Eye gaze differences in school scenes between preschool children and adolescents with high-functioning autism spectrum disorder and those with typical development

This study evaluated 79 Japanese students: 30 high-functioning children with ASD and 49 children with TD. Participants from two discontinuous age groups were included: preschool children age 3–6 years with no previous classroom experience and adolescents age 11–15 years who had attended elementary school or junior high school. The study compared the eye gaze behavior of four groups: 25 preschool children with TD (7 boys), 12 preschool children with ASD (9 boys), 24 adolescents with TD (11 boys), and 18 adolescents with ASD (11 boys). Exclusion criteria were any past or present psychiatric illness; difficulties in eye movement or visual function; and inability to accomplish the 10-min experiment described in the Methods section. Written informed consent for all student–participants was obtained from their parents.

High-functioning ASD was diagnosed by specialists in the field of pediatric neurology and/or developmental pediatrics according to the following criteria:

The CARS score indicates the severity of autism and originally considered that scores < 30 indicated no autism and scores > 30 indicated mild-to-moderate or severe autism [18]. However, Tachimori et al. [20] recently reported that children diagnosed with Asperger syndrome could be distinguished from those without ASD using cutoff values of 25.5 versus 26.0, respectively. The present study also used this criterion to differentiate children with ASD from children with TD (CARS score 25.5 vs. 26.0, respectively). The Japanese version of the PARS-TR [19] was administered in a semi-structured interview with a parent or family member of the child. This scale evaluates both the current symptoms and the most pronounced symptoms during infancy, defined by the PARS-TR peak symptoms scale. A significant correlation exists between PARS-TR scores and Autism Diagnostic Interview-Revised (ADI-R) scores, particularly between qualitative abnormalities in the reciprocal social interaction component in the ADI-R score and the social communication component in the PARS-TR score [21].

The research was approved by the Ethics Committee of Kansai Medical University (No. 1100).

Experiments were conducted in a quiet, well-lit room at Kansai Medical University Medical Center. Participants were seated in front of a 48 × 30 cm monitor for the presentation of visual stimuli, and their chins were placed on a chin rest to minimize head movement. The distance between the monitor and the chin rest was 60 cm. Partitions were placed to ensure that only the monitor was within the participant’s field of vision. On the monitor, two social images—a smiling human face and a classroom scene in a high school setting (Fig. 1)—were presented sequentially, once for each image, with no sound. Each stimulus was shown for 9 s followed by an intertrial interval of 1 s. The duration of the whole experiment was approximately 10 min (Fig. 1, row 1). The participants were instructed to freely watch the static visual images on the monitor. The eye gaze position was measured at 250 Hz using an infrared camera attached to the bottom of the monitor (iView X RED, SensoMotoric Instruments, Teltow, Germany). Eye tracking data were analyzed using a customized software program written in MATLAB (MathWorks, Natick, MA, USA).

Of the 79 participants, five could not complete the 10-min experiment (4 for a human face; 1 participant for a classroom scene) and thus were excluded from the following analyses.

To compare the eye gaze behavior of children with TD and children with ASD and that of preschool children and adolescents, the testing first identified the visual areas that were regions of interest (ROIs) (Fig. 1, row 2). The ROIs were set as the eyes and mouth for the human face image and the face, pointing finger, and object pointed at by the teacher in the classroom image. The eye gaze time of preschool children with ASD and those with TD was compared for each ROI using the Welch t-test. The same was done for adolescents with ASD and those with TD. Within the 9 s of each stimulus presentation, the duration of the gaze in each ROI was measured. Statistical analyses were performed using the statistical software SPSS version 22.0 (IBM Corp., Armonk, NY, USA).

For the developmental assessment of patients with ASD, the means ± standard deviations were as follows: preschool DQ 87.3 ± 14.5 and adolescent FSIQ 96.0 ± 13.7. The mean CARS score of participants with ASD was 28.1 ± 3.6. The mean PARS-TR peak symptom scale score was 30.4 ± 5.4, and the mean current symptom score was 21.0 ± 9.8. These scores were higher than both the cutoff value of 25.5 for CARS for 9 preschool and 13 for elementary school students and the cutoff value for the relevant age group (adolescent/adult) for PARS in 20 junior high school students. These findings mean that autism symptoms were obvious in patients with ASD.

Figure 1 illustrates the representative eye gaze patterns of children with TD and ASD. For the human face stimulus (Fig. 1, left column), TD children held their gaze longer on the eyes and mouth (row 3), whereas ASD children gazed longer on the points between eyes and mouth or the wall, and two participants with ASD never looked at the face (row 4). For the classroom scene (right column), TD children gazed longer at the areas near the teacher’s face and at the object to which the teacher pointed. Conversely, ASD children tended to gaze longer at a location irrelevant to the class, such as the center of the screen, the pencil case on the desk, or the wall. These ASD children almost never looked at the teacher’s face or the object that was pointed out.

Figure 2 presents a box and whisker plot of eye gaze duration for the ROIs of the human face and the classroom scene. A statistically significant neurodevelopmental effect on the duration of the gaze was observed (Table 1). The Welch t test revealed a significant difference between TD and ASD preschool children when they gazed at the object pointed at [t(21) = 4.83, p = 0.039], whereas adolescents with TD tended to look at the object pointed at longer than did those with ASD [t(39) = 3.20, p = 0.081].

Notably, despite the lack of classroom experience for preschool children with TD, they looked at the teacher’s face and the pointed-at object. Moreover, although the shortened gaze duration in preschool children with ASD was evident for the smiling human face image, the difference was not significant for the same face presented within the classroom image. Preschool children with TD gazed significantly longer at the eyes of the human face image than did preschool ASD children [t(31) = 11.7, p = 0.002]. No significant difference was observed between TD and ASD adolescents for gaze duration at the human face image [t(39) = 1.42, p = 0.241].