Parent–infant interaction in infant siblings at risk of autism

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Abstract

Recent models of the early emergence of autism spectrum disorder (ASD) propose an interaction between risk susceptibility and the infant's social environment, resulting in a progressively atypical developmental trajectory. The infant's early social environmental experience consists mostly of interaction with caregivers, yet there has been little systematic study of early parent–infant interaction in infants at risk of ASD. This study examined the global characteristics of parent–infant interaction in 6- to 10-month-old infants with an older sibling diagnosed with ASD (at-risk sibs), in comparison with a group of infants with no family history of ASD (low-risk sibs). As part of the British Autism Study of Infant Siblings (BASIS), 6-min videotaped unstructured play interactions of mother–infant dyads (45 at-risk sibs and 47 low-risk sibs) were rated on global aspects of parent–infant interaction, blind to participant information. Differences in global characteristics of interaction were observed in both infant and parent contributions in the at-risk group compared to low-risk controls. In analyses adjusted for age and developmental level, at-risk sib infants were less lively, and their parents showed higher directiveness, and lower sensitive responding (as a trend after adjustment). Level of infant liveliness was independent of other interactive behaviour. Consistent with reports in previous literature in older children with autism and in other neurodevelopmental disorders, our findings may suggest that infants at genetic risk are exposed to a more directive interactive style relatively early in infancy. We discuss possible explanations for these findings and implications for further developmental study and intervention.

Highlights

► We studied parent–infant interaction in six-month-old infants with a sibling with ASD. ► Play interactions were rated for global parent, infant and dyadic characteristics. ► At-risk sibs were less lively than controls, possibly reflecting a trait difference. ► Parents of at-risk sib infants tended to have a more directive interactive style. ► Research must explore if disrupted interaction may amplify infant social atypicality.

Introduction

In recent years, prospective studies have made important advances in delineating social information processing and communication atypicalities in infants at risk of autism spectrum disorder (ASD) and, increasingly, those who go on to be diagnosed (e.g. Cassel et al., 2007, Goldberg et al., 2005, Rozga et al., 2011, Stone et al., 2007). Other behavioural ‘markers’ in infancy have also been shown to predict later ASD (Landa and Garrett-Mayer, 2006, Landa et al., 2007, Mitchell et al., 2006, Zwaigenbaum et al., 2005). The early emergence of social and other behavioural atypicalities might suggest that perturbations in caregiver–infant interaction are a salient feature in the developmental trajectories of infants at risk of ASD. Unlike the measurement of social functioning per se, caregiver–infant interaction sees each participant influencing the other's behaviour bi-directionally, shaping the social dynamic over time and, in turn, infant social competence. Early atypicalities in social communication may disrupt caregiver response and dyadic mutuality which, over time, may amplify early susceptibilities into an increasingly atypical social developmental trajectory (Dawson, 2008, Elsabbagh and Johnson, 2007, Elsabbagh and Johnson, 2010). Evidence for this transactional view of development is well established in neurotypical development, in which patterns of parent–child interaction form early and help shape the child's ongoing social and communicative development (Feldman and Greenbaum, 1997, NICHD Early Child Care Research Network, 2001, Pastor, 1981).

Studies show that parents of older children already diagnosed with ASD tend to use more directive play interaction, for example, involving more high intensity behaviours, non-verbal prompts, and high physical proximity, compared with controls (e.g. Doussard-Roosevelt et al., 2003, Lemanek et al., 1993, Nassan El-Ghoroury and Romanczyk, 1999). One inference is that, in attempting to encourage ‘desirable’ social behaviour, some parents are inadvertently drawn into increasingly directive interactions. In neurotypical development, a directive style of parental interaction in effect discourages the infant from engaging with the parent (e.g. Lussier, Crimmins, & Alberti, 1994). Higher parent directiveness is also reported to be more common in mothers of infants with other kinds of neurodevelopmental atypicality, such as Down syndrome, and is associated with reduced behaviours or developmental progress in infants (Cielinski et al., 1995, Landry and Chapieski, 1989, Slomins and McConachie, 2006). This transactional or ‘interactive specialisation’ model suggests that such interaction perturbation might have particular salience in the early development of infants at risk for ASD because (i) the social nature of ASD may mean that infants at risk are particularly dependent on the intactness of the dyadic social communication system (i.e. there is a specific risk-diathesis); and (ii) that social brain development in ASD may be particularly environment-dependent thus differentially sensitive to the effects of social interaction. This effect could work both ways, making at-risk infants particularly vulnerable to poor social input but also particularly sensitive to its improvement. Longitudinal evidence from children diagnosed with autism, for instance, shows that interactive synchrony with parents predicts child communication outcomes (Siller and Sigman, 2002, Siller and Sigman, 2008), and specific enhancement of parental communicative synchrony following targeted parent-mediated intervention is associated with significantly improved child communication within the dyad (Green et al., 2010).

