Intact high-level visual functions in congenital rod-monochromacy

Abstract

High-level visual functions such as reading and face recognition rely on global processes, which are often insensitive to high spatial frequencies. However, it is unknown whether a sharp cone signal is necessary for the development of these skills or whether a blurry rod signal is sufficient. CNGA3/B3-achromatopsia is a congenital disease stemming from cone dysfunction, leading to rod-only vision characterized by nystagmus, impaired acuity, and complete color blindness. We tested reading and face recognition in CNGA3/B3-achromatopsia patients (ACHM) to determine whether a rod signal is sufficient for these skills to develop. We tested 10 ACHM and 10 controls in three experiments under dark and light conditions. Initially, we evaluated acuity along the eccentricity axis. Later, we tested reading speed and upright/inverted face matching accuracy while tracking participants' eye movements. Given that ACHM patients' acuity under light conditions resembled that of controls under dark conditions, we selected these conditions for comparison. Remarkably, ACHM reading speed, face recognition abilities, and susceptibility to face inversion were not inferior to those of controls. Additionally, ACHM patients exhibited similar eye movements to controls, focusing their attention on specific areas of words and faces that indicate expertise. Despite the evident low-level limitations, ACHM patients demonstrated notable high-level visual skills, suggesting that rod-only vision is sufficient for the development of proficient reading and face recognition. These findings not only corroborate empirical evidence for high-level vision models but also enrich the discussion regarding the reasons for high-level deficits observed in individuals who have gained sight late in life.

Keywords: CNGA3; CNGB3; achromatopsia; faces; monochromat; reading; rods; scotopic.

Figure 1

Acuity experimental design and results. (A) The experimental design shows the C letter presented at a certain eccentricity and the fixation point in the center of the screen. (B) The log of the acuity thresholds for ACHM and controls in the two lighting conditions as a function of eccentricity. Zero log threshold corresponds to 6/6 vision. Dashed lines in graphs represent the minimal threshold that could be measured directly; measurements below these lines are extrapolations (see Methods for details). Error bars represent ± SEM.

Figure 2

Reading performance and eye tracking results. (A) The fraction of correct responses and reading speed for ACHM and controls. (B) ACHM and controls’ average fixation maps across participants and sentences (normalized from green—fixated at 10% of the time, to red—most fixated). (C) The number of fixations per word for ACHM and controls. L, Light; D, Dark. Individual data points are connected using straight gray lines. *p < 0.05.

Figure 3

Face recognition performance and eye tracking results. (A) The fraction of correct responses for upright (U) and inverted (I) faces for ACHM and controls. (B) ACHM and controls’ average fixation maps across participants (normalized from green—fixated 10% of the time, to red—most fixated). (C) The vertical scatter of eye movements defined by the standard deviation of eye position across the Y axis. L, Light; D, Dark. Individual data points are connected using straight gray lines. Face images were taken from The Glasgow Face Matching Task dataset (White et al., 2022). *p < 0.05.