-Flusberg, 2016). Notably, these studies emphasize the positive role maternal behaviors can have on the development for children with (and without) ASD. Overall, detailing the research on maternal behaviors and early social or language development is beyond the scope of this article; therefore, the following review focuses only on investigations that utilize an infant sibling design.

Within infant sibling studies, findings regarding maternal behaviors in context are mixed. Three studies have reported mothers of high-risk (HR) siblings display lower levels of sensitive responding or higher directedness during play between 6 and 12 months of age when compared to a low-risk (LR) group (Harker et al., 2016; Wan et al., 2012, 2013). Conversely, an observational study of 11-month-old infant siblings did not find significant HR – LR group differences for parent initiating/directing, praise, scaffolding, warmth, or sensitivity (Campbell et al., 2015). Similarly, Talbott et al. (2015, 2016) reported mothers raising an infant at risk for ASD (HR group) used more gestures and comparable linguistic inputs when compared to their LR counterparts. Comparable maternal responsiveness to infant communicative behaviors were also reported in Leezenbaum et al.’s (2014) study of HR (n = 12) and LR infants (n = 14).

When considering child diagnosis or developmental concerns, only a few infant sibling studies have directly reported on maternal behaviors across groups (Talbott et al., 2015, 2016; Wan et al., 2013). Talbott et al. (2015, 2016) assessed a small cohort of infant siblings and compared maternal vocalizations and gesture use across three groups of children: ASD, LR, and HR (with no ASD diagnosis). Notably, maternal behaviors for the infants diagnosed with ASD were not significantly different. Conversely, Wan et al. (2013) used the same groupings and reported higher codes for maternal directiveness when infants were 12 months of age. Within each of these studies, sample sizes were relatively small (less than 60 HR infants) and the mixed findings and attenuated group differences may reflect low power.

Notably, the groupings used across infant sibling studies often vary and sometimes include a LR comparison group and two HR groups (e.g. HR ASD group and HR Non-ASD group). To help ground this work within previous studies (e.g. Wan et al., 2013), two distinct outcome groupings for HR infants were employed in the current study. The first compares infants solely based on their developmental outcome (ASD, non-typical development (Non-TD), and typical development (TD)) and the second incorporated their risk group status (LR, HR Non-ASD, and HR ASD).

Measuring dyadic behaviors

Assessing mother and infant behaviors during play or other social tasks is common in social science research. Unfortunately, there is little agreement on a gold standard in the field (Halle et al., 2011). Studies like Wan et al. (2012, 2013) use indices that assess global maternal behaviors (i.e. Manchester Assessment of Caregiver–Infant Interaction). For this rating scale and others like it, observers rate an interaction using global ratings that assess the quality and intent of parental behaviors (e.g. scaffolding; Campbell et al., 2015; Freeman and Kasari, 2013). Other approaches in the field assess parental cognitions about their interactions (Ohr et al., 2010) or the frequency of positive or negative parenting behaviors per minute of interaction (Cyr et al., 2014). Researchers have also assessed interactions at a more micro-analytic level, assessing core social competencies, vocalizations, or gaze (Lambert-Brown et al., 2015; Leezenbaum et al., 2014; Warlaumont et al., 2014). A micro-analytic approach may reduce rater bias and capture elements of an interaction not readily apparent in real-time or when making more global judgments. For example, in Green et al. (2017), the parent-mediated intervention included two validated behavioral coding schemes for characterizing dyadic interactions (i.e. global ratings and event coding) and observed more instances of behavioral change using the event coding scheme.

The present study uses a micro-analytic approach to take a detailed look at maternal and infant behaviors during dyadic play in order to reduce value interpretations and other rater biases. The coded behaviors pull from previous studies and focus on behaviors that have been highlighted as influential in ASD risk or development including gaze, vocalizations, affect, and multimodal social behaviors like social smiling (Filliter et al., 2015; Gangi et al., 2017; Nichols et al., 2014; Ozonoff et al., 2010; Talbott et al., 2015, 2016; Yirmiya et al., 2006). With these micro-analytic codes, parent-mediated interventions may be informed by identifying potential maternal behaviors that promote infant responsiveness and engagement. For example, in families raising infants at risk for ASD, more maternal positive affect may be associated with more infant prosocial behaviors.

Current study

To inform parent-mediated interventions, the current study focuses on maternal social responsiveness and social behaviors within context but does also include infant social behaviors to provide information on both members of the dyad. Assessing maternal behaviors specifically will help the field move forward in two ways. First, it will add to the growing body of literature assessing maternal dyadic behaviors in HR siblings with the largest sample to date. With this, it has the potential to inform discrepant findings. Second, it will provide insights into the application of questionnaire-based indices of social communicative behaviors to explore if they are useful in identifying mothers that may need more support within parent-mediated interventions.

Method

Participants

One hundred and fifty-two families participated in this study. Infant siblings were recruited from families with at least one older child diagnosed with ASD (n = 90) or at least one typically developing older child and no history of ASD in first, second, and third degree relatives (n = 62). The older HR siblings (called proband siblings) were diagnosed with Diagnostic and Statistical Manual of Mental Disorders, 4th ed. (DSM-IV) Autistic Disorder, Asperger Disorder, or Pervasive Developmental Disorder-Not Otherwise Specified (PDD-NOS). Proband diagnostic status was confirmed with the Autism Diagnostic Observation Schedule (ADOS; Lord et al., 2002). Family demographic information stratified by risk group is provided in Table 1.

Table 1.

Sample demographic characteristics stratified by family risk group.

	Risk group
	Low	High
N	62	90
Maternal age, range, M(SD)	18–44, 32(5)	23–49, 35(5)
Maternal education, n(%)
Some high school	2 (3%)	0 (0%)
High school/GED	11 (18%)	27 (30%)
College degree	27 (44%)	39 (43%)
Graduate degree	20 (32%)	15 (17%)
Other	1 (2%)	2 (2%)
Unreported	1 (2%)	7 (8%)
Marital status, n(% married)	54 (87%)	82 (91%)
Family income, n(%)
Below US$25,000	2 (3%)	5 (6%)
US$25,000–US$49,999	8 (13%)	7 (8%)
US$50,000–US$ 74,999	16 (26%)	15 (17%)
US$75,000–US$99,999	11 (18%)	19 (21%)
US$100,000–US$124,999	9 (15%)	12 (13%)
US$125,000 and above	13 (21%)	24 (27%)
Unreported	3 (5%)	8 (9%)
Maternal SRS T scores, range, M(SD)	44–61, 50(4)	43–70, 49(5)
Enrolled infant, n(%)
Male	38 (61%)	55 (61%)
Female	24 (39%)	35 (39%)
Outcome status, n(%)
TD	59 (95%)	58 (64%)
Non-TD	2 (3%)	16 (18%)
ASD	1 (2%)	16 (18%)

GED: General Education Diploma; SRS: Social Responsiveness Scale; TD: typical development; Non-TD: non-typical development; ASD: autism spectrum disorder.

