Photoreceptor classes and transmission at the photoreceptor synapse in the retina of the clawed frog,Xenopus laevis

Witkovsky, Paul

doi:10.1002/1097-0029(20000901)50:5<338::aid-jemt3>3.0.co;2-i

Cited by 20 publications

(29 citation statements)

References 67 publications

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“…Similar to the adult Xenopus retina [37,55], we found a comparable proportion of rods and cones in the Stage 42 retina. Immunolabeling revealed that of the DAPI + cells in the ONL, 54.4% were rhodopsin + rods and 45.6% were calbindin + cones (mean ± SD: 68.3 ± 4.3 rhodopsin + cells/section (54.4%) versus 57.2 ± 6.4 calbindin + cells/section (45.6%); n = 6 sections).…”

Section: Resultssupporting

confidence: 81%

“…Activation could occur potentially by the formation of the final connections of On BCs with PRs, or by changes in the expression of ion channels that affect cellular depolarization. In this regard, rods and cones establish synapses with BCs and HCs in the INL at Stage 37/38 [55]. Continued development of the circuit then appears to occur by the addition of complete cellular units, such that the ratio of INL to RGC layer c-fos + cells remains constant even though the number of c-fos + cells continues to increase.…”

Section: Discussionmentioning

confidence: 99%

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Wiring the retinal circuits activated by light during early development

2014

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BackgroundLight information is sorted by neuronal circuits to generate image-forming (IF) (interpretation and tracking of visual objects and patterns) and non-image-forming (NIF) tasks. Among the NIF tasks, photic entrainment of circadian rhythms, the pupillary light reflex, and sleep are all associated with physiological responses, mediated mainly by a small group of melanopsin-expressing retinal ganglion cells (mRGCs). Using Xenopus laevis as a model system, and analyzing the c-fos expression induced by light as a surrogate marker of neural activity, we aimed to establish the developmental time at which the cells participating in both systems come on-line in the retina.ResultsWe found that the peripheral retina contains 80% of the two melanopsin-expressing cell types we identified in Xenopus: melanopsin-expressing horizontal cells (mHCs; opn4m+/opn4x+/Prox1+) and mRGCs (2.7% of the total RGCs; opn4m+/opn4x+/Pax6+/Isl1), in a ratio of 6:1. Only mRGCs induced c-fos expression in response to light. Dopaminergic (tyrosine hydroxylase-positive; TH+) amacrine cells (ACs) may be part of the melanopsin-mediated circuit, as shown by preferential c-fos induction by blue light. In the central retina, two cell types in the inner nuclear layer (INL) showed light-mediated induction of c-fos expression [(On-bipolar cells (Otx2+/Isl1+), and a sub-population of ACs (Pax6−/Isl1−)], as well as two RGC sub-populations (Isl1+/Pax6+ and Isl1+/Pax6−). Melanopsin and opsin expression turned on a day before the point at which c-fos expression could first be activated by light (Stage 37/38), in cells of both the classic vision circuit, and those that participate in the retinal component of the NIF circuit. Key to the classic vision circuit is that the component cells engage from the beginning as functional ‘unit circuits’ of two to three cells in the INL for every RGC, with subsequent growth of the vision circuit occurring by the wiring in of more units.ConclusionsWe identified melanopsin-expressing cells and specific cell types in the INL and the RGC layer which induce c-fos expression in response to light, and we determined the developmental time when they become active. We suggest an initial formulation of retinal circuits corresponding to the classic vision pathway and melanopsin-mediated circuits to which they may contribute.

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Section: Resultssupporting

confidence: 81%

Section: Discussionmentioning

confidence: 99%

Wiring the retinal circuits activated by light during early development

2014

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“…In Amphibia, two types of rods and three types of color-specific cones have been described, the latter assumed to represent red-, blue-, and UV-sensitive cones (Xenopus: Röhlich et al 1989a;Röhlich and Szél 2000;Witkovsky 2000;Zhang et al 1994;tiger salamander: Sherry et al 1998). Are all these photoreceptor classes present in the blind cave salamander?…”

Section: Discussionmentioning

confidence: 99%

Immunocytochemical demonstration of visual pigments in the degenerate retinal and pineal photoreceptors of the blind cave salamander ( Proteus anguinus )

