Retinal ganglion cell distribution and spatial resolving power in elasmobranchs

The total number, distribution and peak density of presumed retinal ganglion cells was assessed in 10 species of elasmobranch (nine species of shark and one species of batoid) using counts of Nissl-stained cells in retinal wholemounts. The species sampled include a number of active, predatory benthopelagic and pelagic sharks that are found in a variety of coastal and oceanic habitats and represent elasmobranch groups for which information of this nature is currently lacking. The topographic distribution of cells was heterogeneous in all species. Two benthic species, the shark Chiloscyllium punctatum and the batoid Taeniura lymma, have a dorsal or dorso-central horizontal streak of increased cell density, whereas the majority of the benthopelagic and pelagic sharks examined exhibit a more concentric pattern of increasing cell density, culminating in a central area centralis of higher cell density located close to the optic nerve head. The exception is the shark Alopias superciliosus, which possesses a ventral horizontal streak. Variation in retinal ganglion cell topography appears to be related to the visual demands of different habitats and lifestyles, as well as the positioning of the eyes in the head. The upper limits of spatial resolving power were calculated for all 10 species, using peak ganglion cell densities and estimates of focal length taken from cryo-sectioned eyes in combination with information from the literature. Spatial resolving power ranged from 2.02 to 10.56 cycles deg(-1), which is in accordance with previous studies. Species with a lower spatial resolving power tend to be benthic and/or coastal species that feed on benthic invertebrates and fishes. Active, benthopelagic and pelagic species from more oceanic habitats which feed on larger, more active prey, possess a higher resolving power. Additionally, ganglion cells in a juvenile of C. punctatum, were retrogradely-labeled from the optic nerve with biotinylated dextran amine (BDA). A comparison of the BDA- labeled material and tissue stained for Nissl substance indicates that 76% of the cells in the retinal ganglion cell and inner plexiform layers of the central retina in this species are non-ganglion cells.     

Retinal ganglion cell topography and spatial resolving power in the river hippopotamus (Hippopotamus amphibius)

The river hippopotamus (Hippopotamus amphibius), one of the closest extant relatives to cetaceans, is a large African even‐toed ungulate (Artiodactyla) that grazes and has a semiaquatic lifestyle. Given its unusual phenotype, ecology, and evolutionary history, we sought to measure the topographic distribution of retinal ganglion cell density using stereology and retinal wholemounts. We estimated a total of 243,000 ganglion cells of which 3.4% (8,300) comprise alpha cells. The topographic distribution of both total and alpha cells reveal a dual topographic organization of a temporal and nasal area embedded within a well‐defined horizontal streak. Using maximum density of total ganglion cells and eye size (35 mm, axial length), we estimated upper limits of spatial resolving power of 8 cycles/deg (temporal area, 1,800 cells/mm²), 7.7 cycles/deg (nasal area, 1,700 cells/mm²), and 4.2 cycles/deg (horizontal streak, 250 cells/mm²). Enhanced resolution of the temporal area toward the frontal visual field may facilitate grazing, while resolution of the horizontal streak and nasal area may help the discrimination of objects (predators, conspecifics) in the lateral and posterior visual fields, respectively. Given the presumed role of alpha cells to detect brisk transient stimuli, their similar distribution to the total ganglion cell population may facilitate the detection of approaching objects in equivalent portions of the visual field. Our finding of a nasal area in the river hippopotamus retina supports the notion that this specialization may enhance visual sampling in the posterior visual field to compensate for limited neck mobility as suggested for rhinoceroses and cetaceans.     

Retinal ganglion cell topography and spatial resolving power in the white rhinoceros (Ceratotherium simum)

