Retinal ganglion cell topography and spatial resolution in the Japanese smelt Hypomesus nipponensis (McAllister, 1963)

Abstract

Vision plays a crucial role in the life of the vast majority of vertebrate species. The spatial arrangement of retinal ganglion cells has been reported to be related to a species’ visual behavior. There are many studies focusing on the ganglion cell topography in bony fish species. However, there are still large gaps in our knowledge on the subject. We studied the topography of retinal ganglion cells (GCs) in the Japanese smelt Hypomesus nipponensis, a highly visual teleostean fish with a complex life cycle. DAPI labeling was used to visualize cell nuclei in the ganglion cell and inner plexiform layers. The ganglion cell layer was relatively thin (about 6‐8 μm), even in areas of increased cell density (area retinae temporalis), and was normally composed of a single layer of cells. In all retinal regions, rare cells occurred in the inner plexiform layer. Nissl‐stained retinae were used to estimate the proportion of displaced amacrine cells and glia in different retinal regions. In all retinal regions, about 84.5% of cells in the GC layer were found to be ganglion cells. The density of GCs varied across the retina in a regular way. It was minimum (3990 and 2380 cells/mm2 in the smaller and larger fish, respectively) in the dorsal and ventral periphery. It gradually increased centripetally and reached a maximum of 14,275 and 10,960 cells/mm2 (in the smaller and larger fish, respectively) in the temporal retina, where a pronounced area retinae temporalis was detected. The total number of GCs varied from 177 × 103 (smaller fish) to 212 × 103 cells (larger fish). The theoretical anatomical spatial resolution (the anatomical estimate of the upper limit of visual acuity calculated from the density of GCs and eye geometry and expressed in cycles per degree) was minimum in the ventral periphery (smaller fish, 1.46 cpd; larger fish, 1.26 cpd) and maximum in area retinae temporalis (smaller fish, 2.83 cpd; larger fish, 2.75 cpd). The relatively high density of GCs and the presence of area retinae temporalis in the Japanese smelt are consistent with its highly visual behavior. The present findings contribute to our understanding of the factors affecting the topography of retinal ganglion cells and visual acuity in fish.

Photoreceptors, visual pigments and intraretinal variability in spectral sensitivity in two species of smelts (Pisces, Osmeridae)

“…An additional morphological class of single cones was also found to present in this area of ​the retina based on an analysis of cone mosaics in O. eperlanus (Reckel et al ., 2003). This is quite consistent with the presence of a region of acute vision here (Pushchin et al ., 2021), which is characterized not only by an increased density of distribution of photoreceptor and ganglion cells in general, but also by the presence of additional cone types, and by an altered pattern of the cone mosaic in fish with very different ecologies (Collin, 2008; Fritsch et al ., 2017; Kondrashev et al ., 2017; Reckel & Melzer, 2003). The ratio of porphyropsin in photoreceptors of different types was not equal between different individuals from Group 2.…”

“…After 2–3 h of dark adaptation the fish was deeply anaesthetized and killed with an overdose of 0.1% solution of 3‐aminobenzoic acid ethyl ester, methanesulfonate salt (MS‐222, Sigma, St. Louis, MO). The eyes were enucleated, and photoreceptors were isolated from eight different sectors of the retina (except for the most peripheral and central zone near the optic disk) under infrared light ( λ > 800 nm) using stereomicroscope, guided by the position of the embryonic fissure running ventro‐nasally from the optic disc, which was clearly visible in both species (Figure 1a; see Figure 1 in Pushchin et al ., 2021). The retina was cut into small pieces in a few drops of saline (0.9% or 0.6% NaCl solution in 0.1 M phosphate buffer, pH 7.2).…”

Retinal ganglion cell topography and spatial resolution in the smelt Hypomesus japonicus (Brevoort, 1856)

“…All of them have advantages and disadvantages. It is therefore reasonable to combine different methods of GC labelling when studying their spatial arrangement as was done in our present and previous studies (Pushchin, 2019(Pushchin, , 2021Pushchin et al, 2021).…”

“…Thus, vision should undoubtedly play an important role in the species' biology. The aim of the present study was to examine the spatial arrangement of GCs and spatial resolution in H. japonicus and compare these characteristics with those reported for other fishes including closely related ones, exactly, the European smelt Osmerus eperlanus (Reckel et al, 2003) and Japanese smelt H. nipponensis (Pushchin et al, 2021).…”

“…Large, granular, irregularly shaped profiles were identified as ganglion cells; darkly stained small round profiles, as amacrine cells; and smaller cigar-shaped cells, as glial cells (Collin, 1988; Figure 2a). In each retina, a total of twenty-five 107 × 142 μm sites were sampled at random from different retinal regions as described in (Pushchin et al, 2021). In each site, the proportion of non-ganglion cells was determined, and the mean proportions were calculated for each retinal region.…”