A substantial and unexpected enhancement of motion perception in autism

Abstract

Atypical perceptual processing in autism spectrum disorder (ASD) is well documented. In addition, growing evidence supports the hypothesis that an excitatory/inhibitory neurochemical imbalance might underlie ASD. Here we investigated putative behavioral consequences of the excitatory/inhibitory imbalance in the context of visual motion perception. As stimulus size increases, typical observers exhibit marked impairments in perceiving motion of high-contrast stimuli. This result, termed "spatial suppression," is believed to reflect inhibitory motion-processing mechanisms. Motion processing is also affected by gain control, an inhibitory mechanism that underlies saturation of neural responses at high contrast. Motivated by these behavioral correlates of inhibitory function, we investigated motion perception in human children with ASD (n = 20) and typical development (n = 26). At high contrast, both groups exhibited similar impairments in motion perception with increasing stimulus size, revealing no apparent differences in spatial suppression. However, there was a substantial enhancement of motion perception in ASD: children with ASD exhibited a consistent twofold improvement in perceiving motion. Hypothesizing that this enhancement might indicate abnormal weakening of response gain control, we repeated our measurements at low contrast, where the effects of gain control should be negligible. At low contrast, we indeed found no group differences in motion discrimination thresholds. These low-contrast results, however, revealed weaker spatial suppression in ASD, suggesting the possibility that gain control abnormalities in ASD might have masked spatial suppression differences at high contrast. Overall, we report a pattern of motion perception abnormalities in ASD that includes substantial enhancements at high contrast and is consistent with an underlying excitatory/inhibitory imbalance.

Figure 1.

Stimuli and task. A, Sequence of events constituting a single trial. B, Space–time illustration showing a small stimulus (1°) moving to the right. The depicted duration (25.6 ms) equals the average ASD threshold for this condition at high contrast (Fig. 2A). C, Stimulus sizes used in the study (radius = 1°, 2.5°, and 6°). Only one stimulus was shown per trial.

Figure 2.

Motion discrimination performance and spatial suppression strength at high contrast. A, Comparison of duration thresholds for discriminating high-contrast motion in participants with ASD and TD. Results reveal a substantial enhancement of motion perception in ASD that is independent of stimulus size. The insert shows data for participants who completed both low- and high-contrast experiments. B, Suppression index scores (computed as the difference of log₁₀duration thresholds for large versus small motion stimuli) do not differ between ASD and TD groups. Error bars in A and B represent SEM. C, Box-and-whisker plots showing robust separation of results for participants with ASD and TD. Thick lines indicate median performance. Boxes indicate the interquartile range and whiskers show the data range exclusive of outliers. Outliers (filled circles) are defined as data points >1.5 times the interquartile range beyond the first and the third quartiles. For each stimulus size, the median TD performance approximately equals the threshold exhibited by the worst-performing participant with ASD. Note the different y-axis range for the rightmost plot.

Figure 3.

Motion discrimination performance and spatial summation strength at low contrast. A, Comparison of duration thresholds for discriminating low-contrast motion in participants with ASD and TD. Unlike high-contrast results, there are no substantial differences between groups except an increase in the TD (but not ASD) thresholds for the largest stimulus size (shown by the arrow). The insert shows data for participants who completed both low- and high-contrast experiments. B, Suppression index scores were negative for both groups, indicating spatial summation at low contrast. However, participants with TD also exhibited signs of spatial suppression (A, arrow). This was evident as a significant difference in suppression index score between the two groups. Error bars in both panels represent SEM.

Figure 4.

Effects of contrast on motion direction discriminations for participants with TD and ASD. A, Effect of increasing stimulus contrast on direction discrimination thresholds for small moving stimuli. This plot is constructed by combining the leftmost data points in Figure 2A and Figure 3A and replotting these data as a function of stimulus contrast. B, Same as in A, except that only data from participants who completed both low- and high-contrast experiments are included. Error bars in both panels represent SEM.