This study sought to determine whether the retinal organization of the white rhinoceros (Ceratotherium simum), a large African herbivore with lips specialized for grazing in open savannahs, relates to its foraging ecology and habitat. Using stereology and retinal wholemounts, we estimated a total of 353,000 retinal ganglion cells. Their density distribution reveals an unusual topographic organization of a temporal (2,000 cells/mm²) and a nasal (1,800 cells/mm²) area embedded within a well‐defined horizontal visual streak (800 cells/mm²), which is remarkably similar to the retinal organization in the black rhinoceros. Alpha ganglion cells comprise 3.5% (12,300) of the total population of ganglion cells and show a similar distribution pattern with maximum densities also occurring in the temporal (44 cells/mm²) and nasal (40 cells/mm²) areas. We found higher proportions of alpha cells in the dorsal and ventral retinas. Given their role in the detection of brisk transient stimuli, these higher proportions may facilitate the detection of approaching objects from the front and behind while grazing with the head at 45 °. Using ganglion cell peak density and eye size (29 mm, axial length), we estimated upper limits of spatial resolving power of 7 cycles/deg (temporal area), 6.6 cycles/deg (nasal area), and 4.4 cycles/deg (horizontal streak). The resolution of the temporal area potentially assists with grazing, while the resolution of the streak may be used for panoramic surveillance of the horizon. The nasal area may assist with detection of approaching objects from behind, potentially representing an adaptation compensating for limited neck and head mobility. J. Comp. Neurol., 525:2484–2498, 2017. © 2017 Wiley Periodicals, Inc.     

Retinal ganglion cell degeneration in Alzheimer''s disease

This study documents the light-microscopic and ultrastructural characteristics of ganglion cell degeneration in the retinas of patients with Alzheimer's disease (AD). The results show degeneration in the retinal ganglion cells (RGCs) characterized by a vacuolated, 'frothy' appearance of the cytoplasm. The degeneration is unique in AD because of the absence of neurofibrillary tangles within the RGCs, or of neuritic plaques or amyloid angiopathy in the retinas or optic nerves of any of the cases examined. These results suggest that neuronal degeneration in the ganglion cell layer (GCL) should be added to the constellation of neuropathologic changes found in patients with Alzheimer's disease.     

Development of ganglion cell topography in ferret retina

The adult ferret has approximately 90,000 retinal ganglion cells, arranged in a prominent area centralis and visual streak. The role of differential cell generation, cell death, and retinal growth in the control of adult retinal ganglion cell number and distribution was evaluated by examining basic aspects of retinogenesis, including growth in retinal area, developmental changes in the number, size, and distribution of retinal ganglion cells (identification aided by retrograde transport of HRP), and the incidence of degenerating cells in the ganglion cell layer. Retinal development in the ferret was also compared to retinal development in the cat (which has an even more differentiated area centralis) to determine what alterations of developmental parameters are most closely associated with this species difference in adult morphology. The area of the retina increases linearly from birth (12 mm2) to postnatal day 24 (54 mm2), reaching an eventual adult value of 64 mm2. Ganglion cell numbers peak at 155,000 (approximately twice the adult number) on postnatal day 3, and fall to adult numbers by postnatal day 6. The remaining cells of the ganglion cell layer, principally displaced amacrine cells, reach their peak number on postnatal day 10 (approximately 280,000), falling to 200,000 by adulthood. Degenerating cells are abundant in the ganglion cell layer in the immediate postnatal period. A difference in the incidence of degenerating cells in the presumptive area centralis versus that in the retinal periphery was not observed postnatally, though there were other striking spatial nonuniformities, suggesting that differential cell loss might contribute to other features of retinal topographic organization. Ganglion cell density is virtually uniform across the retina at birth. Cell density is first reduced in the dorsal retina, resulting in a dorsal-to-ventral gradient in cell density that persists until day 10, when ganglion cell number has stabilized. By postnatal day 24, an area centralis and visual streak has emerged, but not of adult magnitude. Because ganglion cell number has stabilized long before the area centralis and visual streak emerge, we conclude that differential retinal growth is the principal mechanism producing this feature of retinal topography. Comparison with the cat suggests that the proportionately greater nonuniform growth of the cat's eye accounts for the greater differentiation of its area centralis.     

Retinal ganglion cell topography and spatial resolving power in African megachiropterans: Influence of roosting microhabitat and foraging