Kos

Bulog

Szél

et al. 2001

Cell and Tissue Research

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Visual pigments in the regressed eye and pineal of the depigmented neotenic urodele, the blind cave salamander (Proteus anguinus anguinus), were studied by immunocytochemistry with anti-opsin antibodies. The study included light- and electron-microscopic investigations of both the eye and the pineal organ. A comparison was made with the black pigmented subspecies Proteus anguinus parkelj (black proteus), which has a normal eye structure. In the retina of the black proteus, we found principal rods, red-sensitive cones and a third photoreceptor type, which might represent a blue- or UV-sensitive cone. Photoreceptors in the regressed eye of the blind cave salamanders from the Planina cave contained degenerate outer segments, consisting of a few whorled discs and irregular clumps of membranes. The great majority of these outer segments showed immunolabelling for the red-sensitive cone opsin and only a few of them were found to be positive for rhodopsin. An even more pronounced degeneration was observed in the photoreceptors of the animals derived from the Otovec doline, which are completely devoid of an outer segment, most of them not even possessing an inner segment. Even in some of these highly degenerate cells, the presence of rhodopsin could be detected in the plasma membrane; however, immunoreactions with antibodies recognizing cone visual pigment were negative. In the pineals of all studied animals, the degenerate photoreceptor outer segments were recognized exclusively by the antibody against the red-sensitive cone opsin. The presence of immunopositive visual pigments indicates the possibility of a retained light sensitivity in the blind cave salamander photoreceptors.

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“…T3 represses the availability of vitamin A2 (3,4-dehydro, 11-cis retinol) used for tadpole visual pigments and leaves vitamin A1 (11-cis retinol) as a chromophore source for bullfrog pigments (Wilt, 1959;Ohtsu et al, 1964). TR␣ and TR␤ receptors in the Xenopus eye are known for their roles in metamorphosis, which include remodeling of the eye and neural interconnections in the retina (Hoskins, 1990;Marsh-Armstrong et al, 1999;Witkovsky, 2000). In fish, ultraviolet (UV) cones are lost during metamorphic changes, and then regenerate later in mature fish.…”

Section: Thyroid Hormone Receptors Act As Sensors Of Thyroid Hormone T3mentioning

confidence: 99%

Transient expression of thyroid hormone nuclear receptor TRβ2 sets S opsin patterning during cone photoreceptor genesis

Applebury

Farhangfar

Glösmann

et al. 2007

Developmental Dynamics

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Cone photoreceptors in the murine retina are patterned by dorsal repression and ventral activation of S opsin. TR␤2, the nuclear thyroid hormone receptor ␤ isoform 2, regulates dorsal repression. To determine the molecular mechanism by which TR␤2 acts, we compared the spatiotemporal expression of TR␤2 and S opsin from embryonic day (E) 13 through adulthood in C57BL/6 retinae. TR␤2 and S opsin are expressed in cone photoreceptors only. Both are transcribed by E13, and their levels increase with cone genesis. TR␤2 is expressed uniformly, but transiently, across the retina. mRNA levels are maximal by E17 at completion of cone genesis and again minimal before P5. S opsin is also transcribed by E13, but only in ventral cones. Repression in dorsal cones is established by E17, consistent with the occurrence of patterning during cone cell genesis. The uniform expression of TR␤2 suggests that repression of S opsin requires other dorsalspecific factors in addition to TR␤2. The mechanism by which TR␤2 functions was probed in transgenic animals with TR␤2 ablated, TR␤2 that is DNA binding defective, and TR␤2 that is ligand binding defective. These studies show that TR␤2 is necessary for dorsal repression, but not ventral activation of S opsin. TR␤2 must bind DNA and the ligand T3 (thyroid hormone) to repress S opsin. Once repression is established, T3 no longer regulates dorsal S opsin repression in adult animals. The transient, embryonic action of TR␤2 is consistent with a role (direct and/or indirect) in chromatin remodeling that leads to permanent gene silencing in terminally differentiated, dorsal cone photoreceptors.

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Photoreceptor classes and transmission at the photoreceptor synapse in the retina of the clawed frog,Xenopus laevis

Cited by 20 publications

References 67 publications

Wiring the retinal circuits activated by light during early development

Wiring the retinal circuits activated by light during early development

Immunocytochemical demonstration of visual pigments in the degenerate retinal and pineal photoreceptors of the blind cave salamander ( Proteus anguinus )

Transient expression of thyroid hormone nuclear receptor TRβ2 sets S opsin patterning during cone photoreceptor genesis

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