However, there has been little observational study of caregiver–infant interaction in the context of emerging ASD and associated atypicalities in infancy. Retrospective studies of parents’ home videos have identified a range of social and communicative differences between infants who later develop ASD from those who do not (Clifford and Dissanayake, 2008, Esposito and Venuti, 2009, Osterling and Dawson, 1994), which may be associated with later social communicative functioning (Poon, Watson, Baranek, & Poe, 2011). One recent study, however, focused on parent–infant interaction specifically in the home videos of a small sample who went on to develop ASD compared with a typically developing and an intellectual disability group. Infants who later developed ASD demonstrated lower social orientation at six months and a smaller increase thereafter that tended to be passive (Saint-Georges et al., 2011). Their caregivers stimulated them for longer (compared with typically developing controls) but appeared to withdraw after the first year. Parental solicitation of response through touch remained high whereas through gestures was low throughout, which may suggest an increasing tendency for caregivers to favour more directive forms of engagement, perhaps due to a lack of infant response to other forms. Although the study of home videos show high ecological validity and are not subject to the limitations of caregiver memory, they are biased by what parents choose to videotape or submit for study and may lack comparability due to varied content. Furthermore, this method does not allow for a comparison group of infants who may show similar early behaviours or interactions (on measures determined retrospectively) but who do not develop ASD later on. These issues are overcome by prospectively studying infants who later develop ASD, but such studies have not been feasible in general population samples because of its low prevalence.

One prospective approach established in recent years is to study a group who is known to be at relatively high risk of developing ASD due to its high heritability – later born siblings of children diagnosed with ASD (hereafter, ‘at-risk sibs’; Rogers, 2009, Yirmiya and Charman, 2010). Two studies to date have adopted this approach to investigate caregiver–child interactions in the first year of life. Yirmiya et al. (2006) examined the unstructured play interactions of 21 four-month-old at-risk siblings compared with 21 infants (hereafter, ‘low-risk sibs’) who had an older typically developing sibling. The total amount of infant-led play did not differ between groups, but within infant-led play itself, a quarter of at-risk sibs showed low synchronous interaction compared to none of the low-risk sibs. One explanation for this finding is that mothers find it difficult to match and respond to their infant's affect and affective change, particularly if at-risk infants show reduced affective expression. Studies using the ‘still-face’ paradigm (involving face-to-face interaction, followed by the adult becoming unresponsive/neutral then resuming interaction – Tronick, Als, Adamson, Wise, & Brazelton, 1978) suggest that at-risk infants do tend to remain unusually affectively neutral during unexpected maternal behaviour change (Cassel et al., 2007, Yirmiya et al., 2006, but no difference was reported by Merin, Young, Ozonoff, & Rogers, 2007). In Yirmiya et al.’s (2006) sample, low-synchrony infant-led interactions were also more common among infants who later had language delays.

More recently, Rozga et al. (2011) studied mother–infant interactions at 6 months in at-risk sibs who later went on to develop ASD (N = 8) compared with those who did not (N = 41) and with low-risk sibs (N = 35). No group differences were observed in social smiles, social vocalisations, or other communicative behaviour towards the mother. However, interactions may have been too short to capture interactive differences (1 min in length) and may not reflect naturalistic interaction (with no touching or use of toys). At 12 months, in an enhanced sample, joint attention and requesting behaviour were lower in at-risk sibs who went on to receive an ASD diagnosis, compared with the other groups, but the findings came from structured observation and not parent–infant interaction.

