Functional differences between the extraordinary eyes of deep-sea hyperiid amphipods.

The ocean's midwater is a uniquely challenging yet predictable and simple visual environment. The need to see without being seen in this dim, open habitat has led to extraordinary visual adaptations. To understand these adaptations, we compared the morphological and functional differences between the eyes of three hyperiid amphipods-Hyperia galba, Streetsia challengeri and Phronima sedentaria. Combining micro-CT data with computational modelling, we mapped visual field topography and predicted detection distances for visual targets viewed in different directions through mesopelagic depths. Hyperia's eyes provide a wide visual field optimized for spatial vision over short distances, while Phronima's and Streetsia's eyes have the potential to achieve greater sensitivity and longer detection distances using spatial summation. These improvements come at the cost of smaller visual fields, but this loss is compensated for by a second pair of eyes in Phronima and by behaviour in Streetsia. The need to improve sensitivity while minimizing visible eye size to maintain crypsis has likely driven the evolution of hyperiid eye diversity. Our results provide an integrative look at how these elusive animals have adapted to the unique visual challenges of the mesopelagic.

Visual system diversity in coral reef fishes.

Coral reefs are one of the most species rich and colourful habitats on earth and for many coral reef teleosts, vision is central to their survival and reproduction. The diversity of reef fish visual systems arises from variations in ocular and retinal anatomy, neural processing and, perhaps most easily revealed by, the peak spectral absorbance of visual pigments. This review examines the interplay between retinal morphology and light environment across a number of reef fish species, but mainly focusses on visual adaptations at the molecular level (i.e. visual pigment structure). Generally, visual pigments tend to match the overall light environment or micro-habitat, with fish inhabiting greener, inshore waters possessing longer wavelength-shifted visual pigments than open water blue-shifted species. In marine fishes, particularly those that live on the reef, most species have between two (likely dichromatic) to four (possible tetrachromatic) cone spectral sensitivities and a single rod for crepuscular vision; however, most are trichromatic with three spectral sensitivities. In addition to variation in spectral sensitivity number, spectral placement of the absorbance maximum (λmax) also has a surprising degree of variability. Variation in ocular and retinal anatomy is also observed at several levels in reef fishes but is best represented by differences in arrangement, density and distribution of neural cell types across the retina (i.e. retinal topography). Here, we focus on the seven reef fish families most comprehensively studied to date to examine and compare how behaviour, environment, activity period, ontogeny and phylogeny might interact to generate the exceptional diversity in visual system design that we observe.

Seeing Picasso: an investigation into the visual system of the triggerfish Rhinecanthus aculeatus.

Vision is used by animals to find food and mates, avoid predators, defend resources and navigate through complex habitats. Behavioural experiments are essential for understanding animals' perception but are often challenging and time-consuming; therefore, using species that can be trained easily for complex tasks is advantageous. Picasso triggerfish, Rhinecanthus aculeatus, have been used in many behavioural studies investigating vision and navigation. However, little is known about the molecular and anatomical basis of their visual system. We addressed this knowledge gap here and behaviourally tested achromatic and chromatic acuity. In terms of visual opsins, R. aculeatus possessed one rod opsin gene (RH1) and at least nine cone opsins: one violet-sensitive SWS2B gene, seven duplicates of the blue-green-sensitive RH2 gene (RH2A, RH2B, RH2C1-5) and one red-sensitive LWS gene. However, only five cone opsins were expressed: SWS2B expression was consistent, while RH2A, RH2C-1 and RH2C-2 expression varied depending on whether fish were sampled from the field or aquaria. Levels of LWS expression were very low. Using fluorescence in situ hybridisation, we found SWS2B was expressed exclusively in single cones, whereas RH2A and RH2Cs were expressed in opposite double cone members. Anatomical resolution estimated from ganglion cell densities was 6.8 cycles per degree (cpd), which was significantly higher than values obtained from behavioural testing for black-and-white achromatic stimuli (3.9 cpd) and chromatic stimuli (1.7-1.8 cpd). These measures were twice as high as previously reported. This detailed information on their visual system will help inform future studies with this emerging focal species.

