Face-to-face interactions between infants and their caregivers provide a natural and well-characterized context within which to examine infants’ earliest capacities for engaging with others. By 6 months of age, typically developing infants use combinations of expressive behavior in multiple modalities, including vocalization, facial expression, and visual orientation (Messinger et al. 1999; Weinberg and Tronick 1994; Yale et al. 2003) and coordinate the timing of these behaviors with those of their interactive partners (Cohn and Tronick 1988; Feldman 2003; Jaffe et al. 2001). In contrast, research with preschool age and older children with autism suggests they rarely integrate gaze, gestures and affective displays to communicate social intention (Dawson et al. 1990; Joseph and Tager-Flusberg 1997; Kasari et al. 1990; Trad et al. 1993). Studying face-to-face interactions between infants at risk for autism and their caregivers provides a unique opportunity to examine whether deficits in the social use of gaze and affect may be apparent as early as 6 months of age.

To date, three groups have examined infants’ social-communicative behaviors in the context of interacting with the caregiver among infant siblings of children with autism (Cassel et al. 2007; Ibanez et al. 2008; Merin et al. 2007; Yirmiya et al. 2006). In all four studies, infants participated in the Still Face Procedure (SFP), a structured paradigm in which the caregiver is asked to withdraw completely from interacting with the infant and assume a neutral expression for a pre-specified period of time before resuming contingent interaction (Tronick et al. 1978). Infants typically react to the caregiver’s still face with significant decrease in eye contact and smiling and an increase in negative affect (Adamson and Frick 2003), a reaction that has been interpreted as reflecting their appreciation of a disruption of positive co-regulation and a violation of social expectations (Hains and Muir 1996; Tronick and Cohn 1989). Employing the traditional face-to-face SFP, researchers found that compared to low-risk controls, 6-month-old siblings of children with autism smiled significantly less prior the caregiver’s withdrawal from interaction, displayed significantly more neutral affect when their caregiver resumed interaction (Cassel et al. 2007), and produced fewer gaze shifts to and away from the caregiver across the SFP (Ibanez et al. 2008). At 4 months, these infants displayed significantly more neutral affect across all three episodes of the SFP (Yirmiya et al. 2006). Merin et al. (2007) used eye tracking to examine infants’ gaze patterns during the SFP as they interacted with caregivers via a closed-circuit TV-video system. They identified a subgroup of infants who spent a greater amount of time looking at their mother’s mouth relative to her eyes, with all but one infant in this subgroup coming from the autism sibling group.

Although some differences in gaze and affective expression between autism siblings and low-risk controls have been reported across these studies, these differences were not tied to the still face episode, suggesting that both groups of infants perceived and reacted to a break in contingent interaction with the caregiver. However, as only one infant in the Yirmiya study was subsequently diagnosed with autism and diagnostic outcome data was not available for infants in the Cassel and Ibanez samples, no definitive conclusions can be drawn regarding the extent to which early social communicative behaviors may be disrupted in infants who go on to receive a diagnosis of autism. Indeed, in a follow-up of the Merin et al. sample, none of the infants in the high-risk group who were subsequently diagnosed with autism were in the subgroup that looked mostly to the mouth at 6 months of age (Young et al. 2009). These results suggest that atypical behaviors identified among infant siblings of children with autism as a group may not be informative regarding early signs of autism. Consequently, we examined whether measures of infants’ gaze and affect during the SFP and during a free play interaction with the caregiver at 6 months of age capture early social impairment among autism siblings who are subsequently diagnosed with an ASD compared to siblings whose outcomes reflect typical development and to low-risk controls.

While a mutual sharing of attention and affect during face-to-face social exchanges characterizes the earliest social interactions, toward the end of the first year of life infants begin to coordinate their attention and interest with others about external objects and events (Bakeman and Adamson 1984; Bruner and Sherwood 1983; Carpenter et al. 1998). Such joint attention behaviors represent a core area of impairment for children with autism well into the preschool years and beyond. Compared to typically developing or developmentally delayed children, children with autism are less likely to use eye contact, affect, and gestures to share and direct their interactive partners’ attention to objects of interest, as well as to respond to the attention-directing cues of others. Their use of these behaviors for more instrumental purpose, such as pointing to obtain an object, is less impaired (Dawson et al. 2004; Mundy et al. 1986; Sigman and Ruskin 1999).

A growing body of research suggests that these deficits may be among the earliest diagnostic indicators of ASD (Baranek 1999; Charman et al. 1997; Osterling and Dawson 1994). Longitudinal studies of infant siblings of children with autism indicate that measures of joint attention and requesting skill may be sensitive to early manifestations of autism and the broader phenotype from 14 to 24 months (Cassel et al. 2007; Landa et al. 2007; Mitchell et al. 2006; Sullivan et al. 2007; Toth et al. 2007; Yirmiya et al. 2006). However, the particular domains affected and the ages at which group differences emerge vary greatly across studies, particularly with respect to those siblings who do not go on to be diagnosed with autism. The present study focuses on a large sample of both affected and unaffected siblings of children with autism with the aim of clarifying the extent to which specific deficits in joint attention, or more general deficits in nonverbal communication that include both sharing/directing attention and requesting behaviors, may be observed in these two groups at 12 months of age.

