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Greg Field, Jeffrey L. Gauthier, Alexander Sher, Martin Greschner, Jonathon Shlens, Tim A. Machado, Deborah E. Gunning, Keith Mathieson, Alan M. Litke, E.J. Chichilnisky; Retinal receptive fields at single cone resolution and implications for color vision. Journal of Vision 2009;9(14):83. doi: 10.1167/9.14.83.
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© ARVO (1962-2015); The Authors (2016-present)
Current understanding of visual processing in the retina and central visual system is largely driven by measurements of receptive field structure. However, relatively little is known about how receptive fields are assembled from their elementary inputs, the photoreceptors. Here we report the first measurements of complete receptive field structure at single cone resolution in the primate retina, and the implications for the circuitry mediating color vision.
We utilized large-scale multi-electrode recordings to probe the light responses of hundreds of identified ganglion cells simultaneously in the macaque retina. Receptive fields were mapped with fine-grained spatiotemporal white noise. These measurements revealed multiple punctate islands of light sensitivity within each receptive field. Comparison of receptive field maps with images of the photoreceptor lattice revealed that these islands corresponded to the inputs of individual cones. Each identified cone input exhibited a characteristic sensitivity to the three display primaries that identified its spectral type: (L)ong, (M)iddle, or (S)hort wavelength-sensitive. These measurements revealed the complete center-surround structure of ganglion cell receptive fields at the resolution of individual cones. Pooling measurements across all simultaneously recorded cells revealed the mosaic of nearly all L, M and S cones, and their complete functional connectivity to nearly all of the 5 numerically dominant RGC types in primate retina (ON and OFF parasol, ON and OFF midget, and small bistratified).
These connectivity maps revealed unexpected specificity of cone inputs to different RGC types with implications for the circuitry of color vision. S cones provided substantial input to the receptive field center of OFF midget cells, but little or no input to ON midget cells or parasol cells. The purity of L and M cone inputs to the receptive field center of midget cells could not be explained by random connectivity between midget cells and cones, nor could it be explained by clumping in the cone mosaic, suggesting adaptive or developmental mechanisms that serve to increase chromatic opponency.
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