Megachiropteran bats (megabats) show remarkable diversity in microhabitat occupation and trophic specializations, but information on how vision relates to their behavioral ecology is scarce. Using stereology and retinal wholemounts, we measured the topographic distribution of retinal ganglion cells and determined the spatial resolution of eight African megachiropterans with distinct roosting and feeding ecologies. We found that species roosting in open microhabitats have a pronounced streak of high retinal ganglion cell density, whereas those favoring more enclosed microhabitats have a less pronounced streak (or its absence in Hypsignathus monstrosus). An exception is the cave‐dwelling Rousettus aegyptiacus, which has a pronounced horizontal streak that potentially correlates with its occurrence in more open environments during foraging. In all species, we found a temporal area with maximum retinal ganglion cell density (～5,000–7,000 cells/mm²) that affords enhanced resolution in the frontal visual field. Our estimates of spatial resolution based on peak retinal ganglion cell density and eye size (～6–12 mm in axial length) range between ～2 and 4 cycles/degree. Species that occur in more enclosed microhabitats and feed on plant material have lower spatial resolution (～2 cycles/degree) compared with those that roost in open and semiopen areas (～3–3.8 cycles/degree). We suggest that the larger eye and concomitant higher spatial resolution (～4 cycles/degree) in H. monstrosus may have facilitated the carnivorous aspect of its diet. In conclusion, variations in the topographic organization and magnitude of retinal ganglion density reflect the specific ecological needs to detect food/predators and the structural complexity of the environments. J. Comp. Neurol. 525:186–203, 2017. © 2016 Wiley Periodicals, Inc.     

Retinal ganglion cell topography in teleosts: a comparison between Nissl-stained material and retrograde labelling from the optic nerve

The retinal topography of cells within the ganglion cell layer of three teleost species is examined in Nissl-stained material in which all neuronal elements containing Nissl substance in the cytoplasm are counted. A topographic comparison is made with retrogradely labelled ganglion cells to differentiate the proportion of nonganglion cells not possessing an axon joining the optic nerve. In the three species studied 92%, 80%, and 66% were found to be the maximum proportion of true ganglion cells in the area centralis, horizontal streak, and periphery, respectively. The proportion of nonganglion cells in the total population of cells counted was 24%. The major contribution to this discrepancy is from peripheral nonspecialized regions of the retina. There is little difference in both topography and peak densities of retinal ganglion cells between the two techniques. The soma areas of both populations are analysed, with the homogeneous nonganglion cell population possessing cells between 5 and 15 micron2 and the heterogeneous ganglion cell soma between 5 and 68 micron2, increasing in size with eccentricity.     

Scene from above: Retinal ganglion cell topography and spatial resolving power in the giraffe (Giraffa camelopardalis)

The giraffe (Giraffa camelopardalis) is a browser that uses its extensible tongue to selectively collect leaves during foraging. As the tallest extant terrestrial mammal, its elevated head height provides panoramic surveillance of the environment. These aspects of the giraffe's ecology and phenotype suggest that vision is of prime importance. Using Nissl‐stained retinal wholemounts and stereological methods, we quantitatively assessed the retinal specializations in the ganglion cell layer of the giraffe. The mean total number of retinal ganglion cells was 1,393,779 and their topographic distribution revealed the presence of a horizontal visual streak and a temporal area. With a mean peak of 14,271 cells/mm², upper limits of spatial resolving power in the temporal area ranged from 25 to 27 cycles/degree. We also observed a dorsotemporal extension (anakatabatic area) that tapers toward the nasal retina giving rise to a complete dorsal arch. Using neurofilament‐200 immunohistochemistry, we also detected a dorsal arch formed by alpha ganglion cells with density peaks in the temporal (14–15 cells/mm²) and dorsonasal (10 cells/mm²) regions. As with other artiodactyls, the giraffe shares the presence of a horizontal streak and a temporal area which, respectively, improve resolution along the horizon and in the frontal visual field. The dorsal arch is related to the giraffe's head height and affords enhanced resolution in the inferior visual field. The alpha ganglion cell distribution pattern is unique to the giraffe and enhances acquisition of motion information for the control of tongue movement during foraging and the detection of predators. J. Comp. Neurol. 521:2042–2057, 2013. © 2012 Wiley Periodicals, Inc.     

