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One hundred and fifty years ago Max Schultze first proposed the duplex theory of vision, that vertebrate eyes have two types of photoreceptor cells with differing sensitivity: rods for dim light and cones for bright light and colour detection. We now know that this division is fundamental not only to the photoreceptors themselves but to the whole of retinal and visual processing. But why are rods more sensitive, and how did the duplex retina first evolve? Cells resembling cones are very old, first appearing among cnidarians; the emergence of rods was a key step in the evolution of the vertebrate eye. Many transduction proteins have different isoforms in rods and cones, and others are expressed at different levels. Moreover rods and cones have a different anatomy, with only rods containing membranous discs enclosed by the plasma membrane. These differences must be responsible for the difference in absolute sensitivity, but which are essential? Recent research particularly expressing cone proteins in rods or changing the level of expression seem to show that many of the molecular differences in the activation and decay of the response may have each made a small contribution as evolution proceeded stepwise with incremental increases in sensitivity. Rod outer-segment discs were not essential and developed after single-photon detection. These experiments collectively provide a new understanding of the two kinds of photoreceptors and help to explain how gene duplication and the formation of rod-specific proteins produced the duplex retina, which has remained remarkably constant in physiology from amphibians to man.

Summary Vertebrate ancestors had only cone-like photoreceptors. The duplex retina evolved in jawless vertebrates with the advent of highly photosensitive rod-like photoreceptors. Despite cones being the arbiters of high-resolution color vision, rods emerged as the dominant photoreceptor in mammals during a nocturnal phase early in their evolution. We investigated the evolutionary and developmental origins of rods in two divergent vertebrate retinas. In mice, we discovered genetic and epigenetic vestiges of short-wavelength cones in developing rods, and cell-lineage tracing validated the genesis of rods from S cones. Curiously, rods did not derive from S cones in zebrafish. Our study illuminates several questions regarding the evolution of duplex retina and supports the hypothesis that, in mammals, the S-cone lineage was recruited via the Maf-family transcription factor NRL to augment rod photoreceptors. We propose that this developmental mechanism allowed the adaptive exploitation of scotopic niches during the nocturnal bottleneck early in mammalian evolution.

The spectral tuning properties of the whale shark (Rhincodon typus) rod (rhodopsin or Rh1) and long-wavelength-sensitive (LWS) cone visual pigments were examined to determine whether these retinal pigments have adapted to the broadband light spectrum available for surface foraging or to the narrowband blue-shifted light spectrum available at depth. Recently published whale shark genomes have identified orthologous genes for both the whale sharkRh1andLWScone opsins suggesting a duplex retina. Here, the whale shark Rh1 and LWS cone opsin sequences were examined to identify amino acid residues critical for spectral tuning. Surprisingly, the predicted absorbance maximum (λmax) for both the whale shark Rh1 and LWS visual pigments is near 500 nm. Although Rh1λmaxvalues near 500 nm are typical of terrestrial vertebrates, as well as surface foraging fish, it is uncommon for a vertebrate LWS cone pigment to be so greatly blue-shifted. We propose that the spectral tuning properties of both the whale shark Rh1 and LWS cone pigments are most likely adaptations to the broadband light spectrum available at the surface. Whale shark melanopsin (Opn4) deactivation kinetics was examined to better understand the underlying molecular mechanisms of the pupillary light reflex. Results show that the deactivation rate of whale shark Opn4 is similar to the Opn4 deactivation rate from vertebrates possessing duplex retinae and is significantly faster than the Opn4 deactivation rate from an aquatic rod monochromat lacking functional cone photoreceptors. The rapid deactivation rate of whale shark Opn4 is consistent with a functional cone class and would provide the animal with an exponential increase in the number of photons required for photoreceptor signaling when transitioning from photopic to scotopic light conditions, as is the case when diving.