Sex differences in behavioural and anatomical estimates of visual acuity in the green swordtail, Xiphophorus helleri.

Among fishes in the family Poeciliidae, signals such as colour patterns, ornaments and courtship displays play important roles in mate choice and male-male competition. Despite this, visual capabilities in poeciliids are understudied, in particular, visual acuity, the ability to resolve detail. We used three methods to quantify visual acuity in male and female green swordtails (Xiphophorus helleri), a species in which body size and the length of the male's extended caudal fin ('sword') serve as assessment signals during mate choice and agonistic encounters. Topographic distribution of retinal ganglion cells (RGCs) was similar in all individuals and was characterized by areas of high cell densities located centro-temporally and nasally, as well as a weak horizontal streak. Based on the peak density of RGCs in the centro-temporal area, anatomical acuity was estimated to be approximately 3 cycles per degree (cpd) in both sexes. However, a behavioural optomotor assay found significantly lower mean acuity in males (0.8 cpd) than females (3.0 cpd), which was not explained by differences in eye size between males and females. An additional behavioural assay, in which we trained individuals to discriminate striped gratings from grey stimuli of the same mean luminance, also showed lower acuity in males (1-2 cpd) than females (2-3 cpd). Thus, although retinal anatomy predicts identical acuity in males and females, two behavioural assays found higher acuity in females than males, a sexual dimorphism that is rare outside of invertebrates. Overall, our results have implications for understanding how poeciliids perceive visual signals during mate choice and agonistic encounters.

Retinal Ganglion Cell Topography and Spatial Resolving Power in Echolocating and Non-Echolocating Bats.

Bats are nocturnal mammals known for their ability to echolocate, yet all bats can see, and most bats of the family Pteropodidae (fruit bats) do not echolocate - instead they rely mainly on vision and olfaction to forage. We investigated whether echolocating bats, given their limited reliance on vision, have poorer spatial resolving power (SRP) than pteropodids and whether tongue click echolocating fruit bats differ from non-echolocating fruit bats in terms of visual performance. We compared the number and distribution of retinal ganglion cells (RGCs) as well as the maximum anatomical SRP derived from these distributions in 4 species of bats: Myotis daubentonii, a laryngeal echolocating bat from the family Vespertilionidae, Rousettus aegyptiacus, a tongue clicking echolocating bat from the family Pteropodidae, and Pteropus alecto and P. poliocephalus, 2 non-echolocating bats (also from the Pteropodidae). We find that all 3 pteropodids have a similar number (≈200,000 cells) and distribution of RGCs and a similar maximum SRP (≈4 cycles/degree). M. daubentonii has fewer (∼6,000 cells) and sparser RGCs than the pteropodids and thus a significantly lower SRP (0.6 cycles/degree). M. daubentonii also differs in terms of the distribution of RGCs by having a unique dorsal area of specialization in the retina. Our findings are consistent with the existing literature and suggest that M. daubentonii likely only uses vision for orientation, while for pteropodids vision is also important for foraging.

Comparison of functional and anatomical estimations of visual acuity in two species of coral reef fish.

The high-contrast, complex patterns typical of many reef fish serve several purposes, including providing disruptive camouflage and a basis for vision-based communication. In trying to understand the role of a specific pattern, it is important to first assess the extent to which an observer can resolve the pattern, itself determined, at least in part, by the observer's visual acuity. Here, we studied the visual acuity of two species of reef fish - Pomacentrus amboinensis and Pseudochromis fuscus - using both anatomical and behavioural estimates. The two species share a common habitat but are members of different trophic levels (predator versus herbivore/omnivore) and perform different visual tasks. On the basis of the anatomical study, we estimated visual acuity to lie between 4.1 and 4.6 cycles deg-1 for P. amboinensis and 3.2 and 3.6 cycles deg-1 for P. fuscus Behavioural acuity estimates were considerably lower, ranging between 1.29 and 1.36 cycles deg-1 for P. amboinensis and 1.61 and 1.71 cycles deg-1 for P. fuscus Our results show that two species from the same habitat have only moderately divergent visual capabilities, despite differences in their general life histories. The difference between anatomical and behavioural estimates is an important finding as the majority of our current knowledge on the resolution capabilities of reef fish comes from anatomical measurements. Our findings suggest that anatomical estimates may represent the highest potential acuity of fish but are not indicative of actual performance, and that there is unlikely to be a simple scaling factor to link the two measures across all fish species.