At the 36-month visit, infants were classified into one of three algorithmically defined outcome groups: TD, Non-TD, and ASD. The grouping criteria were developed by the Baby Siblings Research Consortium, a network of researchers studying autism identification in infants (for details see Ozonoff et al., 2014). Within the HR group, most of the infants were categorized as TD (n = 58, 64%), followed by Non-TD (n = 16, 18%), and ASD (n = 16, 18%). In the LR group, infants were categorized as TD (n = 59, 95%), Non-TD (n = 2, 3%), and ASD (n = 1, 2%). To provide a direct comparison with previous studies (e.g. Wan et al., 2013), a second grouping pattern was also employed which incorporated both risk group status and infant diagnostic outcomes. These groups included a LR comparison group (n = 59) and the HR group was split into those with ASD (HR ASD, n = 16) and without ASD (HR Non-ASD, n = 74).

Measures

Play behaviors

As part of a longitudinal prospective study, mother–infant interactions were videotaped and coded during a play task when infants were 6, 9, and 12 months of age. Dyads were asked to play as they typically do at home and a standardized bin of toys was provided. The toys included a doll, bottle, small blanket, car, shape sorter, ball, rattle, and a pair of toy phones. From this play session, maternal and infant gaze, affect, and vocalizations, respectively, were coded for 3 min. The selected video segment included the first few minutes of active play once the examiner left the room. Initial toy setup and exploration were not coded.

For the present study, mother and infant behaviors were coded independently for frequencies of look face, positive affect, and vocalizations, which could occur in isolation or combination (i.e. multimodal responses or bids). Three multimodal codes were generated and summed: look face and positive affect, look face and vocalization, and vocalization and positive affect. Detailed coding rules were established in a previous study (Ozonoff et al., 2010). For example, positive affect included hearing the infant/mother laugh, seeing at least one corner of the infant’s/mother’s mouth up-turn, and/or flexed orbicularis oculi muscles which raise the cheeks and form “crow’s feet” around the eyes. Coders were asked to identify when positive affect began (on) and ended (off). For each on and off code of positive affect, a frequency count of 1 was given. For smiles or laughs that were in close succession, a break of at least 1 s was required to count them as two separate positive affect expressions. For additional code descriptions see (Ozonoff et al., 2010) and Table 2.

Table 2.

Maternal and infant behaviors coded during a 3-min play episode.

Code	Description
Look face	Gaze is directed toward the face of play partner
Positive affect	Displays positive affect (i.e. smile, laugh)
Vocalizations	Vocalizes using non-word sounds, words, or phrases
Multimodal	Combines at least two of the behaviors above (i.e. look face and positive affect, look face and vocalization, vocalization and positive affect)

Coders were unaware of risk status or outcome group. For training, each coder read the coding manual, shadowed a master coder for the coding of one to four play sessions and then coded four to eight play sessions independently. After this initial independent coding, preliminary intra-class correlation coefficients (ICCs) were calculated and feedback was provided for areas of discrepancy (if needed). Then the coder completed an established reliability set of six play sessions (alpha set). If all coded behaviors (i.e. gaze, positive affect, and vocalizations) did not achieve ICCs at or above .70, additional feedback was provided and then the coder completed a second reliability series (beta set). All independent coders achieved our reliability standard (ICCs at or above .70) on the alpha or beta coding sets. If ICCs at or above .70 were not achieved, then the coder did not move into independent coding. Independent coders had an ICC range of .70–.99 (M = .88). Mother and infant means and correlations and correlations are depicted in Figure 1 and Table 3.

Figure 1.

Mother (M) and child (C) play behaviors when infants were 6, 9, and 12 months of age.

Table 3.

Correlations between maternal and infant play behaviors for all dyads and dyads in the high-risk (HR) and low-risk (LR) groups.

Maternal behaviors	Infant behaviors
Maternal behaviors	6 Months				9 Months				12 Months
	1	2	3	4	1	2	3	4	1	2	3	4
All dyads
1. Look face	.01	−.06	.02	−.03	.10	−.06	.08	−.01	.03	−.07	−.07	−.18
2. Positive affect	.49***	.45***	.06	.40***	.25**	.28**	.04	.23*	.33***	.42***	.28**	.37***
3. Vocalizations	.09	−.10	−.10	.04	.14	.08	.14	.09	.15	.01	.11	−.04
4. Multimodal	.32**	.21	−.03	.24*	.35***	.26**	.08	.23*	.37***	.29***	.38***	.31***
HR group
1. Look face	.09	−.12	−.09	−.09	.04	−.02	−.01	−.02	−.08	−.08	−.03	−.24
2. Positive affect	.41**	.30*	.10	.33*	.31**	.32**	.01	.32**	.26*	.48***	.38**	.44***
3. Vocalizations	.21	−.13	−.27	−.02	.18	.01	.11	−.01	−.06	−.04	.15	−.18
4. Multimodal	.38*	.14	−.08	.25	.49***	.14	.03	.42	.23	.31**	.37**	.24*
LR group
1. Look face	−.11	−.08	.16	−.02	.26	−.11	.20	.03	.15	−.10	−.14	−.11
2. Positive affect	.56***	.61***	.01	.46**	.10	.22	.10	.09	.44**	.33**	.13	.25
3. Vocalizations	−.01	−.07	.08	.16	.04	.17	.19	.22	.44**	.07	.05	.18
4. Multimodal	.22	.28	.05	.21	.16	.36**	.15	.27	.53***	.26	.36*	.40**

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

Social responsiveness

Partner ratings of mothers on the SRS were used to index social responsiveness. The SRS is a 65-item informant-report questionnaire which assesses social interactions, relationships, and communication skills. Items are rated on a 4-point scale of (1) not true, (2) sometimes true, (3) often true, and (4) almost always true. Studies using the SRS report high reliability (Constantino et al., 2009; Constantino and Todd, 2005) and discriminant validity. It differentiates well between typically developing, at-risk, and ASD populations (Constantino et al., 2000, 2003; Reiersen et al., 2007). Partner-reported SRS scores have been validated (Constantino and Gruber, 2012) and are often included in family-based studies (Lyall et al., 2014; Schwichtenberg et al., 2010; Virkud et al., 2008). SRS total T scores may fall within the normal (T score ⩽ 59), mild to moderate (T scores 60–75), or severe range (T score ⩾ 76). Descriptive SRS statistics stratified by risk group are provided in Table 1.

