Functional anatomy of the photoreceptor and second-order cell mosaics in the retina of Xenopus laevis

Abstract

Mosaics of photoreceptors, and horizontal and bipolar cells of the Xenopus laevis retina were studied in whole-mount preparations applying lectin-cytochemical, immunocytochemical and intracellular labeling techniques. The combined density of all photoreceptor types was about 13700/mm2, of which rods represented 53%. Of the cones, the large long-wavelength-sensitive (86% of all cones) and the miniature ultraviolet-wavelength-sensitive (4%) ones could be labeled with peanut agglutinin, whereas the large short-wavelength-sensitive (10%) cones remained unlabeled. There were no significant regional differences in photoreceptor distribution. Bipolar cells were selectively labeled with antibodies against calretinin. Their density was between 4000 and 6000 cells/cm2, with slightly elevated numbers in the superior nasal quadrant. Two types of horizontal cell were injected intracellularly. The luminosity-type cells were more frequent (approximately 1000 cells/mm2) than the chromaticity cells (approximately 450 cells/mm2). The dendritic field size of the latter cell type was threefold bigger than that of the luminosity cells. The coverage factors were estimated to be 3.3 for the luminosity cells and 5.2 for the chromaticity cells. The luminosity cells contacted all photoreceptor types, whereas chromatic horizontal cells received their inputs from the short-wavelength-sensitive cones and from some, but not all, rods. Luminosity cells encounter about 50-60 potential synaptic partners within their dendritic fields, whereas chromatic horizontal cells only about 20. Chromatic horizontal cells form multiple synaptic contacts with the short-wavelength-sensitive cones. The results indicate that the overall photoreceptor to bipolar and bipolar to ganglion cell convergence in Xenopus retina is similar to that in the central retinal specialized regions of mammals, predicting comparable spatial resolutions.

Photoreceptor cells in the Xenopus retina

“…A similar conclusion was reached about the large single cones in the tiger salamander (Sherry et al, 1998). According to counts on retinal wholemounts, Zhang et al, (1994) and Wilhelm and Gá briel (1999) calculated the COS-1 positive cones in the Xenopus to constitute 86 -88% of all cones. Only COS-1 positive large single cones are mentioned, but it is not clear whether double cones were also included in their study.…”

“…More than half (53%) of all photoreceptors consists of rods, with an average density of 7,250 cells/mm 2 (Wilhelm and Gá briel, 1999). Two subclasses of rods can be distinguished: the principal ("red") rods that make about 97-98% of all rods and the somewhat smaller thin ("green") rods.…”

“…This rare cone type makes only 3.6 -4.1% of the total cone population Wilhelm and Gá briel, 1999). The length of the inner segment is about 60% of that of the large single cones and its oil droplet has a diameter of 2-4 m. The slightly oval droplet is embedded in the apical part of the ellipsoid, separated from the base of the outer segment by a thick layer of mitochondria (Fig.…”

“…Two subclasses of rods can be distinguished: the principal ("red") rods that make about 97-98% of all rods and the somewhat smaller thin ("green") rods. Various photoreceptor types are evenly distributed in all parts of the retina and the rod/cone ratio does not show significant changes from center to periphery (Wilhelm and Gá briel, 1999).…”

“…In this paper, we describe the various photoreceptor types in the Xenopus laevis retina, based mainly on the light and electron microscopic immunocytochemical studies on semithin and thin sections by and on light microscopic observations with various antibodies and other probes on frozen sections and retinal flat-mounts by Zhang et al (1994) and by Wilhelm and Gá briel (1999). We concentrate on the classification of spectrally different photoreceptor types rather than describing fine structural details of the visual cells.…”