Across analyses reported herein, we replicated recent findings indicating little evidence that infants who are diagnosed with an ASD at 36 months of age can be differentiated from non-diagnosed autism siblings and low-risk controls at 6 months of age on the basis of early disturbance in socially directed behaviors or in sensitivity to a disruption in contingent interaction with the caregiver. However, by 12 months, these infants exhibited delays in nonverbal communication that cut across joint attention and requesting domains. In contrast, in the group of siblings of children with autism who did not go on to meet diagnostic criteria for an ASD, we found no evidence of early deficits in social interaction at 6 months or in nonverbal communication at 12 months, which we expected to index the presence of the broader autism phenotype.
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.
Several limitations of the study bear acknowledgement. The composition of the sample varied across the analyses reported herein. Moreover, not all infants in the present sample were seen through the 36-month assessment visit. However, it must be noted that all of the infants in the ASD-group had been seen through 36 months of age, and of those infants in the NoASD-sib group who had been seen through the 24-month visit only, none exhibited any behaviors indicative of autism at 24 months based on clinician judgment. The final limitation concerns the small sample size in the affected sibling group for the 6-month analyses, though it should be noted that the means and standard deviations for rates and durations of communicative behaviors in the affected group are nearly identical as those in the other two groups. Nonetheless, the findings of the present study should be replicated with a larger sample of affected infants.