ADOS

The ADOS (Lord et al., 2000) is a semi-structured standardized interaction and observation that measures symptoms of autism. It has two empirically derived cutoffs, one for ASD and one for autistic disorder. It was administered to the proband at the initial visit to confirm inclusion and to the infant siblings at 36 months of age as part of his/her outcome classification. Each administrator completed an initial ADOS training and maintained 80% or greater agreement with a reliable trainer across all items.

Mullen Scales of Early Learning

The Mullen Scales of Early Learning (MSEL; Mullen, 1995) is a standardized developmental test for children ages birth to 68 months. The subscales administered included gross and fine motor, visual reception, and expressive and receptive language. This measure was used in the outcome definition, as described above.

Procedure

This study was conducted under the approval of the Institutional Review Board of the University of California, Davis. The study was explained to parents orally and in writing, all their questions were answered, and consent was obtained before conducting assessments. The SRS was completed at time of enrollment. Mother–infant play interactions were completed at 6, 9, and 12 months as part of a larger experimental battery. Infant outcome classification was determined following a laboratory visit at 36 months of age.

Results

All data were checked for normality, multicollinearity, and homoscedasticity prior to model estimation using IBM Statistical Package for the Social Sciences (SPSS) version 23. Our research questions of interest were assessed using general linear models with terms for infant sex and family income when mother–infant data were included. For the mother–infant data, separate models were specified for 6, 9, and 12 months to maximize the observations that could be incorporated. Group differences were interpreted if p < .05. To aid in the interpretation of our findings, a series of post hoc power analyses were also conducted.

Maternal social responsiveness

To address our first research aim, we compared the maternal SRS scores across the HR and LR groups. As illustrated in Figure 2, maternal SRS T scores were not significantly different across the two groups, F(1, 151) = .70, p = .40. In both groups, a majority of the scores fell within the normal range of reciprocal social behavior (T scores < 60). Within the LR group, only one mother scored in the mild range and none were in the moderate or severe ranges. Within the HR group, only two mothers scored within the mild range (T scores 60–65), one within the moderate range (T scores 66–75), and none in the severe range. These findings replicate two previous studies (e.g. De la Marche et al., 2012; Schwichtenberg et al., 2010) which have reported that mothers of children with ASD do not, at a group level, exhibit more social responsiveness difficulties (i.e. elevated SRS scores) as indexed by partner or self-report questionnaires.

Figure 2.

Maternal SRS T scores by risk group status.

Maternal social behaviors in context

General linear models were used to assess group differences in maternal social behaviors during play, with infant sex and family income as covariates. Mothers in the HR group did not present with significantly lower levels of look face, positive affect, or vocalizations when their infant was 6, 9, or 12 months of age (Table 4). Mothers in the HR group used slightly fewer multimodal bids or responses at 9 and 12 months; however, these differences were not statistically significant (adjusted for multiple comparisons) and, given the size of the effects, are unlikely to be functionally meaningful. With respect to infant sex and family income, mothers in both groups displayed similar patterns. When infants were 6 months of age, mothers used more multimodal bids with boys, and mothers who reported a higher family income tended to use more multimodal bids. Similarly, at 12 months of age, mothers vocalized more to boys, and mothers who reported a higher family income tended to vocalize more.

Maternal social behaviors in context with social responsiveness

To assess whether partner ratings of social responsiveness were associated with maternal social behaviors in context, general linear models were specified with terms for infant sex and family income. These models were specified with all available data (including all dyads regardless of risk group status or infant outcome). Partner ratings of social responsiveness (SRS scores) were not associated with maternal behaviors during play (p = .05–.99). Of the models specified, only one reached our interpretation threshold of p < .05. For this model, maternal vocalizations when infants were 12 months of age were more frequent for interactions with boys. Maternal SRS scores were not a significant predictor.

Maternal and infant social behaviors in context

To inform how maternal behaviors co-occur with infant behaviors, a series of partial correlations were completed with infant sex and family income as covariates. For all dyads, maternal expressions of positive affect and the use of multimodal bids or responses were positively associated with infant positive affect, looks to face, vocalizations, and multimodal bids or responses (Table 3). Overall, this pattern was most consistent when infants were 12 months of age. For mothers raising infants at risk for ASD (HR group), more maternal positive affect was associated with more infant positive affect, vocalizations, looks to face, and multimodal bids or responses. Similarly, more maternal multimodal bids or responses were associated with more infant positive affect, vocalizations, and multimodal bids or responses at 12 months of age. For mothers in the LR group, the overall pattern was similar.

Infant diagnostic outcomes and developmental concerns

We assessed the relations between infant outcome classifications at 36 months of age and (1) partner reports of maternal social responsiveness, (2) maternal social behaviors (when infants were 6, 9, and 12 months of age), and (3) infant social behaviors. To help compare this study directly with previous research, two outcome group classifications were utilized (i.e. ASD, Non-TD, and TD; LR, HR Non-ASD, HR ASD). Partner ratings of maternal social responsiveness (SRS scores) were comparable across the ASD (M = 49.86, SD = 5.26), Non-TD (M = 50.50, SD = 5.26), and TD outcome groups (M = 48.96, SD = 4.22). Similarly, when considering risk and outcome (LR, HR Non-ASD, and HR ASD), no significant differences emerged for maternal social responsiveness. As illustrated in Table 4, maternal social behaviors in context were not significantly different at any age across the three developmental outcome groups. Specifically, mothers of infants within the ASD outcome group (n = 16) had comparable frequencies of positive affect, vocalizations, gaze to face, and multimodal bids or responses. When considering LR, HR Non-ASD, and HR ASD, a similar pattern emerged, with no significant differences in maternal behaviors at 6, 9, or 12 months of age (all p > .05).

