The primary goal of this paper was to examine the degree to which individual differences in gaze and affect behavior at 6 months of age might serve as an early marker of autism diagnosis and related symptoms at outcome. Based on prior literature suggesting that deficits in affect sharing, social orienting in general and gaze to the eye region in particular are features of autism at later ages, we hypothesized that similar affect sharing and visual attention abnormalities might be present much earlier than ages at which formal diagnoses can be made. Indeed, previous cross-sectional research with this same group of infants at 6 months of age (Merin et al., 2007
) suggested that risk-status, with high risk defined as having an older sibling with autism, was associated with less gaze fixation to the eye region in a subgroup of infants during a live interaction between the infant and mother. Although longitudinal follow-up data for the same sample presented here yielded only 3 infants who developed autism by 24 months of age, it was relatively clear that these 3 infants did not exhibit any abnormal face scanning patterns at 6 months. Indeed, these 3 infants exhibited a pattern of face scanning that was very similar to the sample mean and was characterized by increased overall gaze aversion during the unresponsive portion of the still face, high overall gaze to the inner regions of the face, and a majority of time spent looking to the eye region of the mother’s face during the structured interaction task. Moreover, the smiling behavior of all 3 infants was likewise very close to the sample means and showed a typical and normative pattern of significant decrease in response to the mothers’ unresponsivity. The fact that these 3 infants did not differ in any quantitatively meaningful way from typical infants at 6 months was also consistent with clinical impressions and parental reports of behavior at 6 months; none of the parents or examiners noted any evidence of autism related behaviors in any of these 3 infants at 6 months of age, despite later diagnoses of autism. Thus, the possibility suggested by our previous findings that decreased gaze to the eyes at 6 months might predict a later diagnosis of autism was not supported by the profiles of the 3 subjects in the sample who did develop autism. Moreover, when examining gaze behavior and affect as predictors of the severity or frequency of autism symptoms in the sample as a whole, analyses revealed no relationships between individual differences in gaze behavior or affect and autism symptoms at 24 months, further suggesting that gaze behavior and affect at 6 months are not predictive of later autism symptoms even at sub-clinical levels.
Although we did not have data from enough 6 month old infants who later developed autism to comprise a representative sample of autism, these results do help put into perspective our original cross-sectional findings: having an older sibling with autism may have been associated with relatively less gaze to the eyes in a sub-sample of 6-month-olds as originally reported in Merin et al. (2007)
, but any such differences in gaze behavior at 6 months had nothing to do with the later development of autism symptoms. Moreover, the original finding reported by Merin et al. of a significant relationship between high-risk status and decreased gaze to the eyes was not replicated in the current study after the inclusion of additional infants. These findings underscore the fact that “at-risk” status is not synonymous with later delays, concerns, or autism symptomatology at outcome. Indeed, we found only a marginally significant relationship between risk status and clinical outcome (with a number of low-risk infants showing concerns other than autism or language specific symptoms).4
As such, the current results do provide an important corrective to our previous findings by illustrating the importance of obtaining outcome measures in place of risk-status alone when utilizing a prospective study design to identify early markers of autism.5
Although we failed to find evidence for abnormal gaze behavior or affect at 6 months in the 3 children in our sample who developed autism, it may be that such abnormalities might yet develop in these infants by 12 or 18 months of age. Thus, our findings may say more about the timing of symptom onset than about the absolute importance of gaze behavior and affect as early signs of autism. Research on the early developmental course of autism, using a variety of methodologies such as parent report, analysis of home movies, and prospective case studies, has documented significant heterogeneity in symptom onset patterns and course over the first two years of life, ranging from early onset prior to 6 months of age (e.g., Dawson, Osterling, Meltzoff, & Kuhl, 2000
; Werner, Dawson, Munson, & Osterling, 2005
) to developmental regression as late as 18 to 21 months (e.g., Goldberg, Osann, Filipek, Laulhere, Jarvis, Modahl, et al., 2003
). Therefore, it may be that we failed to see abnormal gaze and affect at 6 months in the 3 infants from our sample who developed autism not because gaze and affect are unimportant to the early identification of autism, but because the process of symptom onset had simply not yet begun for any of these 3 infants at 6 months.