Spatial resolving power and spectral sensitivity of the saltwater crocodile, Crocodylus porosus, and the freshwater crocodile, Crocodylus johnstoni.

Crocodilians are apex amphibious predators that occupy a range of tropical habitats. In this study, we examined whether their semi-aquatic lifestyle and ambush hunting mode are reflected in specific adaptations in the peripheral visual system. Design-based stereology and microspectrophotometry were used to assess spatial resolving power and spectral sensitivity of saltwater (Crocodylus porosus) and freshwater crocodiles (Crocodylus johnstoni). Both species possess a foveal streak that spans the naso-temporal axis and mediates high spatial acuity across the central visual field. The saltwater crocodile and freshwater crocodile have a peak spatial resolving power of 8.8 and 8.0 cycles deg(-1), respectively. Measurement of the outer segment dimensions and spectral absorbance revealed five distinct photoreceptor types consisting of three single cones, one twin cone and a rod. The three single cones (saltwater/freshwater crocodile) are violet (424/426 nm λmax), green (502/510 nm λmax) and red (546/554 nm λmax) sensitive, indicating the potential for trichromatic colour vision. The visual pigments of both members of the twin cones have the same λmax as the red-sensitive single cone and the rod has a λmax at 503/510 nm (saltwater/freshwater). The λmax values of all types of visual pigment occur at longer wavelengths in the freshwater crocodile compared with the saltwater crocodile. Given that there is a greater abundance of long wavelength light in freshwater compared with a saltwater environment, the photoreceptors would be more effective at detecting light in their respective habitats. This suggests that the visual systems of both species are adapted to the photic conditions of their respective ecological niche.

A formula for human retinal ganglion cell receptive field density as a function of visual field location.

In the human eye, all visual information must traverse the retinal ganglion cells. The most numerous subclass, the midget retinal ganglion cells, are believed to underlie spatial pattern vision. Thus the density of their receptive fields imposes a fundamental limit on the spatial resolution of human vision. This density varies across the retina, declining rapidly with distance from the fovea. Modeling spatial vision of extended or peripheral targets thus requires a quantitative description of midget cell density throughout the visual field. Through an analysis of published data on human retinal topography of cones and ganglion cells, as well as analysis of prior formulas, we have developed a new formula for midget retinal ganglion cell density as a function of position in the monocular or binocular visual field.

Morphological Plasticity of the Retina of Viperidae Snakes Is Associated With Ontogenetic Changes in Ecology and Behavior.

Snakes of the Viperidae family have retinas adapted to low light conditions, with high packaging of rod-photoreceptors containing the rhodopsin photopigment (RH1), and three types of cone-photoreceptors, large single and double cones with long-wavelength sensitive opsins (LWS), and small single cones with short-wavelength sensitive opsins (SWS1). In this study, we compared the density and distribution of photoreceptors and ganglion cell layer (GCL) cells in whole-mounted retinas of two viperid snakes, the lancehead Bothrops jararaca and the rattlesnake Crotalus durissus, and we estimated the upper limits of spatial resolving power based on anatomical data. The ground-dwelling C. durissus inhabits savannah-like habitats and actively searches for places to hide before using the sit-and-wait hunting strategy to ambush rodents. B. jararaca inhabits forested areas and has ontogenetic changes in ecology and behavior. Adults are terrestrial and use similar hunting strategies to those used by rattlesnakes to prey on rodents. Juveniles are semi-arboreal and use the sit-and-wait strategy and caudal luring to attract ectothermic prey. Our analyses showed that neuronal densities were similar for the two species, but their patterns of distribution were different between and within species. In adults and juveniles of C. durissus, cones were distributed in poorly defined visual streaks and rods were concentrated in the dorsal retina, indicating higher sensitivity in the lower visual field. In adults of B. jararaca, both cones and rods were distributed in poorly defined visual streaks, while in juveniles, rods were concentrated in the dorsal retina and cones in the ventral retina, enhancing sensitivity in the lower visual field and visual acuity in the upper field. The GCL cells had peak densities in the temporal retina of C. durissus and adults of B. jararaca, indicating higher acuity in the frontal field. In juveniles of B. jararaca, the peak density of GCL cells in the ventral retina indicates better acuity in the upper field. The estimated visual acuity varied from 2.3 to 2.8 cycles per degree. Our results showed interspecific differences and suggest ontogenetic plasticity of the retinal architecture associated with changes in the niche occupied by viperid snakes, and highlight the importance of the retinal topography for visual ecology and behavior of snakes.

