King’s Research Portal DOI: 10.3389/fpsyg.2019.01799 Document Version Publisher's PDF, also known as Version of record Link to publication record in King's Research Portal Citation for published version (APA): Parsons, J. P., Bedford, R., Jones, E. J. H., Charman, T., Johnson, M. H., & Gliga, T. (2019). Gaze following and attention to objects in infants at familial risk for ASD. Frontiers in Psychology, 10(JULY), [1799]. https://doi.org/10.3389/fpsyg.2019.01799 Citing this paper Please note that where the full-text provided on King's Research Portal is the Author Accepted Manuscript or Post-Print version this may differ from the final Published version. If citing, it is advised that you check and use the publisher's definitive version for pagination, volume/issue, and date of publication details. And where the final published version is provided on the Research Portal, if citing you are again advised to check the publisher's website for any subsequent corrections. 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Oct. 2021 fpsyg-10-01799 August 17, 2019 Time: 15:44 # 1 ORIGINAL RESEARCH published: 20 August 2019 doi: 10.3389/fpsyg.2019.01799 Gaze Following and Attention to Objects in Infants at Familial Risk for ASD Janet P. Parsons1, Rachael Bedford2, Emily J. H. Jones1*, Tony Charman3 Mark H. Johnson1,4 and Teodora Gliga1,5* on behalf of the BASIS Team 1 Centre for Brain and Cognitive Development, Birkbeck, University of London, London, United Kingdom, 2 Biostatistics Department, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom, 3 Department of Psychology, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, London, United Kingdom, 4 Department of Psychology, University of Cambridge, Cambridge, United Kingdom, 5 Department of Psychology, University of East Anglia, Norwich, United Kingdom Reduced gaze following has been associated previously with lower language scores in children with autism spectrum disorder (ASD). Here, we use eye-tracking in a controlled experimental setting to investigate whether gaze following and attention distribution Edited by: during a word learning task associate with later developmental and clinical outcomes in Jo Van Herwegen, a population of infants at familial risk for ASD. Fifteen-month-old infants (n = 124; n = 101 Kingston University, United Kingdom with familial risk) watched an actress repeatedly gaze toward and label one of two Reviewed by: Carmel Houston-Price, objects present in front of her. We show that infants who later developed ASD followed University of Reading, gaze as frequently as typically developing peers but spent less time engaged with United Kingdom Rechele Brooks, either object. Moreover, more time spent on faces and less on objects was associated University of Washington, with lower concurrent or later verbal abilities, but not with later symptom severity. United States No outcome group showed evidence for word learning. Thus, atypical distribution of *Correspondence: attention rather than poor gaze following is a limiting factor for language development in Emily J. H. Jones [email protected] infants at familial risk for ASD. Teodora Gliga [email protected]; Keywords: gaze following, infants, familial risk, ASD, eye-tracking [email protected] Specialty section: INTRODUCTION This article was submitted to Developmental Psychology, Typically developing infants are sensitive to others’ gaze from birth (Batki et al., 2000; Farroni a section of the journal et al., 2002). Over the first year they follow gaze first reflexively (Hood et al., 1998; Farroni et al., Frontiers in Psychology 2000, 2004) and then learn its referential function (Woodward, 2003; Csibra and Volein, 2008; Received: 12 February 2019 Senju et al., 2008). Being able to follow someone’s gaze, and jointly attend to objects, is thought Accepted: 19 July 2019 to provide a key mechanism by which infants acquire a vocabulary (Baldwin, 1991, 1993; Schafer Published: 20 August 2019 and Plunkett, 1998; Houston-Price et al., 2006) and many studies have associated joint attention Citation: ability with later vocabulary growth (Carpenter et al., 1998; Morales et al., 1998; Charman, 2003; Parsons JP, Bedford R, Brooks and Meltzoff, 2008). Jones EJH, Charman T, Johnson MH Children with autism spectrum disorder (ASD) often have poor joint attention, evidenced by and Gliga T (2019) Gaze Following and Attention to Objects in Infants reduced gaze following in naturalistic situations (e.g., Dawson et al., 2004), and this has been at Familial Risk for ASD. highlighted as one of the most reliable and consistent indicators of ASD during childhood (e.g., Front. Psychol. 