Comparative visual function in elasmobranchs: Spatial arrangement and ecological correlates of photoreceptor and ganglion cell distributions

2008 ◽  
Vol 25 (4) ◽  
pp. 549-561 ◽  
Author(s):  
LENORE LITHERLAND ◽  
SHAUN P. COLLIN
Keyword(s):  
Ganglion Cell ◽  
Behavioral Ecology ◽  
Ganglion Cells ◽  
Spatial Arrangement ◽  
Resolving Power ◽  
Cresyl Violet ◽  
Topographic Analysis ◽  
Scotopic Vision ◽  
Preferential Sampling ◽  
Epaulette Shark

AbstractThe topographic analysis of retinal ganglion and photoreceptor cell distributions yields valuable information for assessing the visual capabilities and behavioral ecology of vertebrates. This study examines whole-mounted retinas of four elasmobranch species, the ornate wobbegong, Orectolobus ornatus; the whitetip reef shark, Triaenodon obesus; the epaulette shark, Hemiscyllium ocellatum; and the east Australia shovelnose ray, Aptychotrema rostrata, for regional specializations mediating zones of improved visual ability. These species represent a range of lifestyles: benthic, mid-water, diurnal, and nocturnal. Both photoreceptors (visualized using differential interference contrast optics) and ganglion cells (stained with cresyl violet) in the retina are extensively sampled, and their spatial distribution is found to be nonuniform, exhibiting areae or “visual streaks.” In general, the topographic distributions of both cell populations are in register and match well with respect to the location of regions of high density. However, the location of peaks in rod and cone densities can vary within a retina, indicating that preferential sampling of different regions of the visual field may occur in photopic and scotopic vision. Anatomical measures of the optical limits of resolving power, indicated by intercone spacing, range from 3.8 to 13.1 cycles/deg. Spatial limits of resolving power, calculated from ganglion cell spacing, range from 2.6 to 4.3 cycles/deg. Summation ratios, assessed by direct comparison of cell densities of photoreceptors (input cells) and ganglion cells (output cells), at more than 150 different loci across the retina, show topographic differences in signal convergence (ranging from 25:1 to over 70:1). Species-specific retinal specializations strongly correlate to the habitat and feeding behavior of each species.

Eye growth in sharks: Ecological implications for changes in retinal topography and visual resolution

2009 ◽  
Vol 26 (4) ◽  
pp. 397-409 ◽  
Author(s):  
LENORE LITHERLAND ◽  
SHAUN P. COLLIN ◽  
KERSTIN A. FRITSCHES
Keyword(s):  
Ganglion Cell ◽  
Spatial Resolution ◽  
Ganglion Cells ◽  
Feeding Strategy ◽  
Resolving Power ◽  
Foraging Strategies ◽  
Sandbar Shark ◽  
Topographic Analysis ◽  
Eye Growth ◽  
Topographic Distribution

AbstractThe visual abilities of sharks show substantial interspecific variability. In addition, sharks may change their habitat and feeding strategy throughout life. As the eyes of sharks continue to grow throughout the animal’s lifetime, ontogenetic variability in visual ability may also occur. The topographic analysis of the photoreceptor and ganglion cell distributions can identify visual specializations and assess changes in visual abilities that may occur concurrently with eye growth. This study examines an ontogenetic series of whole-mounted retinas in two elasmobranch species, the sandbar shark, Carcharhinus plumbeus, and the shortspine spurdog, Squalus mitsukurii, to identify regional specializations mediating zones for improved spatial resolution. The study examines retinal morphology and presents data on summation ratios between photoreceptor and ganglion cell layers, anatomically determined peak spatial resolving power, and the angular extent of the visual field. Peak densities of photoreceptors and ganglion cells occur in similar retinal locations. The topographic distribution of neurons in the ganglion cell layer does not differ substantially with eye growth. However, predicted peak spatial resolution increases with eye growth from 4.3 to 8.9 cycles/deg in C. plumbeus and from 5.7 to 7.2 cycles/deg in S. mitsukurii. The topographic distribution of different-sized ganglion cells is also mapped in C. plumbeus, and a population of large ganglion cells (soma area 120–350 μm2) form a narrow horizontal streak across the retinal meridian, while the spatial distribution of ordinary-sized ganglion cells (soma area 30–120 μm2) forms an area in the central retina. Species-specific retinal specializations highlight differences in visually mediated behaviors and foraging strategies between C. plumbeus and S. mitsukurii.