Development of ganglion cell topography in the postnatal cochlea

In mammals, the size and number of spiral ganglion cells can vary significantly along the length of the cochlea. At present, it is unclear how these topologic differences in spiral ganglion cell morphology and density emerge during development. We addressed this issue by quantifying developmental changes in the number, density, and size of auditory ganglion cells within the cochlea of Mongolian gerbils throughout the first 3 weeks of postnatal life. In each cochlea, cells were measured at five standardized locations along the length of the spiral ganglion, as determined from serial reconstruction of Rosenthal's canal. During the first postnatal week, the total number of gerbil spiral ganglion cells decreased significantly by 27%, without further change thereafter. This brief period of neuronal cell death coincides with a major remodeling in the afferent neural projections to gerbil auditory hair cells (Echteler [1992] Proc. Natl. Acad. Sci. USA 89:6324-6327). The resulting reduction in neuronal density varied with location, being most prominent within the upper basal and lower middle turns of the cochlea. These same regions contained the smallest auditory ganglion cells found within the gerbil ear and exhibited the least amount of developmental expansion in the circumference of Rosenthal's canal. These results suggest the possibility that regional differences in auditory neuron size and number might be influenced by local extrinsic factors, such as the availability of canal space.     

Retinal ganglion cell layer of the Caspian seal Pusa caspica: topography and localization of the high-resolution area

Retinal topography, cell density and sizes of ganglion cells in the Caspian seal (Pusa caspica) were analyzed in retinal whole mounts stained with cresyl-violet. The topographic distribution of ganglion cells displayed an area of high cell density located in the temporal quadrant of the retina and was similar to the area centralis of terrestrial carnivores. It extended nasally, above the optic disk, as a streak of increased cell density. In different whole mounts, the peak cell density in the high-density area ranged from 1,684 to 1,844 cells/mm2 (mean 1,773 cells/mm2). The cell density data predict a retinal resolution of around 8.5 cycles/degree in water. A distinctive feature of the Caspian seal's retina is the large size of ganglion cells and the low cell density compared to terrestrial mammals. The ganglion cell diameter ranged from 10 to 58 μm. Cell size histograms featured bimodal patterns with groups of small and large ganglion cells. The large cells appeared similar to α-cells of terrestrial mammals and constituted 7% of the total ganglion cell population.     

Retinal ganglion cell inputs to the koniocellular pathway

To understand the transmission of sensory signals in visual pathways we studied the morphology and central projection of ganglion cell populations in marmoset monkeys. Retinal ganglion cells were labeled by photofilling following injections of retrograde tracer in the lateral geniculate nucleus (LGN), or by intracellular injection with neurobiotin. Ganglion cell morphology was analyzed using hierarchical cluster analysis. In addition to midget and parasol ganglion cells, this method distinguished three main clusters of wide-field cells that correspond to small bistratified, sparse, and broad thorny cells identified previously. The small bistratified and sparse cells occupy neighboring positions on the hierarchical (linkage distance) tree. These cell types are presumed to carry signals originating in short-wavelength sensitive (S or "blue") cones in the retina. The linkage distance from these putative S-cone pathway ganglion cells to other wide-field cells is similar to the linkage distance from midget cells to parasol cells, suggesting that S-cone cells form a distinct functional subgroup of ganglion cells. Small bistratified cells and large sparse cells were the most commonly labeled wide-field cells following LGN injections in koniocellular layer K3. This is consistent with physiological evidence that the role of this layer includes transmission of S-cone signals to the visual cortex. Other wide-field cell types were also labeled following injections including K3, and other koniocellular LGN layers; these cell types may correspond to "non-blue koniocellular" receptive fields recorded in physiological studies.     

The topography of ganglion cell production in the cat's retina

The ganglion cells of the cat's retina form several classes distinguishable in terms of soma size, axon diameter, dendritic morphology, physiological properties, and central connections. Labeling with [3H]thymidine shows that the ganglion cells which survive in the adult are produced as several temporally shifted, overlapping waves: medium-sized cells are produced before large cells, whereas the smallest ganglion cells are produced throughout the period of ganglion cell generation (Walsh, C., E. H. Polley, T. L. Hickey, and R. W. Guillery (1983) Nature 302: 611-614). Large cells and medium-sized cells show the same distinctive pattern of production, forming rough spirals around the area centralis. The oldest cells tend to lie superior and nasal to the area centralis, whereas cells in the inferior nasal retina and inferior temporal retina are, in general, progressively younger. Within each retinal quadrant, cells nearer the area centralis tend to be older than cells in the periphery, but there is substantial overlap. The retinal raphe divides the superior temporal quadrant into two zones with different patterns of cell addition. Superior temporal retina near the vertical meridian adds cells only slightly later than superior nasal retina, whereas superior temporal retina near the horizontal meridian adds cells very late, contemporaneously with inferior temporal retina. The broader wave of production of smaller ganglion cells seems to follow this same spiral pattern at its beginning and end. The presence of the area centralis as a nodal point about which ganglion cell production in the retinal quadrants pivots suggests that the area centralis is already an important retinal landmark even at the earliest stages of retinal development. This sequence of ganglion cell production differs markedly from that seen in the retinae of nonmammalian vertebrates, where new ganglion cells are added as concentric rings to the retinal periphery, and also bears no simple relationship to the cat's retinal decussation line. However, it can be related in a straightforward manner to the organization of axons in the cat's optic tract, suggesting that the fiber order in the tract represents a grouping of fibers by age.     