10:1799. Baron-Cohen et al., 1996; Charman, 2003). Given that the rate of learning difficulty is often doi: 10.3389/fpsyg.2019.01799 high in children with ASD (∼55%; Charman et al., 2011) and there is frequent language delay Frontiers in Psychology| www.frontiersin.org 1 August 2019| Volume 10| Article 1799 fpsyg-10-01799 August 17, 2019 Time: 15:44 # 2 Parsons et al. Gaze Following in Infants At-Risk for ASD (e.g., Charman et al., 2003), studies have suggested that poor in ASD particularly when the face addresses the child (Shic et al., language in ASD may be explained, in part, by difficulties 2014) or when it establishes mutual gaze (Nyström et al., 2017). with engaging in joint attention (e.g., Mundy et al., 1994; One study has directly addressed the question of whether directed Pickard and Ingersoll, 2015). For example, in their study of communication is particularly problematic (Vernetti et al., 2018). children between 22 to 93 months of age, Pickard and Ingersoll In this study, toddlers could choose between animating (by used the Early Social Communication Scales, a play-based looking at them) either a video of a person that established eye structured assessment that captures both the child’s initiating contact and directly addressed them, or a video of a spinning and responding to joint attention, to show that failing to follow mechanical toy. There was no difference between those with someone’s gaze or pointing to an object were best predictors of a later diagnosis of ASD and those without, with all groups concurrent language. In addition, an intervention targeting joint choosing to animate and engage longer with the face rather than attention in children with ASD yielded better expressive language the toy. Those studies which have analyzed dwell time to the face outcomes when compared to an intervention increasing symbolic during gaze following have also failed to find group differences play (Gulsrud et al., 2014). (Chawarska et al., 2012; Billeci et al., 2016; Vivanti et al., 2017), There are several reasons why children with ASD may struggle suggesting that poor gaze following in ASD may not be due to to use joint attention for learning language. Firstly, they may not insufficient engagement with faces. correctly or consistently follow someone’s gaze to the object they During infancy and early toddlerhood, eye-tracking studies are labeling. This could be because they do not spend enough time are consistent in suggesting that the ability to shift one’s gaze looking at faces to notice or process the gaze shifts. Alternatively, to follow someone else’s gaze direction to an object (henceforth despite looking at faces and eyes, they still may not shift their referent) rather than an equally salient distractor, is intact in gaze in the same direction as the person communicating with toddlers with ASD or infants with later ASD, with differences them. It could also be that, despite correctly following gaze, appearing to emerge later in development (see Table 1.2). There they do not spend enough time on the gazed at object to learn is, however, a more mixed picture when studies analyzed the about it. Looking less toward the gazed at object may also dwell time on objects, with most studies finding decreased reflect poor understanding of the referential nature of gaze. That looking toward the gazed at objects, but a few finding no is, word learning could fail not because there was insufficient differences (see Table 1.3). Some of the inconsistency in findings time dedicated to encoding object properties, but because unlike may reflect differences in the way engagement with objects was typically-developing children (Gliga and Csibra, 2009), children measured. Researchers either directly compared time spent on with ASD may have a reduced appreciation of the referential link referent versus distractor or contrasted time spent on the referent between the uttered word and the gazed at object. to time spent on all areas of interest (AOI), including the face Recently, eye-tracking studies have allowed a detailed or the background. While the former measure directly assesses quantification of attention distribution during joint attention an understanding of which object is the referent of the gaze, the episodes, thus making it possible to reveal the different sources of latter measure also captures infants’ engagement with irrelevant atypicality mentioned above. Eye-tracking studies investigating aspects of the scene or differences in looking toward the face.