In contrast to the lack of relationships between gaze behavior and affect at 6 months and primary autism symptoms at outcome, parallel analyses predicting secondary symptoms such as language functioning and socialization measures revealed a number of significant predictive relationships. Our hypotheses regarding secondary symptoms such as language were similar to those for autism symptoms: less gaze to the eyes would also predict slower developmental rates and poorer outcomes. Although we found significant predictive effects, these effects were in the opposite direction of our initial hypotheses. Growth curve analyses revealed that infants who fixated more on their mother’s mouth during the 6 month mother-infant interaction developed language at significantly higher rates and had significantly higher expressive language scores at 24 months. In terms of age equivalent scores on the MSEL, this effect amounted to a difference of more than 4 months in developmental age by 24 months between infants who looked preferentially at the mouth (−1 SD eye-mouth index) vs. those who looked preferentially at the eyes (+1 SD eye-mouth index).
With respect to other subscales of the MSEL – namely, the receptive language, fine motor, and visual reception subscales – we did not find the same relationships between face scanning and developmental levels except for a weaker relationship between face scanning and receptive language levels at 24 months (with a difference of 2 months at outcome in age equivalent scores between preferential mouth vs. preferential eye gaze). As such, within the MSEL itself, the relationship with face scanning appeared to be fairly specific to expressive language. Indeed, after covarying receptive language, the relationship between face scanning and expressive language remained, suggesting that the effect was specific to an aspect of expressive language separate from the shared variance between expressive and receptive language.
Analysis of the Vineland expressive language scale likewise revealed a similar relationship between gaze to the mouth and rate of development and developmental levels for expressive language at 24 months of age. Moreover, within the Vineland communication domain, this effect was again constrained only to the expressive language subscale and not found with the receptive language subscale. The fact that gaze to the mouth showed a similar relationship to the MacArthur CDI, a parent report measure of expressive vocabulary size at both 18 and 24 months of age, provides additional evidence of the specific relationship between face scanning and expressive language even across two very different measurement methods. Again, this effect remained significant even after covarying the MSEL receptive language scores.
A final growth curve analysis conducted with the Vineland socialization domain age equivalent scores showed the same predictive relationships with face scanning at 6 months: increased relative gaze to the mouth at 6 months was related to increased rates of growth and 24 month outcome socialization scores. Moreover, the amount of smiling behavior displayed at 6 months was also uniquely and significantly related to the rate of change in socialization scores, with greater smiling at 6 months predicting greater rates of growth in socialization scores between 12 and 24 months of age.
The relationship between less eye gaze and socialization scores is reminiscent of results reported by Klin et al. (2002)
. Using similar eye-tracking technology with adolescents and adults diagnosed with high-functioning autism, Klin et al. instructed participants to watch a dynamic movie clip of a complex and emotionally charged social interaction. The analyses of visual scanning patterns indicated that decreased gaze fixation to the eye regions of faces was related to higher Vineland socialization domain age equivalent scores for subjects with high-functioning autism. The interpretation offered by Klin et al. (2002)
was that decreased gaze to the eyes, and the concomitant increased gaze to the mouth, was a compensatory strategy for increasing one’s understanding of social situations by focusing on language, a strategy revealed in higher socialization domain scores.
In our own sample of infants, the relationship between mouth gaze and socialization more likely reflects a normative developmental process rather than a compensatory strategy. Nevertheless, an important component of Klin et al.’s interpretation is the proposition that language processing is a mediator of the relationship between face scanning and social adaptation. Indeed, considering that language is one of many mediums by which an individual might develop and exhibit socially adaptive behavior, this mediation hypothesis is particularly plausible, whether as a compensatory mechanism in adults with a disorder or as a normative developmental process in 6 month old infants who are first beginning to learn language. The role of language in social adaptation is apparent even in the developmentally early items on the Vineland Socialization scale (e.g., “Plays very simple interaction games with others”, “Imitates adult phrases heard on previous occasions,” “Addresses at least two familiar people by name”).