S cones expressing the short wavelength-sensitive type 1 (SWS1) class of visual pigment generally form only a minority type of cone photoreceptor within the vertebrate duplex retina. Hence, their primary role is in color vision, not in high acuity vision. In mammals, S cones may be present as a constant fraction of the cones across the retina, may be restricted to certain regions of the retina or may form a gradient across the retina, and in some species, there is coexpression of SWS1 and the long wavelength-sensitive (LWS) class of pigment in many cones. During retinal development, SWS1 opsin expression generally precedes that of LWS opsin, and evidence from genetic studies indicates that the S cone pathway may be the default pathway for cone development. With the notable exception of the cartilaginous fishes, where S cones appear to be absent, they are present in representative species from all other vertebrate classes. S cone loss is not, however, uncommon; they are absent from most aquatic mammals and from some but not all nocturnal terrestrial species. The peak spectral sensitivity of S cones depends on the spectral characteristics of the pigment present. Evidence from the study of agnathans and teleost fishes indicates that the ancestral vertebrate SWS1 pigment was ultraviolet (UV) sensitive with a peak around 360 nm, but this has shifted into the violet region of the spectrum (>380 nm) on many separate occasions during vertebrate evolution. In all cases, the shift was generated by just one or a few replacements in tuning-relevant residues. Only in the avian lineage has tuning moved in the opposite direction, with the reinvention of UV-sensitive pigments.

Most vertebrates have a duplex retina comprising two photoreceptor types, rods for dim-light (scotopic) vision and cones for bright-light (photopic) and color vision. However, deep-sea fishes are only active in dim-light conditions; hence, most species have lost their cones in favor of a simplex retina composed exclusively of rods. Although the pearlsides, Maurolicus spp., have such a pure rod retina, their behavior is at odds with this simplex visual system. Contrary to other deep-sea fishes, pearlsides are mostly active during dusk and dawn close to the surface, where light levels are intermediate (twilight or mesopic) and require the use of both rod and cone photoreceptors. This study elucidates this paradox by demonstrating that the pearlside retina does not have rod photoreceptors only; instead, it is composed almost exclusively of transmuted cone photoreceptors. These transmuted cells combine the morphological characteristics of a rod photoreceptor with a cone opsin and a cone phototransduction cascade to form a unique photoreceptor type, a rod-like cone, specifically tuned to the light conditions of the pearlsides’ habitat (blue shifted light at mesopic intensities). Combining properties of both rods and cones into a single cell type, instead of using two photoreceptor types that do not function at their full potential under mesopic conditions, is likely to be the most efficient and economical solution to optimize visual performance. These results challenge the standing paradigm of the function and evolution of the vertebrate duplex retina and emphasize the need for a more comprehensive evaluation of visual systems in general., published version, peerReviewed

Unlike in mammals, persistent postembryonic retinal growth is a characteristic feature of fish, which includes major remodeling events that affect all cell types including photoreceptors. Consequently, visual capabilities change during development, where retinal sensitivity to different wavelengths of light (photopic vision), -and to limited photons (scotopic vision) are central capabilities for survival. Differently from well-established model fish, Atlantic cod has a prolonged larval stage where only cone photoreceptors are present. Rods do not appear until juvenile transition (metamorphosis), a hallmark of indirect developing species. Previously we showed that whole gene families of lws (red-sensitive) and sws1 (UV-sensitive) opsins have been lost in cod, while rh2a (green-sensitive) and sws2 (blue-sensitive) genes have tandem duplicated. Here, we provide a comprehensive characterization of a two-step developing duplex retina in Atlantic cod. The study focuses on cone subtype dynamics and delayed rod neurogenesis and differentiation in all cod life stages. Using transcriptomic and histological approaches we show that different opsins disappear in a topographic manner during development where central to peripheral retina is a key axis of expressional change. Early cone differentiation was initiated in dorso-temporal retina different from previously described in fish. Rods first appeared during initiation of metamorphosis and expression of the nuclear receptor transcription factor nr2e3-1, suggest involvement in rod specification. The indirect developmental strategy thus allows for separate studies of cones and rods development, which in nature correlates with visual changes linked to habitat shifts. The clustering of key retinal genes according to life stage, suggests that Atlantic cod with its sequenced genome may be an important resource for identification of underlying factors required for development and function of photopic and scotopic vision. publishedVersion

