Atypical brain activation patterns during a face-to-face joint attention game in adults with autism spectrum disorder

Abstract

Joint attention behaviors include initiating one's own and responding to another's bid for joint attention to an object, person, or topic. Joint attention abilities in autism are pervasively atypical, correlate with development of language and social abilities, and discriminate children with autism from other developmental disorders. Despite the importance of these behaviors, the neural correlates of joint attention in individuals with autism remain unclear. This paucity of data is likely due to the inherent challenge of acquiring data during a real-time social interaction. We used a novel experimental set-up in which participants engaged with an experimenter in an interactive face-to-face joint attention game during fMRI data acquisition. Both initiating and responding to joint attention behaviors were examined as well as a solo attention (SA) control condition. Participants included adults with autism spectrum disorder (ASD) (n = 13), a mean age- and sex-matched neurotypical group (n = 14), and a separate group of neurotypical adults (n = 22). Significant differences were found between groups within social-cognitive brain regions, including dorsal medial prefrontal cortex (dMPFC) and right posterior superior temporal sulcus (pSTS), during the RJA as compared to SA conditions. Region-of-interest analyses revealed a lack of signal differentiation between joint attention and control conditions within left pSTS and dMPFC in individuals with ASD. Within the pSTS, this lack of differentiation was characterized by reduced activation during joint attention and relative hyper-activation during SA. These findings suggest a possible failure of developmental neural specialization within the STS and dMPFC to joint attention in ASD.

Keywords: fMRI; medial prefrontal cortex; social; superior temporal sulcus.

Figure 1

ROI analysis of BOLD response to joint attention conditions by group. Regions of interest from the region‐of‐interest group of controls are displayed on a template image (P < 0.05, voxel‐ and cluster‐corrected). Percent signal change data were extracted from the peak 6–30 s across the block and averaged across condition within each region within each group. Data are plotted with percent signal change on the y‐axis and condition on the x‐axis separated by ASD and NT groups. Standard error of the mean is also plotted. The DMPFC and LpSTS show a significant group × condition interaction (indicated by a “*”) such that differences between joint attention (IJA and RJA) and SA are larger in the NT group than ASD.

Figure 2

Behavioral data from ASD (blue) and NT (red) groups are shown for five behavioral measures. Accuracy (A) is defined as the percent of trials in which the mouse appeared due to a correct fixation to the target location. In the joint attention conditions, both experimenter and subject were required to make a correct fixation to the target location. Eye movements (B) are the averages of the total number of eye movements that occurred within each block. Latency to mouse appearance (C) is the latency to the joint (or solo for SA) attention event and (D) is the length of that joint (or solo for SA) attention event. The latency to first eye movement (E) is defined as the latency between the start of the trial and the subject's first eye movement.

Figure 3

Within‐group comparisons of RJA (A) and IJA (B) in NT (red) and ASD (blue) groups. Group t‐maps are displayed on a template image. Maps are set at a threshold of P < 0.001, voxel‐corrected at P < 0.05.