Table 4.

Maternal and infant behaviors during play across high-risk and low-risk groups at 6, 9, and 12 months of age.

Visit age	6 Months		F	9 Months		F	12 Months		F
Risk group	High	Low		High	Low		High	Low
N	45	41		70	53		71	51
Estimate	Mean (SE)^a			Mean (SE)^a			Mean (SE)^a
Maternal
Look face	19.12 (1.60)	19.79 (1.67)	.08	22.63 (1.20)	22.48 (1.38)	.01	24.27 (1.20)	24.73 (1.40)	.06
Pos. affect	7.78 (0.59)	7.80 (0.62)	.01	8.19 (0.46)	8.42 (0.52)	.11	8.31 (0.43)	8.22 (0.50)	.02
Vocalizations	33.50 (1.43)	34.18 (1.49)	.11	34.66 (1.26)	36.22 (1.45)	.65	37.65 (1.20)	39.47 (1.39)	.97^b,c
Multimodal	37.55 (2.19)	36.30 (2.28)	.15^b,c	36.81 (1.94)	42.26 (2.22)	3.39	38.58 (1.72)	41.67 (1.99)	1.38
Infant
Look face	10.53 (0.69)	9.48 (0.72)	1.10	12.27 (0.72)	12.43 (0.83)	.02	12.38 (0.86)	15.28 (1.00)	4.83*
Pos. affect	2.97 (0.46)	2.17 (0.48)	1.44	4.15 (0.42)	5.05 (0.48)	1.96	4.69 (0.48)	4.68 (0.56)	.00
Vocalizations	9.08 (1.15)	11.30 (1.20)	1.78	11.16 (0.90)	12.26 (1.03)	.66	14.46 (1.09)	17.21 (1.27)	2.70
Multimodal	6.61 (1.20)	4.82 (1.24)	1.70	7.43 (1.07)	9.98 (1.23)	2.45	9.64 (1.33)	11.68 (1.55)	.99

All models contained infant sex and family income as covariates.

All reported means are adjusted means.

Infant sex was a significant covariate.

Family income was a significant covariate.

Although the focus of this research is maternal behaviors, infant behaviors during play were also assessed to provide information on both members of the dyad. Descriptive statistics on infant behaviors are provided in Tables 4 and 5 and are illustrated in Figure 1. Overall, regardless of outcome at 36 months of age, all infants increased their frequency of look face, positive affect, vocalizations, and multimodal bids or responses to their mothers at 6, 9, and 12 months of age (Tables 4 and 5). There were no significant differences in infant behaviors at 6, 9, or 12 months of age across the developmental outcome groups (TD, Non-TD, ASD) or the risk and outcome groups (LR, HR Non-ASD, HR ASD).

Table 5.

Maternal and infant behaviors during play when infants were 6, 9, and 12 months of age across child outcome groups.

Visit age	6 Months			9 Months			12 Months
Risk group	TD	Non-TD	ASD	TD	Non-TD	ASD	TD	Non-TD	ASD
N	55	12	8	94	15	11	93	14	10
Estimate	Mean (SE)^a			Mean (SE)^a			Mean (SE)^a
Maternal
Look face	19.25 (1.49)	23.75 (3.10)	19.44 (3.79)	23.03 (1.05)	20.60 (2.63)	21.72 (3.09)	23.15 (1.02)	23.52 (2.58)	25.77 (3.08)
Positive affect	7.82 (0.55)	8.16 (1.14)	6.85 (1.40)	8.31 (0.38)	7.88 (0.96)	8.14 (1.13)	8.26 (0.39)	8.52 (0.99)	9.77 (1.18)
Vocalizations^b	33.61 (1.25)	34.40 (2.61)	36.99 (3.20)	35.97 (1.09)	30.53 (2.74)	33.21 (3.22)	39.52 (1.02)	34.05 (2.57)	36.87 (3.07)
Multimodal^c	36.45 (2.06)	39.95 (4.30)	37.74 (5.27)	40.32 (1.64)	31.71 (4.12)	33.21 (4.85)	41.99 (1.51)	36.33 (3.82)	40.88 (4.56)
Infant
Look face^d	10.11 (0.65)	9.88 (1.36)	10.63 (1.66)	12.61 (0.59)	10.92 (1.47)	11.70 (1.73)	14.20 (0.79)	12.25 (2.00)	12.34 (2.38)
Positive affect	2.44 (0.45)	2.82 (0.93)	3.86 (1.14)	4.42 (0.35)	3.71 (0.87)	5.84 (1.02)	4.39 (0.41)	5.03 (1.04)	6.21 (1.24)
Vocalizations	10.67 (1.10)	8.15 (2.29)	10.86 (2.80)	11.11 (0.79)	12.22 (1.98)	14.43 (2.33)	15.83 (0.89)	12.39 (2.25)	14.68 (2.69)
Multimodal	5.79 (1.17)	7.00 (2.44)	7.06 (2.99)	8.57 (0.93)	8.19 (2.33)	7.81 (2.74)	9.90 (1.16)	12.43 (2.92)	11.56 (3.48)

TD: typical development; Non-TD: non-typical development; ASD: autism spectrum disorder.

All models contained infant sex and family income as covariates.

All reported means are adjusted means.

Infant sex was a significant covariate at 12 months of age.

Infant sex was a significant covariate at 6 months of age.

Income was a significant covariate at 12 months of age.

Power analyses

Post hoc power analyses completed with G Power verified that our sample sizes were sufficient for detecting medium to large effect sizes. Specifically, analyses comparing risk group (i.e. HR vs LR) with two covariates and an alpha set at 0.05 revealed that our current sample (n = 152) had power above 0.80 to observe a medium (f² = .15) to large effect (f² = .35). In addition, for the outcome group comparisons of TD to ASD (n = 74) and TD to Non-TD (n = 74) with two covariates, power analyses revealed that the outcome comparison groups sample sizes had a power of 0.78 for a medium effect and 0.99 for a large effect size. Given the lack of significant differences for most of our analyses, these post hoc power analyses aid in providing a context for our null results.