Retinal ganglion cell morphology in the frog, Rana pipiens

The morphology of retinal ganglion cells in the frog, Rana pipiens, has been examined in retinal flatmounts following backfilling of axons with horseradish peroxidase (HRP). Size and shape of the cell body and of the dendritic arbor, the dendritic branching pattern, and the depth of dendritic arborization within the inner plexiform layer (IPL) were all used to classify these cells. All of the ganglion cells so visualized can be grouped into one of 7 distinct cell classes. Class 1 contains the largest ganglion cells, with a soma size of 323 +/- 5.3 microns2 and dendritic fields of 86,819 +/- 11,817 microns2; the dendrites branch within strata 1 and 2 of the IPL. The second largest cells are class 2, with somas of 245 +/- 19.7 microns2 and dendritic fields of 55,983 +/- 7,392 microns2; the dendrites also branch within strata 1 and 2 of the IPL. Class 3 cells are the next largest class with somas of 211 +/- 11.8 microns2 and dendritic fields of 18,186 +/- 1,394 microns2; there are three varieties of class 3 cells based on the depth of branching of the dendrites: some cells are bistratified, others are tristratified, while still other cells arborize diffusely within the IPL. Class 4 cells are intermediate in size, with somas of 113 +/- 7.4 microns2 and dendrites of 4800 +/- 759 microns2; the dendrites arborize within strata 4 and 5 of the IPL. Class 5 cells have not been quantitatively analyzed because they are heterogeneous in soma and dendritic size. However, class 5 cells all have cell bodies displaced in location into the inner nuclear layer and all have a unique dendritic specialization: they send from 1 to 3 processes into the outer plexiform layer. Class 6 cells are the second smallest cell class with somas of 68.1 +/- 5.13 microns2 and dendritic fields of 888 +/- 182 microns2; the dendrites arborize within strata 3, 4, and 5 of the IP. Class 7 contains the smallest ganglion cells with somas of 62.1 +/- 2.86 microns2 and dendritic fields of 831 +/- 74.2 microns2; the dendrites arborize within strata 3, 4, and 5 of the IPL. The frequency of each cell class is inversely proportional to the size of the dendritic field. Thus, class 7 cells are the most frequent; class 1 cells are the least frequent. Furthermore, each of these 7 classes of ganglion cells has representative cells located in the inner nuclear layer.(ABSTRACT TRUNCATED AT 400 WORDS)     

Retinal ganglion cell line apoptosis induced by hydrostatic pressure

Cellular responses to changes in pressure are implicated in numerous disease processes. In glaucoma apoptosis of retinal ganglion cells (RGCs) is associated with elevated intra-ocular pressure, however, the exact cellular mechanisms remain unclear. We have previously shown that pressure can induce apoptosis in B35 and PC12 neuronal cell lines, using an in vitro model for pressure elevation. A novel RGC line allows us to study the effects of pressure on retinal neurons. 'RGC-5' cultures were subjected to elevated ambient hydrostatic pressure conditions in our model. Experimental pressure conditions were 100 mm Hg and 30 mm Hg, representing acute (high) and chronic (lower-pressure) glaucoma, and 15 mm Hg for normal intra-ocular pressure, set above atmospheric pressure for 2 h. Negative controls were treated identically except for the application of pressure, while positive controls were generated by treatment with a known apoptotic stimulus. Apoptosis was determined by a combination of cell morphology and specific TUNEL and Annexin V fluorescent markers. These were assessed simultaneously by laser scanning cytometry (LSC), which also enabled quantitative marker analysis. RGC-5 neurons showed a significantly increased proportion of apoptotic cells compared with controls; maximal at 100 mm Hg, moderate at 30 mm Hg and not statistically significant at 15 mm Hg. This graded response, proportionate to the level of pressure elevation, is representative of the severity of analogous clinical settings (acute, chronic glaucoma and normal). These results complement earlier findings of pressure-induced apoptosis in other neuronal cultures. They suggest the possibility of novel mechanisms of pressure-related mechanotransduction and cell death, relevant to the pathogenesis of diseases such as glaucoma.     

