Revealing the benefit of eye motion for acuity under emulated cone loss
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eLife Assessment
This short report is an important study that visual acuity declines nonlinearly with cone dropout, while eye motion partially compensates by improving sampling from remaining cones. The method for experimentally simulating cone dropout is compelling, leveraging state-of-the-art imaging and testing in human subjects. Inclusion of additional analysis on absolute cone density and eye motion would further strengthen the study.
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Abstract
Retinal degenerative diseases progressively erode the cone photoreceptor mosaic, reducing the retina’s spatial sampling power, yet visual acuity is remarkably resilient to cone loss. Prior work has shown that clinically normal visual acuity (20/25 or better) can persist despite up to 50% of cone cells being lost (Ratnam et al. 2013, Foote et al. 2018). However, studies on individuals with retinal degeneration are limited by patient recruitment and cannot control for patients’ stage of disease progression, creating the need for an experimental paradigm that can mimic these diseases in healthy subjects. The Oz Vision system creates visual percepts through programmable, per-cell stimulation of thousands of cone cells. We reprogram this system to emulate cone loss in healthy eyes by withholding stimulation from a subset of randomly-selected cones, rendering them inactive, in a method we term “cone dropout.” Using this approach, we characterize the visual system’s robustness to cone loss, showing that visual acuity declines nonlinearly with increasing cone dropout. Importantly, we uncover the compensatory benefit that eye motion provides under cone-deprived conditions, finding that at the highest level of dropout, a visual system with eye motion has an equivalent acuity to a static dropout condition with nearly twice as many sampling elements. Through analysis of eye motion and stimulation data, we find that this benefit arises from the additional information accumulated by “surviving” cones as they sample more of the letter through fixational eye motion.
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eLife Assessment
This short report is an important study that visual acuity declines nonlinearly with cone dropout, while eye motion partially compensates by improving sampling from remaining cones. The method for experimentally simulating cone dropout is compelling, leveraging state-of-the-art imaging and testing in human subjects. Inclusion of additional analysis on absolute cone density and eye motion would further strengthen the study.
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Reviewer #1 (Public review):
The authors demonstrate an innovative approach to investigate the effect of cone dropout on visual acuity using their newly developed olo system. By systematically reducing the coverage of real-world input to the cone photoreceptor mosaic ("cone dropout condition"), the authors are able to assess how having fewer cones leads to reduced vision, in comparison to existing approaches ("pixel dropout condition").
The capture of a rich dataset, including cone imaging and eye motion, is valuable. Benchmarking with the prior literature, suggesting that good visual acuity can be maintained despite a 50% loss in cone density, is impressive. However, it is known that cone density varies dramatically from the peak cone density location in the foveal center to even a location a few degrees outside of the fovea. In …
Reviewer #1 (Public review):
The authors demonstrate an innovative approach to investigate the effect of cone dropout on visual acuity using their newly developed olo system. By systematically reducing the coverage of real-world input to the cone photoreceptor mosaic ("cone dropout condition"), the authors are able to assess how having fewer cones leads to reduced vision, in comparison to existing approaches ("pixel dropout condition").
The capture of a rich dataset, including cone imaging and eye motion, is valuable. Benchmarking with the prior literature, suggesting that good visual acuity can be maintained despite a 50% loss in cone density, is impressive. However, it is known that cone density varies dramatically from the peak cone density location in the foveal center to even a location a few degrees outside of the fovea. In addition, there is a high degree of subject-to-subject variation in peak cone density. Given that the C stimulus is hollow in the middle, the stimulus does not actually hit the location of the peak cone density but must land slightly outside of it. Therefore, considering the actual cone density of where the stimulus lands will be important to discuss and/or analyze.
The observation of visual acuity maintenance with cone dropout has been a longstanding mystery since the 2013/2018 papers by Ratnam and Foote. The authors should be commended for their approach to addressing this important question. However, there are some simplifications and assumptions being applied to make this jump (i.e., that a 50% reduction in cone stimulation in a healthy eye is comparable to a 50% reduction in cone density in a patient). It seems unlikely that, in a patient's eye, with cone dropout, there will be gaps in the mosaic. Not considering any other non-photoreceptor-related reasons for visual acuity loss, which can occur in patients, the cone aperture acceptance angle may be different due to changes in cone size or packing; the sensitivity of individual cones may also be reduced due to deficits in the visual cycle recovery, which could be affected in disease. Some of these limitations could be addressed and acknowledged more explicitly.
Overall, this is an impressive study incorporating state-of-the-art technology to probe the fundamental limits of human vision.
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