Retinal topography and microhabitat diversity in a group of dragon lizards.

The well-studied phylogeny and ecology of dragon lizards and their range of visually mediated behaviors provide an opportunity to examine the factors that shape retinal organization. Dragon lizards consist of three evolutionarily stable groups based on their shelter type, including burrows, shrubs, and rocks. This allows us to test whether microhabitat changes are reflected in their retinal organization. We examined the retinae of three burrowing species (Ctenophorus pictus, C. gibba, and C. nuchalis), and three species that shelter in rock crevices (C. ornatus, C. decresii, and C. vadnappa). We used design-based stereology to sample both the photoreceptor array and neurons within the retinal ganglion cell layer to estimate areas specialized for acute vision. All species had two retinal specializations mediating enhanced spatial acuity: a fovea in the retinal center and a visual streak across the retinal equator. Furthermore, all species featured a dorsoventrally asymmetric photoreceptor distribution with higher photoreceptor densities in the ventral retina. This dorsoventral asymmetry may provide greater spatial summation of visual information in the dorsal visual field. Burrow-dwelling species had significantly larger eyes, higher total numbers of retinal cells, higher photoreceptor densities in the ventral retina, and higher spatial resolving power than rock-dwelling species. C. pictus, a secondary burrow-dwelling species, was the only species that changed burrow usage over evolutionary time, and its retinal organization revealed features more similar to rock-dwelling species than other burrow-dwelling species. This suggests that phylogeny may play a substantial role in shaping retinal organization in Ctenophorus species compared to microhabitat occupation.

Retinal topography in two species of flamingo (Phoenicopteriformes: Phoenicopteridae).

In this study, we assessed eye morphology and retinal topography in two flamingo species, the Caribbean flamingo (Phoenicopterus ruber) and the Chilean flamingo (P. chilensis). Eye morphology is similar in both species and cornea size relative to eye size (C:A ratio) is intermediate between those previously reported for diurnal and nocturnal birds. Using stereology and retinal whole mounts, we estimate that the total number of Nissl-stained neurons in the retinal ganglion cell (RGC) layer in the Caribbean and Chilean flamingo is ~1.70 and 1.38 million, respectively. Both species have a well-defined visual streak with a peak neuron density of between 13,000 and 16,000 cells mm-2 located in a small central area. Neurons in the high-density regions are smaller and more homogeneous compared to those in medium- and low-density regions. Peak anatomical spatial resolving power in both species is approximately 10-11 cycles/deg. En-face images of the fundus in live Caribbean flamingos acquired using spectral domain optical coherence tomography (SD-OCT) revealed a thin, dark band running nasotemporally just dorsal to the pecten, which aligned with the visual streak in the retinal topography maps. Cross-sectional images (B-scans) obtained with SD-OCT showed that this dark band corresponds with an area of retinal thickening compared to adjacent areas. Neither the retinal whole mounts, nor the SD-OCT imaging revealed any evidence of a central fovea in either species. Overall, we suggest that eye morphology and retinal topography in flamingos reflects their cathemeral activity pattern and the physical nature of the habitats in which they live.

How viewing objects with the dorsal or ventral retina affects colour-related behaviour in guppies (Poecilia reticulata).