Discussion

The present study found no significant group level differences in social communicative behaviors during play or ratings of social responsiveness between mothers of infants at risk for ASD and the comparison group (regardless of infant diagnostic status). We recognize that our analyses present null findings, and that a lack of significant difference is not the same as stating the groups are equivalent. Adequate power was obtained to detect moderate to large differences. However, across three assessment ages and six dimensions of social interaction, marked/significant differences were not apparent. Our study echoes others that report mothers of children with ASD do not exhibit social responsiveness difficulties as indexed by the SRS (De la Marche et al., 2012; Scheeren and Stauder, 2008; Schwichtenberg et al., 2010). In previous research, elevated SRS scores were more commonly reported in fathers and biological siblings of children with ASD than in mothers (Schwichtenberg et al., 2010; Virkud et al., 2008). However, other measures (i.e. BAPQ) have been used to document elevated social difficulties in mothers of children with ASD (Flippin and Watson, 2018; Pruitt et al., 2018). In addition, elevated BAP features in mothers have been associated with less optimal developmental progress for children with ASD (Flippin and Watson, 2018).

Our research questions also addressed how scores on a social communication questionnaire (i.e. SRS) relate to maternal behaviors in a social context. In theory, social communicative behaviors indexed via a questionnaire and observation would be related, but in the present study they were not. This may reflect several factors, including questionnaire content, reporter bias, or simply a lack of relationship. The use of partner or father reports is supported by previous studies (Constantino and Gruber, 2012; Lyall et al., 2014; Pearl et al., 2013; Virkud et al., 2008); however, partner reports may be capturing different or qualitatively distinct behaviors. Statements on the SRS include She is able to communicate feelings to others, She is awkward in turn-taking with others, Her behavior is socially awkward, even when trying to be polite. Each of these assess social communicative behaviors but it is understandable how they may not relate to frequencies of gaze to face, vocalizations, or the use of multimodal bids, such as social smiling. In addition, the SRS has several items that index elements of the BAP that may not relate to social communicative behaviors (e.g. She has repetitive behaviors that others consider odd). Finally, the range of SRS scores within this study was truncated and does not reflect the full range of difficulties faced by some individuals. It could be that associations between behaviors in context and SRS scores are only apparent at the higher (more impacted) end of the scale. A small study of children with autism (n = 20) supports this notion, with a reported association between SRS scores and child gaze behaviors during conversations (Jones et al., 2017). Similarly, Parr et al. (2015) reported more intervention implementation difficulties for mothers with elevated BAP features.

To ground our findings pertaining to infant diagnostic and risk groups within previous literature, we will first address how our findings align with previous research on maternal behaviors and child social communicative development in ASD, and second, we consider infant sibling study designs in particular.

Previous studies highlight the role maternal gaze patterns, vocalizations, pragmatic language, and responsiveness may play on language and social development in children with ASD (Bang and Nadig, 2015; Bottema-Beutel et al., 2014; Flippin and Watson, 2015; McKean et al., 2017; Northrup and Iverson, 2015; Stern et al., 2017). For example, in a study of 20 children with ASD and a matched group of typically developing children, maternal linguistic input (including number of vocalizations) was associated with later vocabulary growth for both groups of children (Bang and Nadig, 2015). Similarly, Flippin and Watson’s (2015) study of children with ASD documented differential growth in language skills based on maternal verbal responsiveness (which included positive affect). In this study, some of these same maternal behaviors early in development were not distinctly different across infant diagnostic or risk groups.

Within studies of infant siblings, a few have documented differences in parenting behaviors in HR samples (Harker et al., 2016; Wan et al., 2012, 2013). Although most studies report no significant differences in maternal behaviors, such as utterance frequency, dyadic synchrony, responsiveness, and warmth (Blacher et al., 2013; Campbell et al., 2015; Leezenbaum et al., 2014; Siller and Sigman, 2002; Talbott et al., 2015, 2016). Our findings align with a majority of these noting a range of social communicative behaviors in mothers of HR infants that is comparable to that of mothers raising typically developing infants.

Parent-mediated interventions rely heavily on parent behaviors in context to promote infant prosocial behaviors. Within the present study, the behaviors indexed in infants during the first year included looking to their mother’s face, expressions of positive affect, vocalizing, and multimodal bids or responses. Each of these behaviors were associated with maternal behaviors. Although the direction of influence cannot be definitively determined, the pattern of correlations suggest that as infants developed, they were more likely to gaze shift to their mother’s face, vocalize more, express more positive affect, and use more multimodal bids or responses as mothers expressed more positive affect and used more multimodal bids or responses. These associations were most consistent when infants were 12 months of age, and may reflect maternal mirroring (Bigelow et al., 2018) or responsiveness to infant cues (Van Egeren et al., 2001). These behaviors provide potential targets for parent-mediated interventions.

Although not a stated aim of this study, the lack of association between infant behaviors and diagnostic status warrants discussion. Infants within this study displayed the expected developmental gains in gaze shifting (more looks to his or her mother’s face), vocalizations, and multimodal commutative bids. This pattern highlights that our index of social communicative behaviors was sensitive enough to capture expected developmental trends, and that our lack of association is not likely a reflection of poor measurement. When considering infant behaviors, this study is not the first to document indistinguishable infant features prior to 1 year for children with ASD (Bedford et al., 2012; Cassel et al., 2007; Elsabbagh et al., 2013; Ozonoff et al., 2010; Rozga et al., 2011; Wan et al., 2013; Yirmiya et al., 2006; Zwaigenbaum et al., 2005). In fact identifying early behavioral markers before 12 months is a noted challenge for the field (see reviews, Elsabbagh and Johnson, 2016; Jones et al., 2014; Szatmari et al., 2016; Zwaigenbaum et al., 2013).

Dyadic coding practices in the social sciences are diverse and may include micro-analytic coding for duration and frequency counts, global rating systems, or research-specific coding schemes (Halle et al., 2011). These discrepancies in measurement may contribute to mixed representations of behavioral differences across studies, as well as an inability to directly compare findings across studies with similar infant sibling samples (e.g. Wan et al., 2013). Specifically, studies that utilize micro-analytic approaches to extract frequency counts (like the present study) document comparable or higher rates of maternal vocalizations, approach behaviors, gestures use, and responsiveness when comparing HR and LR samples (Apicella et al., 2013; Leezenbaum et al., 2013; Talbott et al., 2015, 2016). Conversely, studies that use more global or “gestalt” coding schemes highlight differences in maternal behaviors including more directiveness during play (Harker et al., 2016; Wan et al., 2012), less sensitive responding (Wan et al., 2013), and qualitative differences in approach behaviors (i.e. more physical contact, more high-intensity behaviors; Doussard-Roosevelt et al., 2003). Overall, global ratings of maternal behaviors have documented more difficulties for mothers of children with ASD. However, ratings of this nature are also more prone to rater bias (for a summary see Yoder and Symons, 2010).