Contrary to our hypotheses, infants who were diagnosed with an ASD at 36 months were just as likely to direct gaze, smiles, and vocalizations toward their caregiver during a brief free play interaction at 6 months as low-risk controls. This finding, which held for both duration and frequency measures of the behaviors, was surprising given the well documented deficits in social gaze and social smiling, difficulties perceiving and interpreting the social cues of others, and deficits in emotional responsiveness among preschool age children with autism. Perhaps a more microanalytic analysis of the timing of infant behaviors in relation to the caregiver over a longer period of observation could reveal subtle qualitative differences in early social engagement of infants with autism, such as the lower synchrony in infant-led interactions among non-affected siblings previously documented by Yirmiya et al. (2006). Nonetheless, at present we suggest that global measures of the frequency and amount of time infants spend looking at their caregivers and coordinating their gaze with other communicative behaviors such as vocalizations and smiles, do not reveal evidence of autism-specific deficits at 6 months of age.

Infants subsequently diagnosed with an ASD were also equally sensitive to a disruption of contingent social interaction by their caregiver in the SFP, as evidenced by a decrease in smiling and gaze toward the mother’s face and increased gaze aversion and negative affect when she withdrew from interaction. The caregiver’s sudden withdrawal from interaction is an extremely powerful social cue for young infants (Adamson and Frick 2003), and thus the still face effect may in fact be too robust to capture early autism-specific deficits. Indeed, the sole group difference in the SFP was a statistical trend toward a greater amount of overall time spent looking toward the caregiver’s face across the three episodes of the SFP by infants in the ASD group compared to infants in the other two groups. While this result echoes the Ibanez et al. (2008) finding of lower frequency of gaze shifts and longer mean durations of gaze at the mother’s face among infants at-risk for ASD, it is important to note that a similar result was not observed in the same group of infants in the free play interaction, which included more detailed coding of the onsets and offsets of gaze shifts toward and away from the mother. Thus, the increased attention to the caregiver’s face documented in the SFP was not a stable characteristic of infants subsequently diagnosed with ASD in the present study.

In sum, our results indicate that previous findings of reduced social orienting (Osterling and Dawson 1994; Osterling et al. 2002) and atypicalities in eye contact and social smiling (Zwaigenbaum et al. 2005) among 12-month-old infants subsequently diagnosed with autism cannot be extended downward to 6 months. Although the small number of affected infants reduced our statistical power to detect group differences at 6 months, our findings nonetheless substantiate the results from other longitudinal studies of infant siblings indicating no clear behavioral markers for ASD at 6 months (Landa et al. 2007; Ozonoff et al. 2010; Zwaigenbaum et al. 2005). Despite recognition that autism is a neurodevelopmental disorder, and evidence that the underlying brain abnormality may be present from birth (Bauman and Kemper 2005; Nelson et al. 2001; Rodier et al. 1996), the limited and largely undifferentiated behavioral repertoires of very young infants may not allow us to distinguish clinically meaningful behavioral signs of autism in infancy.

Measures of high level initiating joint attention, responding to joint attention, and requesting behaviors were sensitive to early manifestations of autism at 12 months of age. As predicted, infants subsequently diagnosed with an ASD were less likely to direct the examiner’s attention to toys of interest via pointing and showing gestures and to respond to her attention-sharing bids than infants in the other two groups. These findings support current practices in autism screening, which incorporate a failure to point to objects, to hold objects up for others to see, and to respond to the pointing gestures of others as red flags for ASD in the first two years of life (Bryson et al. 2008; Lord et al. 2000; Robins et al. 2001; Stone et al. 2000). A lack of group differences in low-level joint attention behaviors, such as alternating gaze between an active toy and the examiner, was surprising. The highly structured setting of the ESCS may have proved optimal in eliciting joint attention looks from the infants, as researchers have noted that children with autism perform considerably better in situations where the number of stimuli is limited and presented in a routine, predictable manner (Dawson et al. 2000). An analysis of spontaneous joint attention bids in unstructured play settings, where the child is free to move about and there are multiple objects competing for his attention, is warranted prior to concluding that low-level joint attention behaviors are not disrupted within the first year of life among infants who go on to be diagnosed with autism.

