Photoreceptor distribution in the retinas of subprimate mammals

Szél, Ágoston; Lukáts, Ákos; Fekete, Tibor; Szepessy, Zsuzsanna; Röhlich, P.

doi:10.1364/josaa.17.000568

Cited by 86 publications

(86 citation statements)

References 70 publications

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“…For example, embryonic and early postnatal rabbit and mouse retinal transplants develop a high ratio of S to M cones (reviewed in ref. 17). A thyroid hormone receptor is required for M cone development in mice, and animals lacking Thrb develop only S (UV) cones (35).…”

Section: Discussionmentioning

confidence: 99%

“…The retinal pathology underlying the ESCS phenotype is not known. Noninvasive measurement of photoreceptor physiology (16) and the recent molecular association (9) have led to speculation that an NR2E3 mutant retina could resemble transplants and explants of rabbit and rodent retinas, which develop a high S to M cone ratio (17). Mutant NR2E3 may result in disordered retinal cell-fate determination, with overproduction of S cones at the expense of other photoreceptor types (9,18).…”

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confidence: 99%

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The nuclear receptor NR2E3 plays a role in human retinal photoreceptor differentiation and degeneration

Milam

Rose

Cideciyan

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

206

199

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Normal human retinal development involves orderly generation of rods and cones by complex mechanisms. Cell-fate specification involves progenitor cell lineage and external signals such as soluble factors and cell-cell interactions. In most inherited human retinal degenerations, including retinitis pigmentosa, a mutant gene causes loss of visual function, death of mature rods, and eventually death of all cone subtypes. Only one inherited retinal disorder, the enhanced S cone syndrome (ESCS), shows increased visual function, involving the minority S (blue) cones, and decreased rod and L͞M (red͞green) cone function. This autosomal recessive disease is caused by mutations in NR2E3, a photoreceptor nuclear receptor transcription factor, and may result from abnormal cell-fate determination, leading to excess S cones at the expense of other photoreceptor subtypes. In 16 ESCS patients with the most common NR2E3 mutation, R311Q, we documented an abnormal ratio of S to L͞M cone function and progressive retinal degeneration. We studied the postmortem retina of an ESCS patient homozygous for NR2E3 R311Q. No rods were identified, but cones were increased approximately 2-fold, and 92% were S cones. Only 15% of the cones expressed L͞M cone opsin, and some coexpressed S cone opsin. The retina was disorganized, with densely packed cones intermixed with inner retinal neurons. The retina was also degenerate, retaining photoreceptors in only the central and far peripheral regions. These observations suggest a key role for NR2E3 in regulation of human photoreceptor development. Degeneration of the NR2E3 retina may result from defective development, known S cone fragility, or abnormal maintenance of mature photoreceptors. T he molecular events during development of invertebrate and vertebrate retinas are incompletely understood. The specification of rods and cones involves interactions of both intrinsic and extrinsic factors, including cell lineage, soluble factors, and local cell-cell interactions (1-3). These complex signaling pathways involve nuclear receptors, a superfamily of transcription factors that share structural features, including DNA and ligandbinding domains (4, 5). A human photoreceptor-specific nuclear receptor (PNR), NR2E3, is a member of the nuclear receptor subfamily II (6). Coexpression of NR2E3, CRX (cone-rod homeobox; ref. 7), and NRL (nuclear retina leucine zipper; ref. 8) in human Y79 retinoblastoma cells suggests that NR2E3 is a component of a photoreceptor transcription cascade in human retinal development (6).Mutations in NR2E3 (9, 10) cause a unique human retinal disease, the enhanced S cone syndrome (ESCS), initially described using psychophysical and electrophysiological methods (11). ESCS patients lack rod photoreceptor function, like other inherited retinal degenerations such as retinitis pigmentosa (12), but are unique because their S (blue) cones, normally a minority population (13), are more responsive to light than the usually more populous L͞M (red͞green) cones (11, 14-16). The retinal pathology ...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

The nuclear receptor NR2E3 plays a role in human retinal photoreceptor differentiation and degeneration