In the future, it may be beneficial to code maternal behaviors for both micro-analytic processes (e.g. frequency of gaze shifts) and more globalized ratings (e.g. directiveness during play) to gain a holistic representation of how mothers interact with their infants. For example, Yirmiya et al. (2006) found significant group differences between HR and LR siblings for infant led synchronous interactions when the observers coded maternal and infant behaviors on 10-s intervals and qualitatively rated the intervals on a 6-point Likert-type scale.

Overall the current study has several strengths including a relatively large sample size, longitudinal data, an observational measure of maternal–infant interactions, and strict inclusion/exclusion criteria, but it is not without limitations. Mother-infant interactions are a dynamic process and each member of the dyad contributes to the overall synchrony or “flow” of the interaction. This article’s overall focus is on maternal behaviors; yet it is conceptually challenging to disentangle infant and parent behaviors within dyadic interactions. For example, as illustrated in Figure 1, both infant and maternal codes show developmental growth (i.e. as infant vocalizations increase over time, so do maternal vocalizations). One concern, when studying half of a dyad (mothers) in which the other half experiences social difficulties (e.g. developing ASD), is that the infant influence would pull the frequencies of parent social communication behaviors down. None of our findings support this. Ultimately, the entanglement of parent and infant codes is inherent in any dyadic interaction coding system.

Another limitation of the present study is the focus on only mother–infant interactions. Father–infant interactions are an understudied area in typical child development and in autism. As mentioned above, previous research has found elevated SRS scores for fathers of children with autism. Although some fathers did participate in our laboratory visits, there were too few to include as a separate group in analyses. Future research may address fathers’ social responsiveness and paternal behaviors when engaging in a parent–infant interaction with infant siblings of ASD.

Ultimately, the findings of the present study do not support the notion that mothers raising infants at risk for ASD are in some way less competent social interaction partners. This is an important message for clinicians and researchers to reflect on. These null findings also support the application of parent-mediated interventions to target social communication skills and play behaviors in children with ASD (e.g. Green et al., 2017; Kasari et al., 2014a; Rogers et al., 2014). Maternal behaviors that were associated with prosocial infant behaviors included positive affect and the use of multimodal bids or responses. Future parent-mediated interventions can build on this to optimize developmental progress for infants/children with and at risk for ASD.

Supplemental Material

AUT782220_Lay_Abstract – Supplemental material for Mothers of children with autism spectrum disorders: Play behaviors with infant siblings and social responsiveness

Supplemental material, AUT782220_Lay_Abstract for Mothers of children with autism spectrum disorders: Play behaviors with infant siblings and social responsiveness by AJ Schwichtenberg, Ashleigh M Kellerman, Gregory S Young, Meghan Miller and Sally Ozonoff in Autism

Footnotes

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was funded by the National Institute of Mental Health (“K99/R00 MH092431, R01 MH068398).

ORCID iDs

AJ Schwichtenberg

Ashleigh M Kellerman

References

Apicella

Chericoni

Costanzo

et al . (2013) Reciprocity in interaction: a window on the first year of life in autism. Autism Research and Treatment 2013: 1–12.

Bang

Nadig

(2015) Learning language in autism: maternal linguistic input contributes to later vocabulary. Autism Research 8: 214–223.

Bedford

Elsabbagh

Gliga

et al . (2012) Precursors to social and communication difficulties in infants at-risk for autism: gaze following and attentional Engagement. Journal of Autism and Developmental Disorders 42(10): 2208–2218.

Bigelow

Power

Bulmer

et al . (2018) The effect of maternal mirroring behavior on infants’ early social bidding during the still face task. Infancy 23: 367–385.

Blacher

Baker

Kaladjian

(2013) Syndrome specificity and mother-child interactions: examining positive and negative parenting across contexts and time. Journal of Autism and Developmental Disorders 43: 761–774.

Bottema-Beutel

Yoder

Hochman

et al . (2014) The role of supported joint engagement and parent utterances in language and social communication development in children with autism spectrum disorder. Journal of Autism and Developmental Disorders 44(9): 2162–2174.

Brian

Smith

Zwaigenbaum

et al . (2016) The social ABCs caregiver-mediated intervention for toddlers with autism spectrum disorder: feasibility, acceptability, and evidence of promise from a multisite study. Autism Research 9(8): 899–912.

Campbell

Leezenbaum

Mahoney

et al . (2015) Social engagement with parents in 11-month-old siblings at high and low genetic risk for autism spectrum disorder. Autism 19: 915–924.

Cassel

Messingeer

Ibañez

et al . (2007) Early social and emotional communication in the infant siblings of children with autism spectrum disorders: an examination of the broad phenotype. Journal of Autism and Developmental Disorders 37: 122–132.

10.

Chiang

C-H

Chu

C-L

Lee

T-C

(2016) Efficacy of caregiver-mediated joint engagement intervention for young children with autism spectrum disorders. Autism 20: 172–182.

11.

Constantino

Abbacchi

Lavesser

et al . (2009) Developmental course of autistic social impairment in males. Development and Psychopathology 21: 127–138.

12.

Constantino

Gruber

(2012) The Social Responsiveness Scale Manual. 2nd ed. Los Angeles, CA: Western Psychological Services.

13.

Constantino

Todd

(2003) Autistic traits in the general population: a twin study. Archives of General Psychiatry 60: 524–530.

14.

Constantino

Todd

(2005) Intergenerational transmission of subthreshold autistic traits in the general population. Biological Psychiatry 57: 655–660.

15.

Constantino

Hudziak

Todd

(2003) Deficits in reciprocal social behavior in male twins: evidence for a genetically independent domain of psychopathology. Journal of the American Academy of Child and Adolescent Psychiatry 42: 458–467.

16.