The current cross-sectional study examined parent–infant interactions as part of a larger prospective longitudinal study. Unlike almost all previous study of parent–infant interaction in at-risk sibs – which has been microanalytic, the focus of the current study is on the global characteristics of interaction. While microanalytic measurement provides numeric-rich data on the counts, durations and temporal sequences of clearly defined behaviours and affect, global ratings involve the evaluation of qualitative and quantitative attributes of domains of interaction along a scale, often taking into account contextual information. As discussed, microanalytic study has identified specific at-risk sib differences in affective synchrony in infant-led play (Yirmiya et al., 2006), infant social orientation, and maternal use of touch to elicit response (Saint-Georges et al., 2011). However, the possible impact of such differences on overall quality of dyadic interaction is unclear; for example, is the higher frequency of maternal touch to obtain attention affectionate or intrusive? Moreover, parent-mediated intervention tends to be implemented at a ‘macro’ level. Interaction studies in neurotypical development comparing ‘micro’ and ‘macro’ approaches suggest that the two approaches are complementary. Measures that are conceptually very similar using each approach are poorly correlated and might tap relatively different constructs that hold independent explanatory value in predicting future functioning (Feldman and Greenbaum, 1997, Mesman, 2010). However, one study of global interaction examined maternal sensitivity at 18 months in mothers of at-risk toddlers and found no differences between those who were subsequently diagnosed with ASD (n = 12) and those who were not (n = 21) (Baker, Lyons, Messinger, & Grantz, 2010). The child's interactive behaviour was not investigated.

The aim of the current study was to examine the global aspects of interaction in at-risk sib using a larger sample than previous interaction studies. Based on previous studies on parent–child interaction in children with ASD and in at-risk infants, our objectives were to investigate whether, compared with the low-risk group, parents of at-risk siblings were less sensitively responsive and more directive, the infants were less interactive (less attentive to parent, less positive in affect, and less lively), and the dyadic atmosphere less mutual and less intense in engagement.

Section snippets

Sample

One hundred and four parent–infant dyads were recruited sequentially into the national British Autism Study of Infant Siblings (BASIS): 54 at-risk infants (21 male, 33 female) and 50 low-risk infants (21 male, 29 female). The infants were seen when they were 6–10 months of age (mean = 238.3 days, SD = 37.2). The study had ethical approval from the London Research Ethics Committee (ref: 09/H0718/14). Informed consent was obtained from one or both parents. At enrolment, none of the infants had been

Descriptive analysis

No sibling group differences were found in: Maternal age (years: at-risk sib mean = 36.98 [SD = 36.98]; low-risk sib mean = 36.40 [SD = 36.40]; F = 0.71), infant age (months: at-risk sib mean = 7.16 [SD = 1.17]; low-risk sib mean = 7.36 [SD = 1.19]; F = 0.71), or infant gender (male at-risk sibs: n = 20 [44.40%]; male low-risk sibs: n = 18 [47.40%]; χ2 = 0.36). However, at-risk sibs were more likely to have >1 sibling (n = 27; 60.0%) than low-risk sibs (n = 14; 29.8%; χ2 = 8.49; p < 0.004).

Scores on the scales of parent–infant

Discussion

This study is the first to demonstrate systematic differences in early global parent–infant interaction between infants at risk of ASD and low-risk controls within a prospective study. Firstly, at-risk sibs showed a stronger tendency toward inactivity, with nine of the ten least lively infants coming from the at-risk group. Somewhat consistent with this finding is the low social initiation reported in Saint-Georges et al.’s (2001) home video study of young infants who were later diagnosed with

Acknowledgements

We are very grateful for the enormous contributions BASIS families have made towards this study. We also thank Richard Emsley for providing statistical advice. The research is supported by the UK Economic and Social Research Council (RES-000-22-3525) to M.W. Wan and J. Green; the UK Medical Research Council (G0701484) and the BASIS funding consortium led by Autistica (www.basisnetwork.org) to M.H. Johnson, and by a Leverhulme Early Career Fellowship to M. Elsabbagh.

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    *The BASIS team in alphabetical order: Simon Baron-Cohen, Patrick Bolton, Rachael Bedford, Susie Chandler, Janice Fernandes, Holly Garwood, Kristelle Hudry, Teodora Gliga, Leslie Tucker, and Agnes Volein.

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