Elsevier

Brain Research

Volume 1380, 22 March 2011, Pages 246-254
Brain Research

Research Report
Limited activity monitoring in toddlers with autism spectrum disorder

https://doi.org/10.1016/j.brainres.2010.11.074Get rights and content

Abstract

This study used eye-tracking to examine how 20-month-old toddlers with autism spectrum disorder (ASD) (n = 28), typical development (TD) (n = 34), and non-autistic developmental delays (DD) (n = 16) monitored the activities occurring in a context of an adult–child play interaction. Toddlers with ASD, in comparison to control groups, showed less attention to the activities of others and focused more on background objects (e.g., toys). In addition, while all groups spent the same time overall looking at people, toddlers with ASD looked less at people's heads and more at their bodies. In ASD, these patterns were associated with cognitive deficits and greater autism severity. These results suggest that the monitoring of the social activities of others is disrupted early in the developmental progression of autism, limiting future avenues for observational learning.

Research Highlights

► At 20-months, toddlers with ASD monitor others’ activities less than DD or TD peers. ► Instead toddlers with ASD attend more to background objects (e.g. toys). ► When looking at people, toddlers with ASD look less at faces and more at bodies. ► These atypical looking patterns are associated with social and cognitive deficits. ► Decreased activity monitoring may limit avenues for learning in ASD.

Introduction

Social and communicative difficulties, stereotyped behaviors, and restricted interests lie at the core of autism spectrum disorders (ASDs) (American Psychiatric Association, 2000). As our understanding of autism has increased, however, so too has our appreciation of its heterogeneity (Happé et al., 2006, Szatmari, 1999, Trikalinos et al., 2005). Some have argued that, in order to understand the complex genetic and epigenetic relationships in ASD, it is necessary to consider autism not as a reflection of singular deviations in specific functional cognitive or social modules, but as the emergent and recurrent property of atypical preferences, percepts, learning, and experience (Jones and Klin, 2009, Karmiloff-Smith, 2007, Klin et al., 2003, Johnson et al., 2005). In this study we examine how toddlers with ASD perceive and monitor people engaged in a shared activity. This simple act of activity monitoring is an expression not only of a person's experience-dependent understanding of the scene, but also provides access to new experiences as actions unfold. Thus activity monitoring may be related to both cause and consequence of atypical social and cognitive development in individuals with ASD.

In typical development, the ability to understand intentional and goal directed actions of others arises early in infancy (e.g., Baldwin et al., 2001, Biro and Leslie, 2007, Falck-Ytter et al., 2006, Woodward, 1998, Woodward, 1999; for reviews see Aschersleben, 2006, Tomasello et al., 2005). However, less attention has been paid towards the relative salience of actions as compared to other salient constructs in ecological contexts. Amongst the exceptions is the work of Bahrick et al. (2002) and Bahrick and Newell (2008) who showed that when 5½-month-old infants are presented with videos of people performing everyday tasks, such as brushing their teeth, actions are prioritized for memory over both the identities of the people and the objects those people employ. Furthermore, it is only when the presentation time of the scenes is extended, or the infants are older, that memory for faces and actions is achieved simultaneously (Bahrick and Newell, 2008). These results imply that when the attentional resources are constrained, even faces, one of the most privileged socially relevant objects (Cohen Kadosh and Johnson, 2007, Farah et al., 1998, Haan et al., 2002, Halit et al., 2003, Hershler and Hochstein, 2005, Valenza et al., 1996), ultimately lose to actions.

Attention to the actions and activities of others is also a critical component of the learning and development of cognitive and social skills. For example, attention to others and their actions facilitates learning about affordances (Gibson, 1988, Huang and Charman, 2005, Loveland, 1991, Meltzoff, 1995), is a requisite for imitation and emulation (Abravanel et al., 1976, Carpenter, 2006, Heyes, 2001, Meltzoff and Moore, 1977, Tomasello, 1996, Want and Harris, 2002), and is crucial to the development of higher-level cognitive skills such as joint attention, social play, and the comprehension of intentions, goals, and motivations (Bakeman and Adamson, 1984, Carpenter et al., 1998, Moore and Dunham, 1995). The fact that skills such as affordance learning, imitation, and joint attention emerge in a regular fashion (e.g., see Carpenter et al., 1998, Trevarthen and Aitken, 2001), together with their relationships with later development of language and theory of mind skills (e.g., see Charman et al., 2000), argue for mutual interdependencies and suggest that common requirements, such as activity monitoring, may evolve together with the skills themselves.

