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The Journal of Neuroscience, June 1, 2005, 25(22):5438-5445; doi:10.1523/JNEUROSCI.1117-05.2005

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Behavioral/Systems/Cognitive
The Primordial, Blue-Cone Color System of the Mouse Retina

Silke Haverkamp,¹ Heinz Wässle,¹ Jens Duebel,² Thomas Kuner,³ George J. Augustine,⁴ Guoping Feng,⁴ and Thomas Euler²

¹Department of Neuroanatomy, Max-Planck-Institute for Brain Research, D-60528 Frankfurt/Main, Germany, Departments of ²Biomedical Optics and ³Cell Physiology, Max-Planck-Institute for Medical Research, D-69120 Heidelberg, Germany, and ⁴Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710

Humans and old world primates have trichromatic color vision based on three spectral types of cone [long-wavelength (L-), middle-wavelength (M-), and short-wavelength (S-) cones]. All other placental mammals are dichromats, and their color vision depends on the comparison of L- and S-cone signals; however, their cone-selective retinal circuitry is still unknown. Here, we identified the S-cone-selective (blue cone) bipolar cells of the mouse retina. They were labeled in a transgenic mouse expressing Clomeleon, a chloride-sensitive fluorescent protein, under the control of the thy1 promoter. Blue-cone bipolar cells comprise only 1-2% of the bipolar cell population, and their dendrites selectively contact S-opsin-expressing cones. In the dorsal half of the mouse retina, only 3-5% of the cones express S-opsin, and they are all contacted by blue-cone bipolar cells, whereas all L-opsin-expressing cones (95%) are avoided. In the ventral mouse retina, the great majority of cones express both S- and L-opsin. They are not contacted by blue-cone bipolar cells. A minority of ventral cones express S-opsin only, and they are selectively contacted by blue-cone bipolar cells. We suggest that these are genuine S-cones. In contrast to the other cones, their pedicles contain only low amounts of cone arrestin. The blue-cone bipolar cells of the mouse retina and their cone selectivity are closely similar to primate blue-cone bipolars, and we suggest that they both represent the phylogenetically ancient color system of the mammalian retina.

Key words: retina; S-cones; L-cones; color vision; bipolar cells; mice

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Received March 22, 2005; revised April 25, 2005; accepted April 28, 2005.

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