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Katherine Mancuso, Matthew C. Mauck, William W. Hauswirth, Thomas B. Connor, James A. Kuchenbecker, Jay Neitz, Maureen Neitz; Is the high acuity midget ganglion cell system a prerequisite for red-green color vision?. Journal of Vision 2009;9(14):46. doi: https://doi.org/10.1167/9.14.46.
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It has been assumed that the fine spatial acuity midget system of primates, in which each ganglion cell receives input from a single cone, afforded a shortcut to red-green color vision unavailable to other mammals (Lennie, Haake & Williams, 1991). When a new class of cone was added during evolution, signals collected by the midget system would have automatically provided receptive field structures with spectrally-pure L or M centers compared to L/M surrounds, giving rise to trichromacy. In contrast, in mammals other than primates, ganglion cells underlying spatial contrast contact many cones in the receptive field center. For these, random wiring would produce mostly balanced L/M responses for center and surround, resulting in weak spectral-opponency. Surprisingly, Jacobs and colleagues (2007) found that transgenic mice expressing L and M pigments exhibited measureable red-green color vision. This raises questions about the relative importance of pure cone receptive field centers in providing red-green opponency. Here, we used a gene therapy approach that allowed us to produce either spectrally pure or mixed cone centers within a single species, the Mongolian gerbil. Human L-opsin was targeted to either the endogenous S-cones, producing spectrally-pure centers, or to the M-cones, producing spectrally-mixed centers. Following gene therapy, both the M- and S-cone targeted rodents had significantly increased spectral sensitivity to long-wavelengths measured using electroretinograms. However, while M-cone targeted gerbils showed only modest improvements in behavioral color discriminations, the S-cone targeted animals showed greatly enhanced red-green color vision. These results suggest that while red-green color vision can be produced in animals without a midget system, the quality is dramatically better when spectrally-pure receptive field centers are present. The small amount of color vision resulting from mixed cone centers may not have provided sufficient selective advantage to drive evolution of trichromacy in mammals lacking a midget system.
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