Previous research has shown that individuals with AS display an increased drive for social engagement, and imitate adults showing an “emotionally playful” attitude more often compared to “neutral” adults. In our previous study this modulation was more pronounced compared to typically-developing children7.
Against this background, the present study examined whether children with AS show increased social attention, as indicated by a higher proportion of fixations duration towards faces versus actions, and an increased social-emotional responsivity, expressed by the total fixations duration and proportion of fixations duration to emotionally engaging stimuli versus neutral ones. We found a mixed pattern of results, with limited support for our initial hypotheses. Although, as predicted, the face of the actors in video-stimuli elicited higher proportion of fixations duration than her actions across conditions in both groups, our hypothesis that the increased proportion of fixations duration to the actor’s face versus her actions would be more pronounced in participants with AS was not supported. Indeed, contrary to our hypotheses, the increased proportion of fixations duration to faces versus actions was more pronounced in the CG compared to the ASG, and overall participants with AS proportionally watched the face of the actor depicted in the video-stimuli to a lesser degree compared to mental age-matched typical participants.
Additionally, although our prediction that the emotionally engaging condition would elicit higher proportion of fixations duration towards the actor’s face compared to the neutral condition across groups was supported, we found no evidence supporting our prediction that the increased proportion of fixations duration towards the actor’s face in the playful versus neutral condition would be more pronounced in the ASG. Another relevant finding is that participants in the ASG spent significantly less time watching the screen compared to the CG. This pattern of results suggests that, in the context of an overall reduced attentional engagement with the stimuli presented to them, children with AS increase their proportion of fixations duration in response to social-emotional signals (the playfulness expressed by the actor’s face) but not more than children in the comparison group. Additionally, their tendency to increase their proportion of fixations duration in response to faces versus actions appeared to be lower than in neuro-typical children. Taken together, these results are inconsistent with the notion of hyper-responsivity to social and emotional stimuli in children with AS upon which our hypotheses were developed.
Importantly, however our finding that individuals with AS showed a lower proportion of fixations duration to the actor’s face compared to participants in the CG is consistent with the only previous study that used eye-tracking in subjects with AS17. The lower proportion of fixations duration towards face stimuli presented on a screen compared to mental age-matched controls is unlikely to be explained by general intellectual reasoning deficits in AS, as in both studies a reduced fixations duration was documented in comparison to participants with a similar mental age. Another possibility is that group differences observed in our findings reflect a general attentional problem in AS (e.g. increased distractibility). However, the proportion of fixations duration towards the action performed by the actor on the screen was similar across groups, suggesting that general attentional deficits, while present, might not be a satisfying explanation for the differential proportion of fixations duration to the face area. It is therefore plausible that the reduced visual engagement with the actor’s face documented in the ASG reflects a distinctive clinical manifestation related to the social domain that co-exists with a general inattentiveness, rather than reflecting a mere byproduct of intellectual disability or inattentiveness/distractibility. Reduced social attention might also be related to reduced social reasoning in AS by virtue of reflecting an abnormally heightened arousal in response to social stimuli, which might lead to both increased social approach and social processing difficulties, as observed in Williams syndrome13.
Additionally, we found that, despite an overall reduced total fixations duration to the screen, children with AS modulate their attention in response to the emotional signals expressed by the actors in the video. These sensitivity and responsiveness to social-emotional signals are consistent with the clinical presentation of AS. Indeed, individuals with AS are known to have prominent interest in social interaction18; they laugh and smile with a high frequency with familiar people, when eye contact is maintained19 and when it is elicited by social environmental stimuli20; additionally they show responsivity to social-communicative cues, imitating adults who act in a socially engaging manner versus a neutral one7.
Finally, the current results show that, counterintuitively, children in the ASG who had longer fixations duration to the screen across conditions and areas of interest had lower mental and chronological age. This unexpected negative correlation between the mental/chronological age and total duration of fixations in AS could be due to the child-oriented video content being of less interest to the older participants (i.e. those with more social experience could have found the depicted actions not as engaging as the younger children). A negative correlation between age and social engagement, expressed in a reduced amount of time watching different pictures representing happy faces, has been previously found in children with Rett syndrome21, and attributed to the consequences of their non-verbal and limited communication abilities reducing opportunities for social experiences and affecting social interest. Adams et al.4 showed age-related changes in the sociability of children with AS, reporting not only a decrease in the duration of laughing and smiling as the children get older, but also reduced responsivity to social interaction and eye contact. This age-related decline in social motivation and responsivity may contribute to the counterintuitive negative correlation between chronological/mental age and attention to the stimuli in our study, but further research is needed to substantiate this explanation.
