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Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics

Authors :
Ayoub Lassoued
Donald T. Miller
James A. Crowell
Kazuhiro Kurokawa
Furu Zhang
Source :
Proceedings of the National Academy of Sciences of the United States of America
Publication Year :
2019
Publisher :
Proceedings of the National Academy of Sciences, 2019.

Abstract

Significance The three spectral types of cone photoreceptors underlie color perception and are largely responsible for inherited and acquired color vision anomalies. In vivo mapping of the trichromatic cone mosaic by imaging provides the most direct and quantitative means to assess the role of photoreceptors in color vision, but remains challenging because cone reflections only weakly differentiate cone types. Here, we show a noninvasive light microscopy modality that reveals the cell’s spectral type, using the optical phase change that arises within the cell when stimulated with light. Our procedure is orders of magnitude faster and more accurate than prior approaches and makes in vivo cone classification promising for a much wider range of color vision applications.<br />Human color vision is achieved by mixing neural signals from cone photoreceptors sensitive to different wavelengths of light. The spatial arrangement and proportion of these spectral types in the retina set fundamental limits on color perception, and abnormal or missing types are responsible for color vision loss. Imaging provides the most direct and quantitative means to study these photoreceptor properties at the cellular scale in the living human retina, but remains challenging. Current methods rely on retinal densitometry to distinguish cone types, a prohibitively slow process. Here, we show that photostimulation-induced optical phase changes occur in cone cells and carry substantial information about spectral type, enabling cones to be differentiated with unprecedented accuracy and efficiency. Moreover, these phase dynamics arise from physiological activity occurring on dramatically different timescales (from milliseconds to seconds) inside the cone outer segment, thus exposing the phototransduction cascade and subsequent downstream effects. We captured these dynamics in cones of subjects with normal color vision and a deuteranope, and at different macular locations by: (i) marrying adaptive optics to phase-sensitive optical coherence tomography to avoid optical blurring of the eye, (ii) acquiring images at high speed that samples phase dynamics at up to 3 KHz, and (iii) localizing phase changes to the cone outer segment, where photoactivation occurs. Our method should have broad appeal for color vision applications in which the underlying neural processing of photoreceptors is sought and for investigations of retinal diseases that affect cone function.

Details

ISSN :
10916490 and 00278424
Volume :
116
Database :
OpenAIRE
Journal :
Proceedings of the National Academy of Sciences
Accession number :
edsair.doi.dedup.....631058b343b9c88fe87c5ff014fc442d
Full Text :
https://doi.org/10.1073/pnas.1816360116