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Juan Angueyra, Fred Rieke; Asymmetries between ON and OFF responses in primate vision first arise in photoreceptors. Invest. Ophthalmol. Vis. Sci. 2013;54(15):1293.
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© ARVO (1962-2015); The Authors (2016-present)
Psychophysical evidence in humans suggests higher sensitivity to decreases in contrast than to increases in contrast. Based on the assumption that photoreceptors respond linearly at a given light level, this difference in sensitivity has often been interpreted as a difference in sensitivity of the ON and OFF pathways. Rapid adaptation of cone photoreceptor responses, however, could create asymmetries between responses to increases in light, where adaptation would be engaged, and decreases in light, where it would be relieved. We sought to test if some ON and OFF asymmetries then arise in photoreceptors themselves and if they are physiologically relevant for downstream circuitry and computations.
Isolated primate retina was obtained through the Tissue Distribution Program of the University of Washington National Primate Research Center. Electrophysiological recordings were made from either flat-mounts (cone recordings) or slices (horizontal cell recordings) and cells were stimulated with red, green and blue LEDs.
Cone signals exhibited clear asymmetries between increases and decreases in light, with larger responses to negative contrasts and non-symmetric response kinetics. These asymmetries were observed in the cone photocurrents, photovoltage and output (measured through horizontal cells) and were more pronounced at higher backgrounds and higher contrasts, were adaptation is more readily engaged or relieved. Adaptation also caused measured responses to deviate systematically from descriptions of linear-nonlinear models, which especially failed to capture the kinetics of light responses to temporally-rich stimulation. To provide a physiological context for these findings, we measured the response of single cones to stimulation with a simulated movie of saccades used to explore a natural scene.
ON and OFF asymmetries first arise within the cone phototransduction cascade due to fast adaptational mechanisms that operate within the integration time of photopic vision and confer larger responses to negative contrasts compared to positive contrasts. These ON-OFF asymmetries are inherited by the downstream circuitry and may have relevance in basic visual tasks, like the exploration of a visual scene. The interpretation of computations and non-linearities in downstream retinal or other visual circuits should incorporate this cone non-linearity.
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