Contrary to evidence from studies with preschool age children, which indicate deficits in joint attention but not requesting behaviors differentiate children with autism from neurotypical and developmentally delayed children (Sigman and Ruskin 1999), infants in the ASD group exhibited lower rates of both low and high level requesting behaviors relative to unaffected siblings and comparison infants. These findings complement those of Landa et al. (2007) who found that siblings who received a clinical judgment of ASD by 36 months could be distinguished from typically developing comparison infants and unaffected siblings at 14 months on the basis of less frequent initiation of both joint attention and requesting bids. Thus, what appears to characterize risk for autism at 12 months is not a specific failure to use gaze, affect, and gesture to share attention for purely social purposes, but rather a more general communicative deficit in using such behaviors to actively engage with others around both attention sharing and requesting contexts.

The question of diagnostic predictiveness of specific measures of joint attention and requesting requires further empirical attention. As is expected at this early age (Bakeman and Adamson 1984; Butterworth and Jarrett 1991), the low rate of responding on certain measures and large standard deviations around group means on others indicated large within-group variability in skill across both affected and unaffected infants. The desire to push the search for early markers for autism, and indeed the diagnosis itself, earlier in infancy will inevitably run up against the normative variability in the development of early social-communication skills. The fact that deficits in joint attention and requesting on a group level were identified in the current study at an age when these behaviors are still emerging is quite exciting, and provides new hope for efforts to identify appropriate treatment targets for infants and toddlers showing signs of autism (Kasari 2002).

Infants’ capacity to enter into early communicative interactions allows them to learn from and through others about the environment. Early joint attention behaviors play a self-organizing function, whereby the child’s tendency to initiate social attention coordination with others assures social information input and experience presumed crucial to promoting normative behavioral and neural development (Bernier et al. 2006; Klin et al. 2005; Mundy and Neal 2001). In particular, episodes of object-mediated joint engagement are deemed central to infants’ developing understanding of others’ goals and intentions, and to the emergence of language (Baldwin 1995; Tomasello 1995; Tomasello et al. 2005). Viewed through this lens, the deficits in initiating joint attention and requesting identified in the present study suggest that 12-month-old infants who go on to be diagnosed with ASD may be far less likely to create critical social experiences for themselves. The implications of such early deficits for the subsequent development are underscored by evidence that individual differences in the initiation of joint attention and gestures in general predict language (Charman et al. 2003; Mundy et al. 1990; Sigman and Ruskin 1999) and theory of mind task performance (Charman et al. 2000) among young children with autism, and prosocial behavior and play with peers among adolescents with autism (Sigman and Ruskin 1999; Travis et al. 2001).

Turning to our NoASD siblings, we found no evidence that domains that tap early manifestations of autism at 12 months represent areas of impairment for this group as a whole. Although at first glance our results contradict previously published reports of nonverbal communication delays in non-autistic siblings of children with autism, upon closer examination, the deficits reported in those studies are subtle and inconsistent. Toth et al. (2007) found evidence of lower overall rate of communicating and use of distal gestures but no differences in the frequency of specific behaviors such as gaze shifts, gaze/point following, and requesting and joint attention gestures from 18 to 25 months of age. Cassel et al. (2007) and Yirmiya et al. (2006) reported lower rates of high level requesting behaviors at 12 and 14 months, respectively, but these studies yielded conflicting findings with regard to IJA and RJA impairments at 14–15 months. Finally, findings by Landa et al. (2007) suggest that delays in RJA at 14 months may only be evident in those siblings who subsequently exhibit language delays or social impairments. Beyond methodological considerations, these results suggest there is little consensus regarding a specific profile of deficits in this group.

It is important to note that our analyses focused on investigating whether non-diagnosed siblings as a group experience delays in social skills and nonverbal communication. Although this is a common approach in the infant sibling literature (e.g., Cassel et al. 2007; Yirmiya et al. 2006; Toth et al. 2007), evidence from family studies suggests that only a subset of older siblings and family members may be affected by the BAP (Bailey et al. 1998; Bolton et al. 1994). The practice of exploring features of the BAP by considering all non-diagnosed siblings as potentially demonstrating deficits may in fact obscure distinct subgroups of affected siblings, and place undue emphasis on characterizing this group of children as a whole as being atypical. Another approach has been to create a BAP subgroup by identifying siblings who show language and/or social delays at outcome, and then to examine whether these infants exhibit signs of atypical development in infancy (e.g., Landa et al. 2007; Sullivan et al. 2007). However, to the extent that the question of delineating the BAP, both in terms of the developmental domains that are affected and in terms of the age at which it first emerges, is an empirical one, a priori defining the BAP based on selected outcome measures may also not represent the best approach.

Future research could rely on statistical clustering techniques to identify subgroups of non-autistic siblings that show deficits across multiple domains, including language and nonverbal communication, cognition, and social skills. Ultimately, any evidence of an early BAP involving social and communication deficits in infancy will need to be confirmed through longitudinal follow-up to investigate whether early deficits persist, and whether they have measurable consequences for subsequent social and emotional functioning.