Social and non-social visual attention patterns and associative learning in infants at risk for autism.

Autism Spectrum Disorders (ASDs) represent a set of developmental disorders characterized by social and communication deficits, often along with repetitive behaviors and interests (American Psychiatric Association, 2000). The high prevalence of ASDs, 1 in 110 children, is a major public health issue (ADDM, 2009). There is an urgent need to detect ASDs as early as possible to permit earlier intervention, possibly improving outcome. ASDs are typically diagnosed between three and six years of age (Wiggins, Baio, & Rice, 2006). However, prospective, longitudinal research has been used to identify factors that allow for earlier detection of ASDs in infants at increased genetic risk (e.g., Landa & Garrett-Mayer, 2006; Landa, Holman, & Garrett-Mayer, 2007; Zwaigenbaum, et al., 2005). In addition to having an increased risk for ASDs, siblings of children with autism (AU sibs) are at increased genetic risk for related, milder social and communication impairments (Folstein, et al., 1999). There is growing evidence from prospective studies that social communication development is disrupted between the ages of 14 to 24 months in most children later diagnosed with ASDs. Specifically, disruption in nonverbal communication is characterized by infrequent initiation of and response to joint attention cues of others (Charman et al., 2005; Chawarska, Klin, Paul, & Volkmar, 2007; Sullivan et al., 2006; Landa et al., 2007), infrequent reciprocal social interaction, poor integration of eye gaze within such interactions, and infrequent shared positive affect (Chawarska et al., 2007; Landa et al., 2007). However, little is known about whether similar signs of developmental disruption may be evident earlier in life for infants at risk for autism and related social and communication delays. Therefore, the main purpose of the present study was to compare precursors of social communication, specifically visual attention patterns, in six-month-old infant AU sibs and infants at low risk (LR infants) for ASDs. The few prospective studies that have focused on the first year of life of AU sibs have provided mixed evidence of developmental disruption at this early age. In some studies, early signs of developmental disruption were noted in a subgroup of infant AU sibs. These signs include diminished social attention and eye contact (Zwaigenbaum et al. 2005), failure in orienting to name (Zwaigenbaum et al., 2005), and difficulty disengaging visual attention (Bryson, et al., 2007; Zwaigenbaum et al., 2005). Yet when AU sibs have been compared to LR infants as a group, only subtle differences have been identified. For example, four-month-old AU sibs exhibited more neutral affect, but no differences in visual attention, within the still-face procedure when compared to LR infants (Yirmiya et al., 2006). Another research group reported subtly reduced smiling in six-month-old AU sibs as compared to LR infants (Cassel et al. 2007). Lower rates of attention shifts between social and nonsocial stimuli in AU sibs as compared to LR infants have been reported, with no differences in total proportion of gaze to or away from caregivers (Ibanez et al., 2008). Moreover, Merin and colleagues (2007) reported no group differences in affect or attention between six-month-old AU sibs and LR infants within this same procedure. The inconsistent or modest findings of difference between infants at high and low risk for ASDs may be related to the dyadic nature of these tasks. Tasks requiring attention to a single stimulus within a dyadic interaction (e.g., caregiver-child) may have insufficiently challenged the infant AU sibs, and hence failed to elicit behavior that was notably different from that of typical development. The approach taken in the present study was to introduce infants to a novel, multi-stimuli task that allowed for triadic interactions. A triadic interaction in infancy usually implies interactions involving a caregiver, infant, and object or event (Striano & Dahl, 2005). The triadic task employed in this study was a novel “social-object learning” task. The traditional associative learning paradigms do not involve social interactions with a caregiver (Rovee, Hayne, & Colombo, 2001). In contrast, our social-object learning task provided simultaneously available options for infants to attend to, and engage with, objects as well as their caregiver. The triadic interaction opportunity created within this task was designed as a probe for social orienting and social engagement. There were two primary motivations for the creation of this task. First, social orienting and engagement impairments are among the earliest behaviors to distinguish children with ASDs from those with other delays or typical development (Osterling & Dawson, 2002; Landa et al., 2007; Nadig et al., 2007). Second, these impairments may be precursors to later deficits in joint attention, a hallmark of ASDs (Mundy, Sigman, & Kasari, 1994). Thus, triadic interaction tasks could be particularly useful in identifying infants with vulnerability during the early emergence of social interactions. Historically, learning paradigms have been valuable for quantifying the ontogeny of learning and memory in pre-verbal infants (Rovee et al., 2001). Infants with typical development display robust and rapid action-based associative learning by three months of age, indicating the ability to learn cause-effect relationships (Rovee et al., 2001). Within these tasks, infants also display predictable patterns of attention shifting (Mast, Fagen, & Rovee-Collier, 1980), motor coordination (Heathcock et al., 2005), and affect variation (Alessandri, Sullivan, & Lewis, 1990). These tasks have been used to identify early impairments across a range of other populations such as infants with preterm birth (Rose, Feldman, & Jankowski, 2001; Heathcock et al., 2005; Heathcock et al., 2004), Down syndrome (Ohr & Fagen, 1993), and prenatal cocaine exposure (Alessandri et al., 1993). Although AU sibs have not been tested within learning tasks, preliminary evidence of abnormality in aspects of their visual attention may affect their performance (Bryson et al., 2007; Rose et al., 2001). In contrast, older children with autism, even those with intellectual disability, exhibit a relative strength in the ability to detect simple rule-based contingencies during object play with cause-effect toys (Klinger & Dawson, 2001). Overall, the aim of the present study was to compare patterns of social and non-social attention and learning in six-month-old AU sibs and LR infants when presented with the social-object learning task.