Visual Specializations in Five Sympatric Species of Stingrays from the Family Dasyatidae

2015 ◽  
Vol 85 (4) ◽  
pp. 217-232 ◽  
Author(s):  
Eduardo Garza-Gisholt ◽  
Ryan M. Kempster ◽  
Nathan S. Hart ◽  
Shaun P. Collin
Keyword(s):  
Ganglion Cells ◽  
Sympatric Species ◽  
Geographic Region ◽  
Resolving Power ◽  
Retinal Cell ◽  
Ecological Niches ◽  
Scotopic Vision ◽  
Peak Density ◽  
The Family ◽  
Cell Densities

The eyes of five ray species (Taeniura lymma, Neotrygon kuhlii, Pastinachus atrus, Himantura uarnak and Urogymnus asperrimus) from the same taxonomic family (Dasyatidae) and the same geographic region (Ningaloo Reef, Western Australia) were studied to identify differences in retinal specializations that may reflect niche specialization. The topographic distributions of photoreceptors (rods and all cones) and ganglion cells were assessed and used to identify localized peaks in cell densities that indicate specializations for acute vision. These data were also used to calculate summation ratios of photoreceptors to ganglion cells in each species and estimate the anatomical spatial resolving power of the eye. Subtle differences in the distribution of retinal neurons appear to be related to the ecology of these closely related species of stingrays. The main specialization in the retinal cell density distribution is the dorsal streak that allows these animals to scan the substrate for potential prey. The blue-spotted fantail ray, T. lymma, showed the highest peak density of rods (86,700 rods mm-2) suggesting a specialization for scotopic vision. The highest peak density of cones (9,970 cones mm-2) was found in H. uarnak, and the highest peak density of ganglion cells (4,500 cells mm-2) was found in P. atrus. The proportion of rods to cones in the dorsal streak was higher in the two smaller species (12.5-14:1 in T. lymma and N. kuhlii) than the larger stingrays (6-8:1 in P. atrus, H. uarnak and U. asperrimus). Visual specializations in different sympatric species are subtle but may reflect specializations to specific ecological niches.

A second episode of ganglion cell death takes place when an optic nerve regenerates for a second time in the frog

1993 ◽  
Vol 10 (2) ◽  
pp. 297-301 ◽  
Author(s):  
L. D. Beazley ◽  
J.E. Darby
Keyword(s):  
Cell Death ◽  
Optic Nerve ◽  
Ganglion Cell ◽  
Ganglion Cells ◽  
Cresyl Violet ◽  
Retinal Ganglion ◽  
Nerve Crush ◽  
Optic Nerve Regeneration ◽  
Ability To Regenerate ◽  
Ganglion Cell Death

AbstractWe have previously reported that during optic nerve regeneration in the frog, 30–40% of retinal ganglion cells die, the loss being complete within 10 weeks. In the present study, we crushed the optic nerve, waited 10 weeks, and then recrushed the nerve at the same site. Retinae were examined 10 weeks later. We estimated ganglion cell numbers from cresyl-violet-stained wholemounts and found a fall of 53% compared to normals. The loss was significantly greater than the losses of 36% and 35%, respectively, in frogs which received a single optic nerve crush and were examined 10 or 20–24 weeks later. The results indicate that a second episode of ganglion cell death took place when the optic nerve regenerated a second time. We conclude that ganglion cells in the frog are not comprised of two subpopulations, only one of which intrinsically possesses the ability to regenerate.

Immuocytochemical analysis of spatial organization of photoreceptors and amacrine and ganglion cells in the tiger salamander retina

2004 ◽  
Vol 21 (2) ◽  
pp. 157-166 ◽  
Author(s):  
JIAN ZHANG ◽  
ZHUO YANG ◽  
SAMUEL M. WU
Keyword(s):  
Ganglion Cell ◽  
Spatial Organization ◽  
Ganglion Cells ◽  
Electrophysiological Study ◽  
Outer Nuclear Layer ◽  
Amacrine Cells ◽  
Spatial Arrangement ◽  
Cell Types ◽  
Proximal Region ◽  
Dorsal Retina

