Physiology and Morphology of Color-Opponent Ganglion Cells in a Retina Expressing a Dual Gradient of S and M Opsins

Yin, Lu; Smith, Robert G.; Sterling, Peter; Brainard, David H.

doi:10.1523/jneurosci.5471-08.2009

Cited by 51 publications

(51 citation statements)

References 73 publications

(146 reference statements)

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“…Opsin coexpression gradients have been found in several mammalian species, including mouse, rabbit, and guinea pig (Juliusson et al, 1994;Röhlich et al, 1994). The effect of the gradient on horizontal and ganglion cell responses has been studied in guinea pig (Yin et al, 2006(Yin et al, , 2009, where the local opsin coexpression ratio was found to relate to the chromatic tuning of the neurons-similar to our observations in mouse BCs. Yin et al (2009) found color-opponent GCs across the whole retina, with ventrally recorded cells showing reduced opponency.…”

Section: Influence Of the Opsin Coexpression Gradient On Chromatic Prsupporting

confidence: 86%

“…The effect of the gradient on horizontal and ganglion cell responses has been studied in guinea pig (Yin et al, 2006(Yin et al, , 2009, where the local opsin coexpression ratio was found to relate to the chromatic tuning of the neurons-similar to our observations in mouse BCs. Yin et al (2009) found color-opponent GCs across the whole retina, with ventrally recorded cells showing reduced opponency. Regional opsin coexpression may, however, offer functional advantages [e.g., to enhance contrast detection against different spectral backgrounds (i.e., blue sky vs greenish-brownish ground) (Yin et al, 2006)].…”

Section: Influence Of the Opsin Coexpression Gradient On Chromatic Prsupporting

confidence: 84%

“…A suitable bistratified mouse GC type has been morphologically described ["type 1" in the study by Schubert et al (2005); G 12 in the study by Völgyi et al (2009)], with dendrites ramifying in IPL strata 1 and 5, where they could contact type 1 and 9 BCs. Color-opponent GCs in mouse may also be monostratified, like in guinea pig (Yin et al, 2009). To implement color-opponent monostratified GC presumably requires amacrine cells to generate the necessary green-OFF (or blue-ON) signals (for review, see Dacey and Packer, 2003).…”

Section: Chromatic Circuitry In the Mouse Retinamentioning

confidence: 99%

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Chromatic Bipolar Cell Pathways in the Mouse Retina

Breuninger

Puller²,

Haverkamp³

et al. 2011

J. Neurosci.

134

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Like most mammals, mice feature dichromatic color vision based on short (S) and middle (M) wavelength-sensitive cone types. It is thought that mammals share a retinal circuit that in dichromats compares S-and M-cone output to generate blue/green opponent signals, with bipolar cells (BCs) providing separate chromatic channels. Although S-cone-selective ON-BCs (type 9 in mouse) have been anatomically identified, little is known about their counterparts, the M-cone-selective OFF-BCs. Here, we characterized cone connectivity and light responses of selected mouse BC types using immunohistochemistry and electrophysiology. Our anatomical data indicate that four (types 2, 3a/b, and 4) of the five mouse OFF-BCs indiscriminately contact both cone types, whereas type 1 BCs avoid S-cones. Light responses showed that the chromatic tuning of the BCs strongly depended on their position along the dorsoventral axis because of the coexpression gradient of M-and S-opsin found in mice. In dorsal retina, where coexpression is low, most type 2 cells were green biased, with a fraction of cells (Ϸ14%) displaying strongly blue-biased responses, likely reflecting S-cone input. Type 1 cells were also green biased but did not comprise blue-biased "outliers," consistent with type 1 BCs avoiding S-cones. We therefore suggest that type 1 represents the green OFF pathway in mouse. In addition, we confirmed that type 9 BCs display blue-ON responses. In ventral retina, all BC types studied here displayed similar blue-biased responses, suggesting that color vision is hampered in ventral retina. In conclusion, our data support an antagonistically organized blue/green circuit as the common basis for mammalian dichromatic color vision.