To interact with its visual environment, an organism needs to perceive objects in both space and time. High temporal resolution is hence important to the fitness of diurnally active animals, not least highly active aerial species such as birds. However, temporal resolution, as assessed by flicker fusion frequency (FFF; the stimulus frequency at which a flickering light stimulus can no longer be resolved and appears continuous) or critical flicker fusion frequency (CFF; the highest flicker fusion frequency at any light intensity) has rarely been assessed in birds. In order to further our understanding of temporal resolution as a function of light intensity in birds we used behavioural experiments with domestic chickens (Gallus gallus domesticus) from an old game breed 'Gammalsvensk dvärghöna' (which is morphologically and behaviourally similar to the wildtype ancestor, the red jungle fowl, G. gallus), to generate an 'Intensity/FFF curve' (I/FFF curve) across full spectrum light intensities ranging from 0.2 to 2812 cd m⁻². The I/FFF curve is double-branched, resembling that of other chordates with a duplex retina of both rods and cones. Assuming that the branches represent rod and cone mediated responses respectively, the break point between them places the transition between scotopic and photopic vision at between 0.8 and 1.9 cd m⁻². Average FFF ranged from 19.8 Hz at the lowest light intensity to a CFF 87.0 Hz at 1375 cd m⁻². FFF dropped slightly at the highest light intensity. There was some individual variation with certain birds displaying CFFs of 90-100 Hz. The FFF values demonstrated by this non-selected breed appear to be considerably higher than other behaviourally derived FFF values for similar stimuli reported for white and brown commercial laying hens, indicating that the domestication process might have influenced temporal resolution in chicken.

The neutrally buoyant Antarctic fishes of the sister taxa Dissostichus (D. eleginoides and D. maw- soni) and Pleuragramma antarcticum diverged early in the notothenioid radiation and filled different niches in the pelagic realm of the developing Southern Ocean. To assess the influence of phylogenetic and ecological factors in shaping neural morphology in these taxa, we studied the anatomy and histology of the brains and ret- inae, and determined the proportional weights of brain regions. With the brain of the non-Antarctic sister taxon Eleginops maclovinus as plesiomorphic, statistically sig- nificant departures in the brains of the two Antarctic taxa include reduction of the corpus cerebelli and expan- sion of the mesencephalon and medulla. Compared to Ele- ginops, both species also have a relatively smaller telencephalon, although this is significant only in Dissostichus. There are a number of apomorphic features in the brain of Pleuragramma including reduced olfactory nerves and bulbs, an extremely small corpus cerebelli and an expanded mesencephalon. Although there is not a sig- nificant difference in the relative weights of the medulla in the two taxa, the prominence of the eminentia granularis and bulging cap-like appearance of the crista cerebellaris are distinctive in Pleuragramma. Brain histology of Dis- sostichus and Pleuragramma reflects typical perciform patterns and the two species of Dissostichus are histologi- cally identical. Lateral compression in Pleuragramma and notable lobation in Dissostichus also contribute to differen- ces between the taxa. Compression in Pleuragramma is at- tributable to convergence on an anchovy/herring body shape and to the relatively large brain in this small fish. The less prominent pattern of lobation of the telencepha- lon, inferior lobes and corpus cerebelli in Pleuragramma probably reflects underlying histology, specifically a reduc- tion in cellularity of the neuropil in the nuclei and lobes. The retinal histology of Dissostichus and Pleuragramma encompasses the extremes seen in Antarctic notothenioids. Dissostichus has a thin scotopic retina with few cones and a high degree of summation. The retina of Pleuragramma is thick and cellular with many small single cones and rods and resembles that of Eleginops. Pedomorphy has not influenced brain morphology in these species but Pleura- gramma has superficial neuromasts that are pedomorphic. Although Dissostichus and Pleuragramma are sympatric in the water column, their brains and retinae are highly divergent and reflect the influences of both phylogeny and ecological partitioning of the pelagic realm. Compared to Eleginops, the relatively smaller corpus cerebelli but rela- tively larger medulla probably indicates, respectively, reduced activity levels of notothenioids in subzero tem- peratures and expansion of the mechanosensory lateral line system as a supplement to vision under conditions of reduced light. Compared to Dissostichus, Pleura- gramma has reduced olfactory bulbs and corpus cere- belli and an expanded mesencephalon. The reduction of the corpus to a small round knob is consistent with physiological parameters and video observations sug- gesting that, although pelagic, it is relatively inactive. Because mesencephalic weights also include the valvula cerebelli, the relatively large value for Pleuragramma may be attributable to its role in integration and senso- rimotor coordination of information from the highly cellular duplex retina and to integration of signals from the well- developed octavolateralis system. The brain of Dissostichus displays considerable persistent morphology in its overall resemblance to that of Eleginops, especially the large olfac- tory bulbs and the relatively large caudally projecting cor- pus, and Dissostichus exhibits olfactory tracking ability and migratory behavior in common with Eleginops .J. Mor- phol. 272:419-441, 2011. 2011 Wiley-Liss, Inc.