In the present study, using double- or triple-label immunocytochemistry in conjunction with confocal microscopy, we aimed to examine the population and distribution of photoreceptors, GABAergic and glycinergic amacrine cells, and ganglion cells, which are basic but important parameters for studying the structure–function relationship of the salamander retina. We found that the outer nuclear layer (ONL) contained 82,019 ± 3203 photoreceptors, of which 52% were rods and 48% were cones. The density of photoreceptors peaked at ∼8000 cells/mm2 in the ventral and dropped to ∼4000 cells/mm2 in the dorsal retina. In addition, the rod/cone ratio was less than 1 in the central retina but larger than 1 in the periphery. Moreover, in the proximal region of the inner nuclear layer (INL3), the total number of cells was 50,576 ± 8400. GABAergic and glycinergic amacrine cells made up approximately 78% of all cells in this layer, including 43% GABAergic, 32% glycinergic, and 3% GABA/glycine colocalized amacrine cells. The density of these amacrine cells was ∼6500 cells/mm2 in the ventral and ∼3200 cells/mm2 in the dorsal area. The ratio of GABAergic to glycinergic amacrine cells was larger than 1. Furthermore, in the ganglion cell layer (GCL), among a total of 36,007 ± 2010 cells, ganglion cells accounted for 65.7 ± 1.5% of the total cells, whereas displaced GABAergic and glycinergic amacrine cells comprised about 4% of the cells in this layer. The ganglion cell density was ∼1800 cells/mm2 in the ventral and ∼600 cells/mm2 in the dorsal retina. Our data demonstrate that all three major cell types are not uniformly distributed across the salamander retina. Instead, they exhibit a higher density in the ventral than in the dorsal retina and their spatial arrangement is associated with the retinal topography. These findings provide a basic anatomical reference for the electrophysiological study of this species.

Visual Capability of the Weakly Electric Fish Apteronotus albifrons as Revealed by a Modified Retinal Flat-Mount Method

2015 ◽  
Vol 86 (2) ◽  
pp. 122-130 ◽  
Author(s):  
Tomo Takiyama ◽  
Valdir Luna da Silva ◽  
Daniel Moura Silva ◽  
Sawako Hamasaki ◽  
Masayuki Yoshida
Keyword(s):  
Ganglion Cell ◽  
Ganglion Cells ◽  
Pigment Epithelium ◽  
The Body ◽  
Weakly Electric Fish ◽  
Resolving Power ◽  
Cell Distribution ◽  
High Acuity ◽  
Continuous Sheet ◽  
Cell Densities

Apteronotus albifrons (Gymnotiformes, Apteronotidae) is well known to have a sophisticated active electrosense system and is commonly described as having poor vision or being almost blind. However, some studies on this species suggest that the visual system may have a role in sensing objects in the environment. In this study, we investigated the visual capabilities of A. albifrons by focusing on eye morphology and retinal ganglion cell distribution. The eyes were almost embedded below the body surface and pigmented dermal tissue covered the peripheral regions of the pupil, limiting the direction of incoming light. The lens was remarkably flattened compared to the almost spherical lenses of other teleosts. The layered structure of the retina was not well delineated and ganglion cells did not form a continuous sheet of cell bodies. A newly modified retinal flat-mount method was applied to reveal the ganglion cell distribution. This method involved postembedding removal of the pigment epithelium of the retina for easier visualization of ganglion cells in small and/or fragile retinal tissues. We found that ganglion cell densities were relatively high in the periphery and highest in the nasal and temporal retina, although specialization was not so high (approx. 3:1) with regard to the medionasal or mediotemporal axis. The estimated highest possible spatial resolving power was around 0.57 and 0.54 cycles/degree in the nasal and temporal retina, respectively, confirming the lower importance of the visual sense in this species. However, considering the hunting nature of A. albifrons, the relatively high acuity of the caudal visual field in combination with electrolocation may well be used to locate prey situated close to the side of the body.

Topographic analysis of the ganglion cell layer in the retina of the four-eyed fish Anableps anableps

2006 ◽  
Vol 23 (6) ◽  
pp. 879-886 ◽  
Author(s):  
FRANCISCO GILBERTO OLIVEIRA ◽  
JOÃO PAULO COIMBRA ◽  
ELIZABETH SUMI YAMADA ◽  
LUCIANO FOGAÇA DE ASSIS MONTAG ◽  
FRANCYLLENA L. NASCIMENTO ◽  
...  
Keyword(s):  
Visual Field ◽  
Ganglion Cell ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Behavioral Strategies ◽  
Topographic Analysis ◽  
Contour Maps ◽  
Visual Streak ◽  
Peak Cell Density

Fish of the genus Anableps (Anablepidae, Cyprinodontiformes) have eyes that are adapted for simultaneous aerial and aquatic vision. In this study we investigate some of the corresponding retinal specializations of the adult Anableps anableps eye using retinal transverse sections and wholemounts. The linear dimensions of the retina were found to be asymmetric with a greater representation of the dorsal compared to the ventral visual field. The total number of neurons in the ganglion cell layer of the ventral hemiretina was on average 3.6 times greater than the values obtained in the dorsal hemiretina. Isodensity contour maps revealed a prominent horizontal visual streak in the ventral hemiretina with an average peak cell density of 18,286 cells/mm2. A second less-well-developed horizontal visual streak was also observed in the dorsal hemiretina. A sub-population of large cells with soma areas between 74 and 188 μm2 was identified and found to be distributed evenly across both hemiretinas. Together, these results show that the sampling gain of the ventral retina is significantly greater than the dorsal segment, that retinal specializations important for mediating acute vision are present in the parts of the visual field immediately above and below the surface of the water, and that visual functions related with the large ganglion cells require more even sampling across the visual field. The relevance of these retinal specializations to the feeding and other behavioral strategies adopted by Anableps is discussed.