Constantino

Przybeck

Friesen

et al . (2000) Reciprocal social behavior in children with and without pervasive developmental disorders. Journal of Developmental and Behavioral Pediatrics 21: 2–11.

17.

Constantino

Zhang

Frazier

et al . (2010) Sibling recurrence and the genetic epidemiology of autism. The American Journal of Psychiatry 167: 1349–1356.

18.

Cyr

Pasalich

McMahon

et al . (2014) The longitudinal link between parenting and child aggression: the moderating effect of attachment security. Child Psychiatry and Human Development 45: 555–564.

19.

De la Marche

Noens

Luts

et al . (2012) Quantitative autism traits in first degree relatives: evidence for the broader autism phenotype in fathers, but not in mothers and siblings. Autism 16: 247–260.

20.

Doussard-Roosevelt

Joe

Bazhenova

et al . (2003) Mother–child interaction in autistic and non-autistic children: characteristics of maternal approach behaviors child social responses. Developmental and Psychopathology 15: 277–295.

21.

Elsabbagh

Johnson

(2016) Autism and the social brain: the first-year puzzle. Biological Psychiatry 80(2): 94–99.

22.

Elsabbagh

Gliga

Pickles

et al . (2013) The development of face orienting mechanisms in infants at-risk for autism. Behavioural Brain Research 251: 147–154.

23.

Feczko

Bliss-Moreau

Walum

et al . (2016) The Macaque Social Responsiveness Scale (mSRS): a rapid screening tool for assessing variability in the social responsiveness of rhesus monkeys ( Macaca mulatta). PLoS ONE 11: e0145956.

24.

Filliter

Longard

Lawrence

et al . (2015) Positive affect in infant siblings of children diagnosed with autism spectrum disorder. Journal of Abnormal Child Psychology 43(3): 567–575.

25.

Flippin

Watson

(2015) Fathers’ and mothers’ verbal responsiveness and the language skills of young children with autism spectrum disorder. American Journal of Speech-Language Pathology 24: 400–410.

26.

Flippin

Watson

(2018) Parental broad autism phenotype and the language skills of children with autism spectrum disorder. Journal of Autism and Developmental Disorders 48: 1895–1907.

27.

Freeman

Kasari

(2013) Parent-child interactions in autism: characteristics of play. Autism 17: 147–161.

28.

Gangi

Schwichtenberg

Iosif

A-M

et al . (2017) Gaze to faces across interactive contexts in infants at heightened risk for autism. Autism. Epub ahead of print 7 July. DOI: 10.1177/1362361317704421.

29.

Green

Charman

Pickles

et al . (2015) Parent-mediated intervention versus no intervention for infants at high risk of autism: a parallel, single-blind, randomised trial. Psychiatry 2: 133–140.

30.

Green

Pickles

Pasco

et al . (2017) Randomised trial of a parent-mediated intervention for infants at high risk for autism: longitudinal outcomes to age 3 years. Journal of Child Psychology and Psychiatry 58: 1330–1340.

31.

Green

Wan

Guiraud

et al . (2013) Intervention for infants at risk of developing autism: a case series. Journal of Autism and Developmental Disorders 43: 2502–2514.

32.

Gulsrud

Hellemann

Shire

et al . (2016) Isolating active ingredients in a parent-mediated social communication intervention for toddlers with autism spectrum disorder. Journal of Child Psychology and Psychiatry 57: 606–613.

33.

Halle

Anderson

Blasberg

et al . (2011) Quality of caregiver-child interactions for infants and toddlers (Q-CCIT): a review of the literature. OPRE 2011-25. Washington, DC: Office of Planning, Research and Evaluation, Administration of Children and Families, US Department of Health and Human Services. Available at: https://www.acf.hhs.gov/sites/default/files/opre/quality_caregiver.pdf

34.

Harker

Ibañez

Nguyen

et al . (2016) The effect of parenting style on social smiling in infants at high and low risk for ASD. Journal of Autism and Developmental Disorders 46: 2399–2407.

35.

Jones

Gliga

Bedford

et al . (2014) Developmental pathways to autism: a review of prospective studies of infants at risk. Neuroscience and Biobehavioral Reviews 39: 1–33.

36.

Jones

Southerland

Homa

et al . (2017) Increased eye contact during conversation compared to play in children with autism. Journal of Autism and Developmental Disorders 47: 607–614.

37.

Kasari

Gulsrud

Paparella

et al . (2015) Randomized comparative efficacy study of parent-mediated interventions for toddlers with autism. Journal of Consulting and Clinical Psychology 83: 554–563.

38.

Kasari

Lawton

Shih

et al . (2014a) Caregiver-mediated intervention for low-resourced preschoolers with autism: an RCT. Pediatrics 134: e72–e79.

39.

Kasari

Siller

Huynh

et al . (2014b) Randomized controlled trial of parental responsiveness intervention for toddlers at high risk for autism. Infant Behavior & Development 37: 711–721.

40.

Kim

Mahoney

(2004) The effects of mother’s style of interaction on children’s engagement: implications for using responsive interventions with parents. Topics in Early Childhood Special Education 24: 31–38.

41.

Lambert-Brown

McDonald

Mattson

et al . (2015) Positive emotional engagement and autism risk. Developmental Psychology 51: 848–855.

42.

Leezenbaum

Campbell

Butler

et al . (2014) Maternal verbal responses to communication of infants at low and heightened risk of autism. Autism 18: 694–703.

43.

Lord

Risi

Lambrecht

et al . (2000) The autism diagnostic observation schedule—generic: a standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders 303(3): 205–223.

44.

Lord

Rutter

Dilavore

et al . (2002) Autism Diagnostic Observation Schedule:. Los Angeles, CA: Western Psychological Services.

45.

Lyall

Constantino

Weisskopf

et al . (2014) Parental social responsiveness and risk of autism spectrum disorder in offspring. JAMA Psychiatry 71: 936–942.

46.

McKean

Reilly

Bavin

et al . (2017) Language outcomes at 7 years: early predictors and co-occurring difficulties. Pediatrics. Available at: https://pdfs.semanticscholar.org/d8ca/ef8380fc1944d23418e5692e188601f6225e.pdf

47.

Mullen

(1995) Mullen Scales of Early Learning. (AGS ed.). Circle Pines, MN: American Guidance Service Inc.

48.