Visual pigments can vary across the retina in many vertebrates, but the behavioural consequences of this retinal heterogeneity are unknown. Guppies (Poecilia reticulata) vary dorsoventrally in visual pigments and forage both on the ground and at the water surface, exposing different retinal regions to two very different visual environments. We tested guppy behaviour towards a moving stimulus presented below or above the guppy. We used 12 different narrow-band wavelength stimuli matching each of the opsin peak sensitivities presented either at the top or the bottom of our experimental apparatus. We analysed behaviours of 50 male and 50 female guppies over 4800 trials where a moving stimulus pattern was presented to each guppy. We found that wavelength, position and speed of the stimuli influenced male and female behaviour and seems to be mediated by the long wavelength sensitive photoreceptors. Males also had stronger behavioural responses than females whereas females performed more foraging-related pecking behaviour. Our results suggest that the spatial requirement of visual tasks and their ecological context are important and appear to be partly correlated with photoreceptor arrangement in the retina.

Unusual topographic specializations of retinal ganglion cell density and spatial resolution in a cliff-dwelling artiodactyl, the Nubian ibex (Capra nubiana).

The Nubian ibex (Capra nubiana) occurs in information-rich visual habitats including the edges of cliffs and escarpments. In addition to needing enhanced spatial resolution to find food and detect predators, enhanced visual sampling of the lower visual field would be advantageous for the control of locomotion in such precarious terrains. Using retinal wholemounts and stereology, we sought to measure how the ganglion cell density varies across the retina of the Nubian ibex to reveal which portions of its surroundings are sampled with high resolution. We estimated a total of ~1 million ganglion cells in the Nubian ibex retinal ganglion cell layer. Topographic variations of ganglion cell density reveal a temporal area, a horizontal streak, and a dorsotemporal extension, which are topographic retinal features also found in other artiodactyls. In contrast to savannah-dwelling artiodactyls, the horizontal streak of the Nubian ibex appears loosely organized possibly reflecting a reduced predation risk in mountainous habitats. Estimates of spatial resolving power (~17 cycles/degree) for the temporal area would be reasonable to facilitate foraging in the frontal visual field. Embedded in the dorsotemporal extension, we also found an unusual dorsotemporal area not yet reported in any other mammal. Given its location and spatial resolving power (~6 cycles/degree), this specialization enhances visual sampling toward the lower visual field, which would be advantageous for visually guided locomotion. This study expands our understanding of the retinal organization in artiodactyls and offers insights on the importance of vision for the Nubian ibex ecology.

Retinal dysfunction characterizes subtypes of dominant optic atrophy.

PURPOSE: To assess preganglionic retinal function using multifocal electroretinogram (mfERG) in patients affected by dominant optic atrophy (DOA) stratified by OPA1 gene mutation. METHODS: Multifocal electroretinogram (mfERG) was recorded in 18 DOA patients (DOA group, 35 eyes) and 25 age-matched healthy subjects (control group, 25 eyes). Patients were stratified in two groups based on gene mutation: missense mutation (DOA-M group, 11 eyes) and mutation causing haploinsufficiency (DOA-H group, 24 eyes). The mfERG N1-P1 response amplitude density (RAD) has been evaluated in five annular retinal areas with different eccentricity from the fovea (ring 1: 0-5 degrees, R1; ring 2: 5-10 degrees, R2; ring 3: 10-15 degrees, R3; ring 4: 15-20 degrees, R4; and ring 5: 20-25 degrees, R5) and in eight sectors on the basis of the retinal topography: temporal-superior (TS), temporal-inferior (TI), nasal-superior (NS) and nasal-inferior (NI), temporal (T), superior (S), nasal (N) and inferior (I). RESULTS: Compared to controls, DOA group revealed a significant reduction in N1-P1 RADs values in R1-R4 rings and in TI, NS and N sectors [analysis of variance (ANOVA), p < 0.01). DOA-M group showed a significant reduction in N1-P1 RADs values in R1-R5 rings and in TI, NS, NI, T, N and I sectors (p < 0.01). Dominant optic atrophy-H (DOA-H) group displayed only a significant (p < 0.01) reduction in N1-P1 RADs values, exclusively in R1 and in the NS sector. CONCLUSION: Preganglionic retinal impairment occurs in DOA with a clear genotype to retinal dysfunction association. Missense mutations are characterized by a far more severe functional impairment.