The number, morphology, and distribution of retinal ganglion cells and optic axons in the Australian lungfishNeoceratodus forsteri(Krefft 1870)

2006 ◽  
Vol 23 (2) ◽  
pp. 257-273 ◽  
Author(s):  
HELENA J. BAILES ◽  
ANN E.O. TREZISE ◽  
SHAUN P. COLLIN
Keyword(s):  
Optic Nerve ◽  
Ganglion Cell ◽  
Retinal Ganglion Cells ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Resolving Power ◽  
Retinal Ganglion ◽  
Retrograde Labelling

Australian lungfishNeoceratodus forsterimay be the closest living relative to the first tetrapods and yet little is known about their retinal ganglion cells. This study reveals that lungfish possess a heterogeneous population of ganglion cells distributed in a horizontal streak across the retinal meridian, which is formed early in development and maintained through to adult stages. The number and complement of both ganglion cells and a population of putative amacrine cells within the ganglion cell layer are examined using retrograde labelling from the optic nerve and transmission electron-microscopic analysis of axons within the optic nerve. At least four types of retinal ganglion cells are present and lie predominantly within a thin ganglion cell layer, although two subpopulations are identified, one within the inner plexiform and the other within the inner nuclear layer. A subpopulation of retinal ganglion cells comprising up to 7% of the total population are significantly larger (>400 μm2) and are characterized as giant or alpha-like cells. Up to 44% of cells within the retinal ganglion cell layer represent a population of presumed amacrine cells. The optic nerve is heavily fasciculated and the proportion of myelinated axons increases with body length from 17% in subadults to 74% in adults. Spatial resolving power, based on ganglion cell spacing, is low (1.6–1.9 cycles deg−1,n= 2) and does not significantly increase with growth. This represents the first detailed study of retinal ganglion cells in sarcopterygian fish, and reveals that, despite variation amongst animal groups, trends in ganglion cell density distribution and characteristics of cell types were defined early in vertebrate evolution.

The Topographic Organization of Retinal Ganglion Cell Density and Spatial Resolving Power in an Unusual Arboreal and Slow-Moving Strepsirhine Primate, the Potto (Perodicticus potto)

2016 ◽  
Vol 87 (1) ◽  
pp. 4-18 ◽  
Author(s):  
João Paulo Coimbra ◽  
Consolate Kaswera-Kyamakya ◽  
Emmanuel Gilissen ◽  
Paul R. Manger ◽  
Shaun P. Collin
Keyword(s):  
Ganglion Cell ◽  
Cell Density ◽  
Retinal Ganglion Cells ◽  
Spatial Resolution ◽  
Ganglion Cells ◽  
Resolving Power ◽  
Retinal Ganglion ◽  
Upper Limits ◽  
Slow Moving ◽  
Topographic Distribution

The potto (Perodicticus potto) is an arboreal strepsirhine found in the rainforests of central Africa. In contrast to most primates, the potto shows slow-moving locomotion over the upper surface of branches, where it forages for exudates and crawling invertebrates with its head held very close to the substrate. Here, we asked whether the retina of the potto displays topographic specializations in neuronal density that correlate with its unusual lifestyle. Using stereology and retinal wholemounts, we measured the total number and topographic distribution of retinal ganglion cells (total and presumed parasol), as well as estimating the upper limits of the spatial resolution of the potto eye. We estimated ∼210,000 retinal ganglion cells, of which ∼7% (∼14,000) comprise presumed parasol ganglion cells. The topographic distribution of both total and parasol ganglion cells reveals a concentric centroperipheral organization with a nasoventral asymmetry. Combined with the upwardly shifted orbits of the potto, this nasoventral increase in parasol ganglion cell density enhances contrast sensitivity and motion detection skywards, which potentially assists with the detection of predators in the high canopy. The central area of the potto occurs ∼2.5 mm temporal to the optic disc and contains a maximum ganglion cell density of ∼4,300 cells/mm2. We found no anatomical evidence of a fovea within this region. Using maximum ganglion cell density and eye size (∼14 mm), we estimated upper limits of spatial resolving power between 4.1 and 4.4 cycles/degree. Despite their reported reliance on olfaction to detect exudates, this level of spatial resolution potentially assists pottos with foraging for small invertebrates and in the detection of predators.

