Perceptual Center-Surround Contrast Suppression in Adolescence

Abstract

Purpose: Center-surround contrast suppression-typically induced when a center pattern is surrounded by another pattern with similar spatial features-is considered a perceptual analogue of center-surround neurophysiology in the visual system. Surround suppression strength is altered in a range of brain conditions affecting young people (e.g., schizophrenia, depression, migraine) and is modulated by various neurotransmitters. The early teen years are associated with neurotransmitter changes in the human visual cortex, which could impact on excitation-inhibition balance and center-surround antagonistic effects. Hence, we predict that early adolescence is associated with perceptual changes in center-surround suppression.

Methods: In this cross-sectional study, we tested 196 students at every age from 10 to 17 years and 30 adults (aged 21-34 years) to capture the preteen, adolescent, and adult periods. Contrast discrimination thresholds were measured for a central, circular, vertical sinusoidal grating pattern (0.67° radius, 2 cyc/deg spatial frequency, 2 deg/s drift rate) with and without the surround (4° radius, otherwise same spatial properties as the center). Individual suppression strength was determined by comparing the perceived contrast of the target with and without the surround.

Results: After excluding unreliable data (7% of total), we found an effect of age on perceptual center-surround contrast suppression strength, F(8,201) = 2.30, P = 0.02, with weaker suppression in the youngest adolescents relative to adults (Bonferroni pairwise comparisons between adults vs 12-year-olds P = 0.01; adults vs 13-year-olds P = 0.002).

Conclusions: Our data demonstrate different center-surround interactions in the visual system-a key building block for visual perception-in early adolescence relative to adulthood.

Figure 1.

Example test stimulus presentation for the (A) no surround and (B) surround conditions. The stimulus on the left was the reference stimulus of fixed contrast (40% center, 95% surround). The stimulus on the right varied in contrast according to the staircase thresholding algorithm. Participants indicated their choice (“which center is higher in contrast?”) by pressing one of the two touchscreen buttons (light gray squares) that appeared in the two bottom corners of the iPad.

Figure 2.

Results of the visual perceptual task. (A) Contrast matching thresholds as a function of age, relative to the 40% contrast no surround reference stimulus. (B) Contrast matching thresholds as a function of age, relative to the 40% contrast center 95% contrast surround stimulus. Perceptual surround suppression is demonstrated by a reduction in perceived contrast in the presence of the surround. (C) Suppression index (calculated from Equation 1) as a function of age. A higher suppression index means stronger suppression. In all panels, boxplots show the median and 25th and 75th percentiles, whiskers are the 10th and 90th percentiles, and symbols indicate the outliers for each group. The horizontal dotted line in (A) and (B) depicts the veridical contrast of the center pattern (40%). Asterisks indicate statistical significance (P < 0.05) of post hoc Bonferroni multiple pairwise comparisons of suppression index between each age group relative to adult performance.

Figure 3.

Number of staircase trials required to converge as a function of age for the (A) no surround and (B) surround conditions. Boxplots show the median and 25th and 75th percentiles, whiskers are the 10th and 90th percentiles, and symbols indicate the outliers for each group.

Figure 4.

Bland–Altman plots of test–retest variability, showing the difference in contrast matching threshold (%) between two runs of the no surround condition as a function of average contrast matching threshold (%) of two runs. The bias (average difference) is indicated by the horizontal dotted line. The 95% limits of agreement are shown by the two horizontal dashed lines.

Figure 5.

Bland–Altman plots of test–retest variability, showing the difference in contrast matching threshold (%) between the two runs of the surround condition as a function of average contrast matching threshold (%) of two runs. The bias (average difference) is indicated by the horizontal dotted line. The 95% limits of agreement are shown by the two horizontal dashed lines.

Figure 6.

Proportion of females (unfilled) and males (gray) in each age group, according to self-reported gender identity.