Many of the skills outlined above have been found to be impaired in autism spectrum disorders. Children with ASD have been shown to use objects in an atypical manner, for example by spinning coins, shaking toy cars, or using a sock as a container (Bruckner and Yoder, 2007, Ozonoff et al., 2007). These unusual object manipulations may indicate self-stimulatory or regulatory behavior (Turner, 1997, Turner, 1999, Whitman, 2004); however, as noted by Loveland (1991), such behaviors might also indicate that they have not discovered the culturally appropriate affordances of objects via typical observation of adults and peers. In this case, attending to the behaviors of others would be a requisite to learning about those socially agreed upon conventions. Studies have also found deficits in imitation in ASD (Charman et al., 1997, Colombi et al., 2009, Rogers et al., 2003, Vivanti et al., 2008; for reviews see Williams et al., 2004, Rogers and Williams, 2006). For example, Vivanti and colleagues (2008) showed that high-functioning children with autism were less precise in imitation than controls. Furthermore, greater attention to actions in children with autism corresponded to better imitation of certain types of gestures. Through eye-tracking, the authors were able to differentiate between attention to the actor, background, and the act itself, bringing into focus the possibility that a seemingly similar overall engagement in an experimental task may be comprised of very different internal patterns of selective attention. Finally, systematic deficits observed in joint attention suggest that reduced attention to the attentional focus of others may be a particularly striking characteristic of ASD (Bono et al., 2004, Bruinsma et al., 2004, Charman, 2003, Charman et al., 1997, Dawson et al., 2004, Hecke et al., 2007, Leekam et al., 2000, Leekam and Ramsden, 2006, Mundy and Vaughan, 2002, Mundy et al., 1990, Sullivan et al., 2007). Taken as a whole, these studies suggest that activity monitoring, a component of all these skills, may be affected by the developmental progression of the autistic syndrome.

In this study we examine to what extent toddlers with ASD attend to the activities of others as compared to chronologically matched typically developing (TD) toddlers and chronologically and mental age matched toddlers with developmental delays (DD). Traditionally, in studies of phenomena such as joint attention and imitation, the child is explicitly included as an active participant in the ongoing social exchange. By contrast, in this study, we examine the gaze response of children to the activities of others during natural viewing. Also in contrast to other studies, there is no attempt to actively engage the child's attention socially at the onset of the experiment (e.g., through infant-directed motherese or direct gaze), there are no predefined instructions to the subjects, and the study is conducted via presentation of a naturalistic play interaction. The study targets toddlers at 20 months of age, the earliest age at which a stable diagnosis of ASD can be obtained (Chawarska et al., 2007), employing an ecologically valid paradigm in terms of what children may naturally encounter at any age.

Based on the extant literature, we hypothesize that that toddlers with ASD will spend less time attending to the actors of the scene and the area of shared activity. Instead, we expect they will spend more time looking at toys and objects in the background. Finally, given hypothesized relationships between social functioning and visual scanning patterns in ASD (Anderson et al., 2006, Jones et al., 2008, Klin et al., 2002, Speer et al., 2007, Chawarska and Shic, 2009), we expect that deviations from prototypical scanning behavior will correlate with measures of social deficits and impaired cognitive functioning in toddlers with ASD.

Section snippets

Results

To examine if the groups included into the study (for characterization, see Table 1) differed in their overall level of attention, we compared the toddlers on the total time spent looking at the movie. There were no between-group differences: on average, toddlers with ASD viewed the scene for 23.5 s (SD = 5.6), the DD group for 24.6 s (SD = 5.1), and the TD group for 26.2 s (SD = 5.0) (p > .13 for all pairwise group comparisons).

To examine overall differences in scanning patterns between groups, a

Discussion

While a vast majority of studies of social perception in young children with autism have focused on attention to faces and facial cues, our study examined the ability of these children to attend to the shared activities of others. This is important because attending to what others do is the critical first step in understanding what they do: a deficit at this stage limits further learning, potentially reducing the relevance of others' activities to the observer and consequently depressing the

Participants

Three groups of 20-month-old toddlers (n = 78) were recruited for this study: toddlers with autism spectrum disorder (ASD) (n = 28), typically developing (TD) toddlers (n = 34), and toddlers displaying developmental delays (DD) but who did not meet criteria for ASD (n = 16) (Table 1). Classification of developmental status was determined by clinicians on the basis of a review of medical and developmental history, diagnostic tests (Autism Diagnostic Observation schedule – Generic (ADOS-G) Module 1) (

Acknowledgments

The study was supported by NIMH grant T32 MH18268 (to F.S.), P50 MH 081756 (Autism Centers of Excellence) project 2 (PI: K.C.), NICHD P01 HD 003008 Project 1 (PI: K.C.), Autism Speaks and the NAAR foundation (to K.C.), and the National Science Foundation CDI award #0835767 (PIs: K.C. and B.S.). We would like to thank Suzanne Macari for her insights regarding the subjects and details of this work; Warren Jones for his help in initial conceptualization of experiments from which this project grew;

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