scholarly journals Retinal specializations to a micro-predatory and crypto-benthic life-style in the Mediterranean triplefin blenny Tripterygion delaisi

2017 ◽  
Author(s):  
Roland Fritsch ◽  
Shaun P. Collin ◽  
Nico K. Michiels
Keyword(s):  
Visual Field ◽  
Ganglion Cell ◽  
Cross Sections ◽  
Ganglion Cells ◽  
Average Density ◽  
Resolving Power ◽  
Retinal Ganglion ◽  
Vast Number ◽  
The Mediterranean ◽  
Tripterygion Delaisi

AbstractThe environment and lifestyle of a species are known to exert selective pressure on the visual system, often demonstrating a tight link between visual morphology and ecology. Many studies have predicted the visual requirements of a species by examining the anatomical features of the eye. However, among the vast number of studies on visual specializations in aquatic animals, only a few have focused on small benthic fishes that occupy a heterogeneous and spatially complex visual environment. This study investigates the general retinal anatomy including the topography of both the photoreceptor and ganglion cell populations and estimates the spatial resolving power of the eye of the Mediterranean triplefin Tripterygion delaisi. Retinal wholemounts were prepared to systematically and quantitatively analyze photoreceptor and retinal ganglion cell densities using design-based stereology. To further examine the retinal structure, we also used magnetic resonance imaging and histological examination of retinal cross sections. Observations of the triplefin's eyes revealed them to be highly mobile, allowing them to view the surroundings without body movements. A rostral aphakic gap and the elliptical shape of the eye extend its visual field rostrally and allow for a rostro-caudal accommodatory axis, enabling this species to focus on prey at close range. Single and twin cones dominate the retina and are consistently arranged in one of two regular patterns, which may enhance motion detection and color vision. The retina features a prominent, dorso-temporal, convexiclivate fovea with an average density of 104,400 double and 30,800 single cones per mm2, and 81,000 retinal ganglion cells per mm2. Based on photoreceptor spacing, spatial resolving power was calculated to be between 6.7 and 9.0 cycles per degree. Location and resolving power of the fovea would benefit the detection and identification of small prey in the lower frontal region of the visual field.

A morphological classification of ganglion cells in the zebrafish retina

2002 ◽  
Vol 19 (6) ◽  
pp. 767-779 ◽  
Author(s):  
WELLS I. MANGRUM ◽  
JOHN E. DOWLING ◽  
ETHAN D. COHEN
Keyword(s):  
Ganglion Cell ◽  
Ganglion Cells ◽  
Central Area ◽  
Plexiform Layer ◽  
Cell Types ◽  
Cresyl Violet ◽  
Blue Staining ◽  
Inner Plexiform Layer ◽  
Branching Patterns ◽  
Type V

We examined the distribution and morphological types of ganglion cells in the retina of the zebrafish, a model vertebrate genetic organism. Using cresyl violet and methylene blue staining, a prominent central area was observed in the ventral temporal retina. The density of ganglion cell layer neurons averaged from ∼12,000/mm2 in the dorsal-nasal retina to a peak of ∼37,000/mm2 in the ventral-temporal retina. Individual zebrafish ganglion cells were labeled by backfilling with DiI through the optic nerve followed by reconstruction using confocal microscopy. The dendritic stratification and branching pattern of each labeled ganglion cell was examined in relation to the borders of the inner plexiform layer (IPL). We identified 11 different morphological types of ganglion cell. The most commonly labeled ganglion cells were two types termed Type III or IV, which displayed highly stratified dendritic arborizations in their respective ON-, OFF-sublaminae of the IPL. Their dendritic branching patterns were highly asymmetric with many thorn-like varicosities that profusely filled the area of arborization. In contrast, Type V cells formed a small simply branching dendritic field in the innermost portion of the ON-sublamina of the IPL. Two large ganglion cell types (Types I and II) with wide monostratified dendritic fields were found in both the ON- and OFF-sublamina of the IPL. Three different types of multistratified/bistratified ganglion cells were found (Types, IX, X, and XI.) whose dendrites occupied different regions of the IPL. The multistratified dendrites of IX cells occupied the whole width of the IPL, while the dendrites of Type XI cells formed vertical claw-like endings in only the ON-sublamina of the IPL. We conclude that zebrafish ganglion cells display a rich variety of types and branching patterns. This study establishes a series of baseline measurements of zebrafish ganglion cells to facilitate examination of genes playing a role in the specification and stratification of ganglion cell types.

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