Context modulates attention to social scenes in toddlers with autism

Young children with autism spend relatively little time monitoring other people and the facial expressions and gestures of others (Dawson et al., 2004; Swettenham et al., 1998). Given that the acquisition of language and the development of social cognition are highly experience-dependent processes (Greenough, Black, & Wallace, 1987), deficits in the ability to select for processing and to sustain attention on faces early in development are likely to have a detrimental effect on early socio-cognitive (Leppanen & Nelson, 2009; Pascalis et al., 2005) and language development (Kuhl, Williams, Lacerda, Stevens, & Lindblum,1992; Thiessen, Hill, & Saffran, 2007). Furthermore, given the role observational learning plays in the development of nonsocial cognition, atypical attention towards people is likely to result in collateral difficulties in other domains as well (Shic, Bradshaw, Klin, Scassellati, & Chawarska, 2011). Thus, it is essential to advance our understanding of the processes that underlie atypical social attention at the earliest ages when autism can be reliably identified. The benefit of such an approach is two-fold: it will advance identification of target skills for intervention, and will inform the design of methods for screening infants at risk for autism spectrum disorders (ASDs) in the first year of life. In the past decade, studies utilizing eye movements as indices of perception and attention have shown great promise for identifying mechanisms underlying social disability in autism. A majority of studies have employed static images of faces and people, sometimes presented in isolation from their social context. This line of research has generated important insights into the attentional, perceptual, and learning strategies associated with autism in the first three years of life. Empirical evidence suggests that faces do not capture the attention of toddlers with ASD as readily as they capture the attention of non-affected toddlers (Coffman, Shic, Meltvedt, Bradshaw & Chawarska, 2011). When examining a novel face, toddlers with ASD exhibit atypical scanning patterns (Chawarska & Shic, 2009) and require more time to extract invariant face features necessary for recognition (Bradshaw, Shic, & Chawarska, 2011; Chawarska & Shic, 2009; Chawarska & Volkmar, 2007; Webb et al. 2010). Although studies examining the processing of static faces are essential for parsing the nature of deficits in autism and reflect upon the atypical functioning of cortical networks involved in the structural analysis of faces (Haxby, Hoffman, & Gobbini, 2002), in real life faces present as dynamic stimuli. This aspect of face processing relies heavily upon multisensory brain areas involved in the perception of biological motion, speech, and social cognition such as the posterior superior temporal sulcus (pSTS) as well as the attentional network involved in selection of and sustained attention to these salient stimuli (Allison, Puce, & McCarthy, 2000; Calvert & Campbell, 2003; Haxby et al., 2002). Several eye-tracking studies have examined the attentional responses to dynamic faces embedded in complex naturalistic contexts in toddlers with ASD (Jones, Carr, & Klin, 2008; Shic, et al., 2011). These studies suggest that when toddlers with ASD view videos of adults trying to engage them through simple social games (e.g., peek-a-boo) (Jones et al., 2008) or observe parent-child dyads engaged in a shared activity (Shic et al., 2011), they tend to look at faces less than control participants, a pattern similar to that seen in high-functioning adolescents with ASD (Klin, Jones, Schultz, Volkmar, & Cohen, 2002). The reasons for limited face monitoring in dynamic displays are not clear. It is possible that toddlers with autism spend less time attending to faces as means of regulating their arousal (Hutt & Ounsted,1966). It is also possible that they spend less time monitoring faces simply because faces are not prioritized in their attentional system for processing to the same extent as faces are in non-autistic individuals (Chawarska, Klin, & Volkmar,2003; Chawarska, Volkmar, & Klin, 2010). Finally, it is possible that limited attention to people is a direct result of increased salience of objects, whether it be due to high-level (e.g., cars) (Sasson, Turner-Brown, Holtzclaw, Lam, & Bodfish, 2008) or low-level (e.g., high contrast) attributes (Bertone, Mottron, Jelenic, & Faubert, 2005; McCleery, Allman, Carver, & Dobkins, 2007; Shic, Chawarska, Lin, & Scassellati, 2007). In the present study we examine the effect of context on the regulation of attention in toddlers with autism (AUT) as well as developmentally delayed (DD) and typically developing (TD) controls using dynamic social scenes. To parse the factors that are responsible for limited attention to faces we manipulated context with regard to the presence of salient social (child-directed speech and eye contact) and nonsocial (distractor toys) cues. If toddlers with autism exhibit a generalized social attention deficit, they would spend, compared to non-ASD controls, less time examining the person’s face in all contexts; instead we would expect their attention to be directed toward toys in the background. However, if they show elementary sensitivity to the context in which people appear in their visual field, then the atypical patterns should be condition-specific. In this case we would expect the smallest differences between groups in the condition with highly salient non-social distractors (moving mechanical toys) and the greatest differences in the condition containing explicit and prolonged social bids, including eye contact and child-directed speech.