Anatomical Analysis of the Retinal Specializations to a Crypto-Benthic, Micro-Predatory Lifestyle in the Mediterranean Triplefin Blenny Tripterygion delaisi.

The 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 (SRP) of the eye of the Mediterranean triplefin Tripterygion delaisi. Retinal wholemounts were prepared to systematically and quantitatively analyze photoreceptor and retinal ganglion cell (RGC) densities using design-based stereology. To further examine the retinal structure, we also used magnetic resonance imaging (MRI) 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 RGCs per mm2. Based on photoreceptor spacing, SRP 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.

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 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 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.

Variations in retinal photoreceptor topography and the organization of the rod-free zone reflect behavioral diversity in Australian passerines.

The avian retina possesses one of the most diverse complements of photoreceptor types among vertebrates but little is known about their spatial distribution. Here we used retinal wholemounts and stereological methods to present the first complete maps of the topographic distribution of rods and cones in four species of Australian passerines with diverse trophic specializations. All species studied have one central and one temporal rod-free zone. In the insectivorous yellow-rumped thornbill, the central rod-free zone is unusually large, occupying ∼17% (56°) of the retinal area (angular subtense), whereas in nectarivorous and frugivorous species it represents only ∼0.1% (5-7°) to 0.3% (10°) of the retinal area (angular subtense). In contrast, the temporal rod-free zone varies little between species (∼0.02-0.4%; 2-10°). In all species, rods follow a pronounced dorsoventral gradient with highest densities in the ventral retina. The topographic distribution of cones is concentric and reveals a central fovea and a temporal area. In the yellow-rumped thornbill, cone densities form an extended plateau surrounding the fovea, beyond which densities fall rapidly towards the retinal periphery. For the other species, cone densities decline gradually along a foveal to peripheral gradient. Estimates of spatial resolving power calculated using cone peak densities are higher in the central fovea (19-41 cycles/degree) than in the temporal area (9-15 cycles/degree). In conclusion, we suggest that the unusual organization of the rod-free zone and the distinct topographic distribution of rods and cones correlate with specific ecological needs for enhanced visual sensitivity and spatial resolution in these birds.

Topographic specializations in the retinal ganglion cell layer correlate with lateralized visual behavior, ecology, and evolution in cockatoos.

Cockatoos are a unique avian group inhabiting a diversity of arboreal and terrestrial microhabitats. Most species display strong lateralized visual behaviors using their left eye/foot to assist with food manipulation during foraging. In this study, we used retinal wholemounts and stereological methods to investigate whether the topographic distribution of retinal ganglion cells in cockatoos reflects their lateralized behaviors and microhabitat diversity. We found that all species studied possess a horizontal visual streak and a shallow central fovea that afford increased spatial resolution in the lateral visual field. Arboreal cockatoos have a well-defined dorsotemporal area, in contrast to terrestrial cockatoos, in which this specialization is inconspicuous or absent. Terrestrial cockatoos also have a triangular extension of increased ganglion cell density directed toward the dorsotemporal retinal periphery. Both the dorsotemporal area and the triangular extension enhance spatial resolution in the frontal and inferior visual fields, which potentially assists with binocular coordination during foraging. We found significantly higher ganglion cell densities in the left (52,000-72,000 cells/mm2) compared with the right (42,500-50,000 cells/mm2) perifoveal region of species that have strong left eye-left foot lateralized behaviors. In contrast, cockatoo species that show no lateralized behaviors have equivalent retinal ganglion cell densities in both left and right perifoveal regions (42,500-52,500 cells/mm2). Retinal ganglion cell peak densities in the dorsotemporal area showed no significant difference between left and right eyes for any species, suggesting that cockatoos use both eyes to extract information in the binocular visual field, independent of the degree of lateralization.