Milam

Rose

Cideciyan

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

206

199

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“…That these cells follow the dual opsin gradient supports the hypothesis that the opsin gradients optimize contrast detection across spectral variation along the vertical meridian. Although the ecological basis for this optimization presumably lies in the spectral shift between ground and sky (Szél et al, 2000;Osorio and Vorobyev, 2005), a detailed account awaits a fuller characterization of the guinea pig's photic environment and the signal-to-noise properties of its photoreceptors. Recent work has begun to characterize noise sources in the photoreceptors of various species and how these vary between rods and cones Figure 6.…”

Section: Opsin Expression Predicts Cone Input To Horizontal and Briskmentioning

confidence: 99%

“…However, in certain rodents, such as guinea pig, rabbit, and mouse, immunostaining shows a dual gradient: cones expressing M opsin peak in superior retina and decline inferiorly; whereas cones expressing S opsin peak in inferior retina and decline superiorly (Röhlich et al, 1994;Applebury et al, 2000;Haverkamp et al, 2005;Nikonov et al, 2005). This dual gradient in animals that scurry along the ground might be an evolutionary adaptation to detect objects against different spectral backgrounds, such as ground vegetation (seen by superior retina) and sky (seen by inferior retina) (Szél et al, 2000;Osorio and Vorobyev, 2005).…”

Section: Introductionmentioning

confidence: 99%

Chromatic Properties of Horizontal and Ganglion Cell Responses Follow a Dual Gradient in Cone Opsin Expression

Yin¹,

Smith²,

Sterling³

et al. 2006

J. Neurosci.

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In guinea pig retina, immunostaining reveals a dual gradient of opsins: cones expressing opsin sensitive to medium wavelengths (M) predominate in the upper retina, whereas cones expressing opsin sensitive to shorter wavelengths (S) predominate in the lower retina. Whether these gradients correspond to functional gradients in postreceptoral neurons is essentially unknown. Using monochromatic flashes, we measured the relative weights with which M, S, and rod signals contribute to horizontal cell responses. For a background that produced 4.76 log 10 photoisomerizations per rod per second (Rh*/rod/s), mean weights in superior retina were 52% (M), 2% (S), and 46% (rod). Mean weights in inferior retina were 9% (M), 50% (S), and 41% (rod). In superior retina, cone opsin weights agreed quantitatively with relative pigment density estimates from immunostaining. In inferior retina, cone opsin weights agreed qualitatively with relative pigment density estimates, but quantitative comparison was impossible because individual cones coexpress both opsins to varying and unquantifiable degrees. We further characterized the functional gradients in horizontal and brisk-transient ganglion cells using flickering stimuli produced by various mixtures of blue and green primary lights. Cone weights for both cell types resembled those obtained for horizontal cells using monochromatic flashes. Because the brisk-transient ganglion cell is thought to mediate behavioral detection of luminance contrast, our results are consistent with the hypothesis that the dual gradient of cone opsins assists achromatic contrast detection against different spectral backgrounds. In our preparation, rod responses did not completely saturate, even at background light levels typical of outdoor sunlight (5.14 log 10 Rh*/rod/s).

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“…So far, only circumstantial evidence for the existence of blue-cone bipolar cells in mammals other than primates has been presented [rabbit (Famiglietti, 1981), cat (Cohen and Sterling, 1990), rat (Euler and Wässle, 1995), and mouse (Ghosh et al, 2004;Pignatelli and Strettoi, 2004)]. Because S-cones show very specific distributions across the retina in different mammals, such as the S-cone-rich area in the ventral retina of mice and rabbits, one also has to ask how an S-cone-selective channel has adapted to such variations (Szél et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

The Primordial, Blue-Cone Color System of the Mouse Retina

Haverkamp¹,

Wässle²,

Duebel³

et al. 2005

J. Neurosci.

262

316

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Humans and old world primates have trichromatic color vision based on three spectral types of cone [long-wavelength (L-), middlewavelength (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-coneselective (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 (ϳ95%) 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.

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Photoreceptor distribution in the retinas of subprimate mammals

Cited by 86 publications

References 70 publications

The nuclear receptor NR2E3 plays a role in human retinal photoreceptor differentiation and degeneration

The nuclear receptor NR2E3 plays a role in human retinal photoreceptor differentiation and degeneration

Chromatic Properties of Horizontal and Ganglion Cell Responses Follow a Dual Gradient in Cone Opsin Expression

The Primordial, Blue-Cone Color System of the Mouse Retina

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