Statistically, such a mediation effect would be detectable by the disappearance or at least dramatic reduction of any previously significant relationship between eye-mouth index scores and socialization scores after co-varying for significant language effects (Baron & Kenny, 1986
; Judd & Kenny, 1981
; MacKinnon, Warsi, & Dwyer, 1995
). In fact, our own reanalysis of the growth curve model examining Vineland socialization scores revealed that the inclusion of expressive language scores as a covariate resulted in a highly significant relationship between expressive language and socialization domain scores while the relationship between eye-mouth index scores and socialization domain scores became non-significant. Moreover, the significant relationship between smiling behavior at 6 months and rates of growth in socialization scores was not affected to the same degree by the inclusion of expressive language as a mediator – a finding that suggests that smiling behavior at 6 months is related to the development of social adaptation either more directly as a measure of the same construct, or indirectly through an altogether different developmental mechanism.
Despite the fact that we found a clear relationship between gaze to the mouth at 6 months and language development over the first two years, it is important to note that this finding was entirely independent of autism diagnoses at outcome or initial risk status at enrollment. Although we did find one indication for a risk-status effect in receptive language at 24 months, there were no group differences in gaze behaviors as predictors of language and, indeed, no group differences in gaze behavior itself aside from a trend for more high-risk infants in the lowest eye-preference group (the “LLL” group). Even this latter finding is tempered by the fact that the relationship between gaze to mouth and language was significant only for the interactive phases of the still face paradigm, a finding which encompasses both the “LLL” cluster and “LHL” cluster – or 44% of the entire sample, both low-risk (n=9) and high-risk (n=13) infants combined. Nevertheless, the findings for a relationship between gaze to mouth at 6 months and language development, though unexpected, are important in their own right for what they tell us about possible normative mechanisms of language development.
One area of early language development that has received intensive research focus is the mechanism by which infants are able to perceive meaningful components within the streams of speech to which they are constantly exposed (e.g., see Aslin, Jusczyk, & Pisoni, 1998
). The task of learning language – of word comprehension and articulation and expression – is perhaps initially facilitated by an infant’s ability to perceive the phonemic building blocks of spoken language (Aldridge, Stillman, & Bower, 2001
; Eimas, Siqueland, Jusczyk, & Vigorito, 1971
; Jusczyk & Aslin, 1995
; Maye, Werker, & Gerken, 2002
). Moreover, individual differences in such early speech perception abilities have been found to predict language development by 24 months of age in several recent longitudinal studies (Fernald, Perfors, & Marchman, 2006
; Newman, Ratner, Jusczyk, Jusczyk, & Dow, 2006
; Tsao, Liu, & Kuhl, 2004
). This suggests that any developmental phenomenon that might facilitate an infant’s early speech perception abilities might likewise facilitate later language development
Of particular relevance to our own data showing a relationship between gaze to mouth and expressive language is research on infants’ ability to integrate auditory and visual information in the service of speech perception. Several lines of research have demonstrated that visual attention to the mouth can profoundly influence and facilitate speech perception. Perhaps one of the most long-standing lines of research demonstrating this is the McGurk effect (McGurk & MacDonald, 1976
) which consists of the alteration of speech perception with the presentation of synchronized but unrelated audio and video input (e.g., the sound [ba] and the image of [ga] produces the perception of [da]). Even in infants as young as 2 months of age, visual input of speech is readily integrated with auditory input (Burnham & Dodd, 2004
; Kuhl & Meltzoff, 1982
; Patterson & Werker, 2003
). In paradigms using degraded auditory speech signals coupled with clear corresponding visual signals (e.g., Schwartz, Berthommier, & Savariaux, 2004
), research has also demonstrated that access to visual input allows the perceiver to “recover” what is lost in the auditory signal. Thus, although the acoustic properties of speech are undoubtedly important for learning language, the fact that visual attention to the mouth can greatly influence and facilitate language perception, coupled with the fact that such audiovisual integration appears to occur quite naturally even in 2 month old infants, it is reasonable to assume that the degree to which an infant focuses on his or her mother’s mouth during vocal face-to-face interactions may likewise facilitate speech perception and, in the long-run, language development.