Several implications can be drawn from the study findings. First, the findings are aligned with the literature documenting that typically developing children increase their attentional engagement when viewing stimuli that are more socially salient (faces as opposed to actions) and more emotionally salient (playful versus neutral actions). This phenomenon is considered to play a critical role in the development of social communication, as an increased engagement with social and emotional stimuli allows children to register and respond to important social cues like gaze direction, affect, as well as other verbal and nonverbal information. The prioritization of frequent engagement with these stimuli over non-social and non-emotional stimuli, in turn, is believed to shape neural specialization and behavioral expertise in the social domain during sensitive periods22,23,24.
Importantly, our study found that children with AS also attend more to social versus non-social and emotional versus neutral stimuli – however, this modulation is not more pronounced in this group as we predicted. Indeed, the unusual social phenotype in AS, characterized by both social processing impairments (e.g. difficulties in joint attention) and increased motivation for social approach, led us to hypothesize that children with this condition are hyper-responsive to social and emotional stimuli. This notion could provide a potential explanation for both processing difficulties, as a hyper-response to social stimuli could affect cognitive processing in the social domain while enhancing social motivation. However, our results are not consistent with this explanation, pointing to the need for different explanatory frameworks for the complex social phenotype of those with AS. Importantly, our finding that children with AS preferentially attend social and emotional stimuli points to the potential for interventions to capitalize on social attention and social-emotional modulation to facilitate early learning. Several intervention practices developed for other neurodevelopmental conditions are designed to increase the saliency of social signals (e.g. through exaggerated facial and affective cues) to enhance attentional engagement and processing of others’ communication and actions25. Recent research has shown that these techniques can facilitate early learning across a variety of domains, including areas that are affected in AS, such as joint attention, imitation and adaptive social behaviors26. Our results provide a rationale for extending such interventions to children with AS.
Our study has several limitations that should be acknowledged. First, the stimuli presented to participants were displayed through a computer screen, providing an experience that might be processed differently compared to real-life interactions. This could have disproportionally penalized participants in ASG, as AS has been associated with neuro-visual dysfunctions affecting the processing of complex visual scenes27,28,29, difficulties in recognising facial expressions and difficulties processing “impoverished” visual information, such as the 2-D information presented via the computer screen30,31. Although these visual-attentional difficulties could have contributed to our findings, the ASG had proportion of fixations duration towards the action area similar to CG and normative emotional modulation, suggesting that our paradigm was able to capture social-domain specific patterns. However, a live version of the paradigm would have allowed ascertaining whether group differences documented here reflected a true reduction in social attention versus difficulties specific to processing 2-D social information30,31. Such a paradigm could be coupled with the use of eye-tracking glasses to maximise both ecological validity and measurement precision.
Another limitation is the wide range in chronological age in the ASG, due to the recruitment difficulties associated with the low prevalence of this syndrome. Additionally, the groups were not gender-matched. However, no gender effect was found across our variables of interest.
One additional limitation is the use of a comparison group matched by mental age but not chronological age. Although this strategy was designed to ensure that participants had similar general intellectual reasoning abilities across groups, future research should attempt to replicate our results using alternative matching strategies, including both chronological and mental age-matched comparison groups. Importantly, the chronological age difference between the groups could have affected results due to the different histories of social experiences in the two groups. However, although participants in the ASG had theoretically a longer history of social interactions than control participants by virtue of being older, cognitive impairments associated with AS likely limited the breadth and range of social experiences – consistent with our finding that older children in the ASG did not show more social attention and other literature with other syndromic conditions and similar intellectual profile21. Furthermore, several factors that were not controlled for in the analyses could have affected participants’ performance. These include the gender (female) of the actors in the videos (although research suggests that males and females are attended to a similar amount of time in children in the age range of participants in the study32,33), as well as treatments and interventions received by participants in the AS group. For example, specific trainings addressing maladaptive behaviors in the social domain (e.g. aggression, inappropriate social approach) could have affected results directly (contributing to attentional social engagement with the stimuli) or indirectly (by affecting compliance with instructions). An additional limitation is that the study did not assess how eye-tracking patterns related to clinical dimensions of AS other than mental age, including maladaptive behaviors, thus limiting the implication that can be derived from the results. Future research should examine the potential role of these and other factors that were not controlled for or measured in the current study, and also focus on a more fine-grained analysis of moment-by-moment changes in the position of fixations to examine to gain more insight into how events displayed in the videos affect gaze patterns in this population.
Despite these limitations, to our knowledge, this is the first controlled study focusing on social attention and social modulation of attention in individuals with AS, thus providing new insights into the social phenotype of this under-studied population.
In conclusion, our study documented both typical social processes (increased proportion of fixations duration towards social-emotional versus neutral stimuli) and atypical ones (diminished proportion of fixations duration towards faces) in individuals with AS, and did not support the notion of enhanced social attention or social modulation in this population. Further research is needed to substantiate these results and to examine domain-general and social domain-specific mechanisms underlying these puzzling phenomena.