Retinal ganglion cell dendritic fields in old-world monkeys are oriented radially

We analyzed the dendritic field morphology of 297 ganglion cells from peripheral regions of monkey retina. Most of the dendritic fields were elongated, and there was a significant tendency for the dendritic fields to be oriented radially, i.e., like the spokes of a wheel with the fovea at the hub. An overrepresentation of radial orientations in the peripheral retina of primates might explain why humans are best able to detect stimuli which are oriented radially using peripheral vision.     

Retinal remodeling following photoreceptor degeneration causes retinal ganglion cell death

正The retina is the extension of the central nervous system that senses light.Cones and rods,situated in the outer retina,convert light into electrical signals that travel through intermediate neurons where these are further processed until they finally reach retinal ganglion cells(RGCs).The afferent neurons of the retina,the RGCs,send the     

Relationships between ganglion cell dendritic structure and retinal topography in the cat

The morphology of ganglion cell dendritic trees varies across the cat retina. Evidence is presented that the variation in two attributes of ganglion cell dendritic structure can be accounted for by specific aspects of the topography of the adult and developing retina. The first attribute considered was the displacement of the center of the dendritic field from the cell body in the plane of the retina. The results of this study provide evidence that most ganglion cell dendritic fields are displaced away from neighboring cells, i.e., down the retinal ganglion cell density gradient. Because of the systematic dendritic displacement locally, the centers of the dendritic fields are arranged in a more precise mosaic than are their cell bodies. The second attribute considered was the elongation and orientation of the dendritic fields. From approximately embryonic day 50 to postnatal day 10 the cat retina undergoes a process of maturation (reviewed by Rapaport and Stone: Neuroscience 11:289-301, '84) that begins at the area centralis and spreads over the retina in a horizontally elongated wave. We found that the elongation and orientation of retinal ganglion cell dendritic fields is significantly correlated with the shape of the wave of maturation. The orientation of a dendritic field is not predicted by the direction of its displacement nor is it directly related to the distribution of neighboring retinal ganglion cells. These results indicate that the displacement of a ganglion cell's dendritic field from its cell body results from mechanisms different from those responsible for the orientation of the dendritic field. Factors that may be responsible for these two attributes of ganglion cell dendritic morphology are discussed.     

Retinal ganglion cell axons regenerate in the presence of intact sensory fibres

A novel allograft paradigm was used to test whether adult mammalian central axons regenerate within a peripheral nerve environment containing intact sensory axons. Retinal ganglion cell axon regeneration was compared following anastomosis of dorsal root ganglia grafts or conventional peripheral nerve grafts to the adult rat optic nerve. Dorsal root ganglia grafts comprised intact sensory and degenerate motor axons, whereas conventional grafts comprised both degenerating sensory and motor axons. Retinal ganglion cell axons were traced after 2 months. Dorsal root ganglia survived with their axons persisting throughout the graft. Comparable numbers of retinal ganglion cells regenerated axons into both dorsal root ganglia (1053+/-223) and conventional grafts (1323+/-881; P>0.05). The results indicate that an intact sensory environment supports central axon regeneration.     

A quantitative analysis of the cat retinal ganglion cell topography.

A retinal ganglion cell distribution map has been prepared for the cresyl violet stained cat retina. It differs from previously published maps in revealing the visual streak to be more substantial and in showing a higher peak density of 9-10,000 ganglion cells/mm2 at the presumed visual pole. The map was used to obtain a minimum estimate of the retinal ganglion cell population as 217,000 cells, more than double the total previously reported. The problem of classifying the cells of the ganglion cell layer is discussed in detail and examples of criterion cells illustrated. The paper also includes an account of retinal mensuration (dimensions, area, etc.) and a discussion of the visual streak orientation.