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Michael Tri Hoang Do, Gregory S. Bryman, Andreas Liu; High-Fidelity Signal Transmission through Foveal Photoreceptors. Invest. Ophthalmol. Vis. Sci. 2019;60(9):1005.
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Vision in humans and other primates is exceptional—its spatial acuity is the highest among mammals (~100-fold greater than mice) and its contrast sensitivity exceeds that of all animals tested (~10-fold greater than eagles). This performance originates in the fovea, where the image is resolved at a fine grain by cone photoreceptors that are extremely slender and tightly packed. Light has direct access to this cone array due to the lateral displacement of downstream cells. Foveal cones drive these cells by extending axons that reach up to ~400 microns in length. Visual acuity and sensitivity depend on the effective transmission of graded electrical responses through the elongated foveal cones. However, computational modeling has suggested that responses are steeply diminished as they travel. We have addressed this topic experimentally using macaque foveal cones.
We applied patch-clamp electrophysiology to macaque cones in the flat-mount retina or following acute dissociation into single cells. We also made morphological reconstructions and computational models of recorded cells.
Dual-site patch-clamp recordings reveal that foveal cones transmit responses with negligible distortion. Transmission is not hindered by block of voltage-gated ion channels; thus, active amplification appears unnecessary. Indeed, effective transmission is exhibited by passive compartmental models built according to the responses and morphologies of recorded cones. These models indicate that the key biophysical feature is an internal (cytoplasmic) conductivity that is >1 order of magnitude higher than that reported for cones of other species. Internal conductivity also appears high for cones outside of the fovea, in the peripheral retina, and responses show practically no change while propagating through these stout cells (which have axons of <40 microns).
Intrinsically high internal conductivity allows primate cones to be elongated with little compromise to signaling fidelity, supporting the sharpness and sensitivity of sight that originates from the unique structural organization of the fovea.
This abstract was presented at the 2019 ARVO Annual Meeting, held in Vancouver, Canada, April 28 - May 2, 2019.
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