Turning back to our own findings regarding the relationship between face scanning and language, individual differences in looking times to the mouth may index the degree to which infants utilize visual information of a speaker’s mouth to assist in the task of segmenting speech. This interpretation is supported by the fact that we found the relationship between gaze to the mouth and language development to be particularly strong only during the episodes when the mother was actively talking to the infant. The face scanning data recorded during the unresponsive still-face condition did not predict language development as strongly, particularly as measured by vocabulary size on the MacArthur.
Nevertheless, it might still be argued that speech perception is primarily, if not entirely dependent on acoustic properties of speech (Ohala, 1996
) and that individual differences in early speech perception abilities have little to do with visual attention to the mouth. In fact, it could be argued that our findings for an association between visual attention to the mouth and language development are spurious – that both of these phenomena are related to the mothers’ use of infant directed speech. To the extent that infant directed speech involves exaggerated articulation and prosody, it might also involve exaggerated movement – a visual aspect that may encourage greater amounts of looking behavior to the mouth but without any related facilitative effects on speech perception. Future research should include a measure of individual differences in audio-visual integration and cross-modal mapping in relation to visual attention to the mouth and later language development in order to better address these various interpretations.
Although our own data from 6 month olds does little to help predict the development of autism, it clearly suggests a normative developmental mechanism that might be involved in the development of language skills – a mechanism that was perhaps understandably overlooked in working backwards from prior research on older individuals with autism who look relatively little to the eyes when scanning faces. Armed now instead with a more developmentally appropriate hypothesis of the importance of looking to the mouth when learning language between 6 and 24 months of age, it is interesting to return to the question of early predictors for autism. Clearly, language development is severely affected in autism (see Tager-Flusberg & Caronna, 2007
for a review). Might it be possible that early audiovisual integration of speech perception is derailed in infants who later develop autism, and that this plays some role in their later deficits in language development? Could the poor language skills in the 3 children in our own sample who later developed autism be due in some small part to their failure to attend preferentially to the mouth during speech as an aid to learning language? Recent research examining audiovisual speech integration in adolescents with autism using a speech-in-noise paradigm, has indeed demonstrated significant deficits in such integration (Alacantra, Weisblatt, Moore, & Bolton, 2004
; Smith & Bennetto, 2007
). Moreover, this deficit is consistent with more general accounts of significant deficits in cross-modal integration (e.g., see Iarocci & McDonald, 2006
), and in the visual processing of biological motion (e.g., Blake, Turner, Smoski, Pozdol & Stone, 2003
; Gepner & Mestre, 2002
). Research on the links between cortical motor centers and speech perception (e.g., Fadiga, Craighero, Buccino, & Rizzolatti, 2002
; Pekkola et al., 2006
; Skipper, Nusbaum, & Small, 2005
) further suggests that deficits in audiovisual integration during speech perception might be a function of abnormalities in specific neural substrates underlying multisensory processing such as Broca’s area and the superior temporal sulcus. The degree to which such areas may be specifically impaired in autism compared to other disorders may ultimately provide important clues to the nature of language deficits in autism (cf., Oberman & Ramachandran, 2007
In conclusion, although we found no evidence for early markers of autism in gaze behavior and affective responsivity at 6 months of age, our findings do raise a number of issues and questions for future research. This lack of relationship may suggest that early behavioral signs emerge later in the first year of life for most children with autism. As such, future research employing longitudinal measurement of variables such as face scanning at multiple timepoints may be better suited to identify if and when variables such as gaze fixation to the eyes or mouth become abnormal in autism. Our results regarding language development and face scanning will also need to be replicated with a much larger sample, and refined using more sensitive measurements of language development, maternal speech characteristics, and infant face scanning behavior, collected more frequently during development. To the extent that these findings can be replicated and refined for typically developing infants and integrated with the extant developmental literature, it would then be informative to re-examine the role of face scanning in autism and to what extent abnormalities in face scanning are related to comorbid deficits in audiovisual integration, speech perception, and language development in a larger sample of young children already diagnosed with autism. After such groundwork has been done, the next question to be asked may be whether or not any of these newly detailed phenomena can be used as an early marker for autism.