Nichols

Ibanez

Foss-Feig

et al . (2014) Social smiling and its components in high-risk infant siblings without later ASD symptomatology. Journal of Autism and Developmental Disorders 44: 894–902.

49.

Northrup

Iverson

(2015) Vocal coordination during early parent–infant interactions predicts language outcome in infant siblings of children with autism spectrum disorder. Infancy 20: 523–547.

50.

Ohr

Vidair

Gunlicks-Stoessel

et al . (2010) Maternal mood, video-mediated cognitions, and daily stress during home-based, family interactions. Journal of Family Psychology 245(5): 625–634.

51.

Ozonoff

Iosif

A-M

Baguio

et al . (2010) A prospective study of the emergence of early behavioral signs of autism. Journal of the American Academy of Child and Adolescent Psychiatry 49(3): 256–266e2.

52.

Ozonoff

Young

Belding

et al . (2014) The broader autism phenotype in infancy: when does it emerge? Journal of the American Academy of Child and Adolescent Psychiatry 53: 398–407.

53.

Page

Constantino

Zambrana

et al . (2017) Quantitative autistic trait measurements index background genetic risk for ASD in Hispanic families. Molecular Autism 7: 39.

54.

Parr

Gray

Wigham

et al . (2015) Measuring the relationship between the parental Broader Autism Phenotype, parent–child interaction, and children’s progress following parent mediated intervention. Research in Autism Spectrum Disorders 20(Suppl. C): 24–30.

55.

Pearl

Murra y

Smith

et al . (2013) Assessing adolescent social competence using the social responsiveness scale: should we ask both parents or will just one do? Autism 17: 736–742.

56.

Pickles

Le Couteur

Leadbitter

et al . (2016) Parent-mediated social communication therapy for young children with autism (PACT): long-term follow-up of a randomised controlled trial. The Lancet 388(10059): 2501–2509.

57.

Pruitt

Rhoden

Ekas

(2018) Relationship between the broad autism phenotype, social relationships and mental health for mothers of children with autism spectrum disorder. Autism 22: 171–180.

58.

Reiersen

Constantino

Volk

et al . (2007) Autistic traits in a population-based ADHD twin sample. Journal of Child Psychology and Psychiatry 48(5): 464–472.

59.

Rogers

Vismara

Wagner

et al . (2014) Autism treatment in the first year of life: a pilot study of infant start, a parent-implemented intervention for symptomatic infants. Journal of Autism and Developmental Disorders 44: 2981–2995.

60.

Rozga

Hutman

Young

et al . (2011) Behavioral profiles of affected and unaffected siblings of children with autism: contribution of measures of mother-infant interaction and nonverbal communication. Journal of Autism and Developmental Disorders 41: 287–301.

61.

Scheeren

Stauder

(2008) Broader autism phenotype in parents of autistic children: reality or myth? Journal of Autism and Developmental Disorders 382(2): 276–287.

62.

Schwichtenberg

Young

Sigman

et al . (2010) Can family affectedness inform infant sibling outcomes of autism spectrum disorders? Journal of Child Psychology and Psychiatry 51(9): 1021–1030.

63.

Shire

Gulsrud

Kasari

(2016) Increasing responsive parent–child interactions and joint engagement: comparing the influence of parent-mediated intervention and parent psychoeducation. Journal of Autism and Developmental Disorders 46: 1737–1747.

64.

Siller

Sigman

(2002) The behaviors of parents of children with autism predict the subsequent development of their children’s communication. Journal of Autism and Developmental Disorders 32: 77–89.

65.

Siller

Swanson

Gerber

et al . (2014) A parent-mediated intervention that targets responsive parental behaviors increases attachment behaviors in children with ASD: results from a randomized clinical trial. Journal of Autism and Developmental Disorders 44: 1720–1732.

66.

Stern

Maltman

Roberts

(2017) The influence of maternal pragmatics on the language skills of children with autism. Journal of Developmental and Behavioral Pediatrics 38: 339–344.

67.

Szatmari

Chawarska

Dawson

et al . (2016) Prospective longitudinal studies of infant siblings of children with autism: lessons learned and future directions. Journal of the American Academy of Child and Adolescent Psychiatry 55: 179–187.

68.

Tager-Flusberg

(2016) Risk factors associated with language in autism spectrum disorder: clues to underlying mechanisms. Journal of Speech Language and Hearing Research 59: 143–154.

69.

Talbott

Nelson

Tager-Flusberg

(2015) Maternal gesture use and language development in infant siblings of children with autism spectrum disorder. Journal of Autism and Developmental Disorders 45: 4–14.

70.

Talbott

Nelson

Tager-Flusberg

(2016) Maternal vocal feedback to 9-month-old infant siblings of children with ASD. Autism Research 9: 460–470.

71.

Van Egeren

Barratt

Roach

(2001) Mother–infant responsiveness: timing, mutual regulation, and interactional context. Developmental Psychology 37: 684–697.

72.

Virkud

Todd

Abbacchi

et al . (2008) Familial aggregation of quantitative autistic traits in multiplex versus simplex autism. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics 1503(3): 328–334.

73.

Wan

Green

Elsabbagh

et al . (2012) Parent-infant interaction in infant siblings at risk of autism. Research in Developmental Disabilities 33: 924–932.

74.

Wan

Green

Elsabbagh

et al . (2013) Quality of interaction between at-risk infants and caregiver at 12–15 months is associated with 3-year autism outcome. Journal of Child Psychology and Psychiatry 54: 763–771.

75.

Warlaumont

Richards

Gikerson

et al . (2014) A social feedback loop for speech development and its reduction in autism. Psychological Science 25: 1314–1324.

76.

Yirmiya

Gamliel

Pilowsky

et al . (2006) The development of siblings of children with autism at 4 and 14 months: social engagement, communication, and cognition. Journal of Child Psychology and Psychiatry 47: 511–523.

77.

Yoder

Symons

(2010) Observational Measurement of Behavior. New York: Springer.

78.

Zwaigenbaum

Bryson

Rogers

et al . (2005) Behavioral manifestations of autism in the first year of life. International Journal of Developmental Neuroscience 23(2): 143–152.

79.

Zwaigenbaum

Bryson

Garon

(2013) Early identification of autism spectrum disorders. Behavioural Brain Research 251: 133–146.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.43 MB