Visual attention and inhibitory control in children, teenagers and adults with autism without intellectual disability: results of oculomotor tasks from a 2-year longitudinal follow-up study (InFoR)

Abstract

Background: Inhibitory control and attention processing atypicalities are implicated in various diseases, including autism spectrum disorders (ASD). These cognitive functions can be tested by using visually guided saccade-based paradigms in children, adolescents and adults to determine the time course of such disorders.

Methods: In this study, using Gap, Step, Overlap and Antisaccade tasks, we analyzed the oculomotor behavior of 82 children, teenagers and adults with high functioning ASD and their peer typically developing (TD) controls in a two-year follow-up study under the auspices of the InFoR-Autism project. Analysis of correlations between oculomotors task measurements and diagnostic assessment of attentional (ADHD-RS and ADHD comorbidity indices) and executive functioning (BRIEF scales) were conducted in order to evaluate their relationship with the oculomotor performance of participants with ASD.

Results: As indicated by the presence of a Gap and Overlap effects in all age groups, the oculomotor performances of ASD participants showed a preserved capability in overt attention switching. In contrast, the difference in performances of ASD participants in the Antisaccade task, compared to their TD peers, indicated an atypical development of inhibition and executive functions. From correlation analysis between our oculomotor data and ADHD comorbidity index, and scores of attention and executive function difficulties, our findings support the hypothesis that a specific dysfunction of inhibition skills occurs in ASD participants that is independent of the presence of ADHD comorbidity.

Limitations: These include the relatively small sample size of the ASD group over the study's two-year period, the absence of an ADHD-only control group and the evaluation of a TD control group solely at the study's inception.

Conclusions: Children and teenagers with ASD have greater difficulty in attention switching and inhibiting prepotent stimuli. Adults with ASD can overcome these difficulties, but, similar to teenagers and children with ASD, they make more erroneous and anticipatory saccades and display a greater trial-to-trial variability in all oculomotor tasks compared to their peers. Our results are indicative of a developmental delay in the maturation of executive and attentional functioning in ASD and of a specific impairment in inhibitory control.

Trial registration: ClinicalTrials.gov NCT02628808.

Keywords: Antisaccade task; Attention shifting; Autism spectrum disorders (ASD); Eye-tracking; Gap–Overlap–Step tasks; Inhibitory control; Oculomotor behavior.

Fig. 1

Experimental design. From left to right: Gap, Step, Overlap and Antisaccade tasks. As indicated by the white arrows (in lower panels), in the first three tasks, after an initial center screen fixation (green boxes), participants had to move their gaze toward a peripheral target (red squares) as soon as it appeared on the screen. The central anchoring point (green square) disappeared prior to (Gap task) or coincident with (Step task, i.e., 0-Gap) the peripheral target’s appearance, or it remained on screen along with target in the Overlap task. In the Antisaccade task, participants had to move their eyes in the opposite direction to that of the target. The Gap, Step and Overlap tasks allow the evaluation of attention disengagement by means of the Gap (Gap latency < Step latency) and Overlap effects (Step latency < Overlap latency). The Antisaccade task allows assessment of inhibitory control (Gap latency < Antisaccade latency)

Fig. 2

Gap and Overlap task effects. A Plots of mean latency values in the three tasks (All participants, N = 146). Note the progressive significant increase in latency from Gap to Overlap task. B Gap (B1) and Overlap (B2) effects assessed by computing the differences in latency between Step and Gap tasks and between Overlap and Step tasks. A Adults (N = 64); C children (N = 42); T: teenagers (N = 40). C Plots of mean coefficient of variation (COV) of latency values in the three tasks (All participants, N = 146). Bars indicate the standard error of the mean; *p < 0.05

Fig. 3

Anticipatory saccade. Plots of mean percentage of anticipatory saccades performed in the three tasks. ASD participants made significantly more anticipatory saccades than their TD peers in the three tasks. Bars indicate the standard error of the mean; *p < 0.05

Fig. 4

Analysis of accuracy in Gap, Step and Overlap tasks. A Plots of mean gain values. There was a significant difference in gain to first fixation between ASD and TD participants (A1), in the course of development (A2) and between tasks (A3). B Plots of mean coefficient of variation of gain values. While there were no significant differences between ASD and TD participants, there was a significant developmental improvement between age groups (B2), and between tasks. Bars indicate the standard error of the mean; *p < 0.05

Fig. 5

Antisaccade task effects. A Plots of mean differences in latency between Gap and Antisaccade tasks indicating significant differences between clinical groups for children and teenagers. B Plots of mean gain values indicate significant differences between age groups and significant differences in accuracy in the Gap task versus Antisaccade task for ASD participants. C ASD participants performed more erroneous saccades in the Antisaccade task compared to Gap task and more than TD participants in the Antisaccade task (C1). The percentage of erroneous saccades decreased over development (C2). D Plots of mean coefficient of variation of latency (D1)/gain (D2) indicating significant differences between the two tasks. Bars indicate the standard error of the mean; *p < 0.05

Fig. 6

Correlations between oculomotor variables and clinical measures. A Correlation plots were drawn for ASD participants between ADHD-RS total score and delta Overlap–Gap, erroneous saccade percentage and gain (averaged values from all trials in prosaccade tasks. B Correlation plots were drawn for all participants between BRIEF-GEC and delta Overlap–Gap, erroneous saccade percentage and gain (averaged values from all trials in prosaccade tasks). Bars indicate the standard error of the mean; *p < 0.05

Fig. 7

Analysis of changes in oculomotor variables over 2 years of follow-up. A Plots of mean latency difference values to assess changes in Gap and Overlap effects over 2 years. B Plots of mean gain values over 2 years. T0: Study onset; Y1: year 1; Y2: year 2. Bars indicate the standard error of the mean; *p < 0.05