Using Interactive Eye-Tracking and fMRI to Investigate Joint Attention in Children and Adolescents with and without Autism Spectrum Disorder

Background: Joint attention (JA) refers to the shared attentional focus of at least two people on a specific object and is an essential prerequisite for the development of early social interaction skills. Concurrently, deficits in JA are considered the earliest sign to be at risk for autism spectrum disorder (ASD), suggesting a more protracted development in ASD. The neurodevelopment of JA is poorly understood (Schilbach et al., 2013), in particular with respect to influences such as the familiarity of the interaction partner and self- vs. other-initiation of JA. Only recently, JA has been investigated in adults using interactive fMRI paradigms (Redcay et al., 2010; Schilbach et al., 2010).

Objectives: We examined neural correlates of JA and its modulation by a familiar and unfamiliar interaction partner and by self- and other-initiated JA during typical development, and atypical patterns in patients with ASD.

Methods: We used an interactive eye-tracking setup (Wilms et al. 2010), in which participants were looking at a face surrounded by three targets (left, right and top). In the Self-Initiated conditions, participants shifted their gaze towards one of the three targets. In the JA Self-Initiated condition, the interaction partner followed the participant’s gaze. In the Control Self-Initiated condition, the interaction partner shifted her gaze downwards. In the JA Other-Initiated condition, participants were instructed to follow the interaction partner’s gaze. In the Control Cue-Initiated condition, participants were instructed to shift the gaze towards the target that changed color while the interaction partner shifted her gaze downwards. Our current analysis includes 39 TD (8-18 years) and 10 ASD subjects (8-18 years). Brain imaging data were analyzed with SPM8, using a flexible factorial ANOVA model (random effects analysis, threshold: p<0.05 cluster-level FWE corrected, voxel level p<0.001).

Results: Irrespective of age, TD subjects recruited a JA network comparable to findings in adults with only minor effects of age. The JA network encompassed areas related to reward and motivation (ventral striatum, bilateral Acc, pallidum, OFC), spatial orientation and movement control (e.g. superior and inferior parietal lobe) as well as motor processing (precentral gyrus). Our data indicates that the degree of familiarity of the interaction partner significantly modulates brain activity, in particular during self-initiated interactions. These effects were mainly confined to brain areas recruited by JA across conditions (inferior parietal lobe extending into to precuneus), suggesting enhanced processing for familiar interaction partners, which is functionally specific for JA. Furthermore, additional emotion processing areas (e.g. insula) were activated significantly stronger during self-initiated interactions than during other-initiated interactions suggesting enhanced emotional involvement. Further data analysis with respect to atypical development in ASD will follow. 

Conclusions: Our results suggest early maturity of JA in typical development not only on the behavioral but also on the neural level. However, modulation by familiarity and self- vs. other initiation of JA reveals further insights into the neural underpinnings of JA and its development. Comparison to atypical (potentially protracted) development in ASD will further advance the understanding of JA deficits in ASD.