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Section: Influence Of the Opsin Coexpression Gradient On Chromatic Prsupporting

confidence: 86%

Section: Influence Of the Opsin Coexpression Gradient On Chromatic Prsupporting

confidence: 84%

Section: Chromatic Circuitry In the Mouse Retinamentioning

confidence: 99%

See 1 more Smart Citation

Chromatic Bipolar Cell Pathways in the Mouse Retina

Breuninger

Puller²,

Haverkamp³

et al. 2011

J. Neurosci.

134

View full text Add to dashboard Cite

show abstract

“…Yin et al (2009) describe a rarely encountered color opponent ganglion cell type in guinea pig retina that have monostratified morphology quite different than that of small bistratified cells in monkey retina. But the morphological correlate of the color-coded retinal ganglion cell in cats is yet to be found, and is an important gap in our knowledge of this otherwise best-studied mammalian visual system.…”

Section: The Primordial Color System In Catsmentioning

confidence: 98%

“…In the retinae of rodents Li and DeVries, 2006;Puller et al, 2011) and cats (Cohen and Sterling, 1990a,b), S-cones connect a specific bipolar cell type. Antagonistic responses to the activation of S-and ML-cones were demonstrated in several species including cats by recordings from retinal ganglion cells (Michael, 1966;Cleland and Levick, 1974;Vaney et al, 1981;Hemmi et al, 2002;Ekesten and Gouras, 2005;Yin et al, 2009) or from relay neurons of the LGN (Daw and Pearlman, 1970;Michail, 1973;Cleland et al, 1976;Wilson et al, 1976). Their spatial receptive field structure has not been studied systematically, and it is not known whether they constitute one or more coherent functional channels.…”

Section: Introductionmentioning

confidence: 99%

Receptive Field Properties of Color Opponent Neurons in the Cat Lateral Geniculate Nucleus

et al. 2013

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Most nonprimate mammals possess dichromatic ("red-green color blind") color vision based on short-wavelength-sensitive (S) and medium/long-wavelength-sensitive (ML) cone photoreceptor classes. However, the neural pathways carrying signals underlying the primitive "blue-yellow" axis of color vision in nonprimate mammals are largely unexplored. Here, we have characterized a population of color opponent (blue-ON) cells in recordings from the dorsal lateral geniculate nucleus of anesthetized cats. We found five points of similarity to previous descriptions of primate blue-ON cells. First, cat blue-ON cells receive ON-type excitation from S-cones, and OFF-type excitation from ML-cones. We found no blue-OFF cells. Second, the S-and ML-cone-driven receptive field regions of cat blue-ON cells are closely matched in size, consistent with specialization for detecting color contrast. Third, the receptive field center diameter of cat blue-ON cells is approximately three times larger than the center diameter of non-color opponent receptive fields at any eccentricity. Fourth, S-and ML-cones contribute weak surround inhibition to cat blue-ON cells. These data show that blue-ON receptive fields in cats are functionally very similar to blue-ON type receptive fields previously described in macaque and marmoset monkeys. Finally, cat blue-ON cells are found in the same layers as W-cells, which are thought to be homologous to the primate koniocellular system. Based on these data, we suggest that cat blue-ON cells are part of a "blue-yellow" color opponent system that is the evolutionary homolog of the blue-ON division of the koniocellular pathway in primates.

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Synaptic inputs onto small bistratified (blue‐ON/yellow‐OFF) ganglion cells in marmoset retina

Percival¹,

Jusuf²,

Martin³

2009

J of Comparative Neurology

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The inner plexiform layer of the retina contains functional subdivisions, which segregate ON and OFF type light responses. Here, we studied quantitatively the ON and OFF synaptic input to small bistratified (blue-ON/yellow-OFF) ganglion cells in marmosets (Callithrix jacchus). Small bistratified cells display an extensive inner dendritic tier that receives blue-ON input from short-wavelength-sensitive (S) cones via blue cone bipolar cells. The outer dendritic tier is sparse and is thought to receive yellow-OFF input from medium (M)- and long (L)-wavelength-sensitive cones via OFF diffuse bipolar cells. In total, 14 small bistratified cells from different eccentricities were analyzed. The cells were retrogradely labeled from the koniocellular layers of the lateral geniculate nucleus and subsequently photofilled. Retinal preparations were processed with antibodies against the C-terminal binding protein 2, the AMPA receptor subunit GluR4, and/or gephyrin to identify bipolar and/or amacrine input. The results show that the synaptic input is evenly distributed across the dendritic tree, with a density similar to that reported previously for other ganglion cell types. The population of cells showed a consistent pattern, where bipolar input to the inner tier is about fourfold greater than bipolar input to the outer tier. This structural asymmetry of bipolar input may help to balance the weight of cone signals from the sparse S cone array against inputs from the much denser M/L cone array.

show abstract

Physiology and Morphology of Color-Opponent Ganglion Cells in a Retina Expressing a Dual Gradient of S and M Opsins

Cited by 51 publications

References 73 publications

Chromatic Bipolar Cell Pathways in the Mouse Retina

Chromatic Bipolar Cell Pathways in the Mouse Retina

Receptive Field Properties of Color Opponent Neurons in the Cat Lateral Geniculate Nucleus

Synaptic inputs onto small bistratified (blue‐ON/yellow‐OFF) ganglion cells in marmoset retina

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