Photoreceptors in metazoans can be grouped into two classes, with their photoreceptive membrane derived either from cilia or microvilli. Both classes use some form of the visual pigment protein opsin, which together with 11-cis retinaldehyde absorbs light and activates a G-protein cascade, resulting in the opening or closing of ion channels. Considerable attention has recently been given to the molecular evolution of the opsins and other photoreceptor proteins; much is also known about transduction in the various photoreceptor types. Here we combine this knowledge in an attempt to understand why certain photoreceptors might have conferred particular selective advantages during evolution. We suggest that microvillar photoreceptors became predominant in most invertebrate species because of their single-photon sensitivity, high temporal resolution, and large dynamic range, and that rods and a duplex retina provided primitive chordates and vertebrates with similar sensitivity and dynamic range, but with a smaller expenditure of ATP.

The biologist Gordon Walls proposed his "transmutation" theory through the 1930s and the 1940s to explain cone-like morphology of rods (and vice versa) in the duplex retinas of modern-day reptiles, with snakes regarded as the epitome of his hypothesis. Despite Walls' interest, the visual system of reptiles, and in particular snakes, has been widely neglected in favor of studies of fishes and mammals. By analyzing the visual pigments of two henophidian snakes, Xenopeltis unicolor and Python regius, we show that both species express two cone opsins, an ultraviolet-sensitive short-wavelength-sensitive 1 (SWS1) (lambda(max) = 361 nm) pigment and a long-wavelength-sensitive (LWS) (lambda(max) = 550 nm) pigment, providing the potential for dichromatic color vision. They also possess rod photoreceptors which express the usual rod opsin (Rh1) pigment with a lambda(max) at 497 nm. This is the first molecular study of the visual pigments expressed in the photoreceptors of any snake species. The presence of a duplex retina and the characterization of LWS, SWS1, and Rh1 visual pigments in henophidian snakes implies that "lower" snakes do not provide support for Walls' transmutation theory, unlike some "higher" (caenophidian) snakes and other reptiles, such as geckos. More data from other snake lineages will be required to test this hypothesis further.

During their complex life history, anguilliform eels go through a major metamorphosis when developing from a fresh water yellow eel into a deep-sea silver eel. In addition to major changes in body morphology, the visual system also adapts from a fresh water teleost duplex retina with rods and cones, to a specialized deep-sea retina containing only rods. The history of the rods is well documented with an initial switch from a porphyropsin to a rhodopsin (P5232to P5011) and then a total change in gene expression with the down regulation of a “freshwater” opsin and its concomitant replacement by the expression of a typical “deep-sea” opsin (P5011to P4821). Yellow eels possess only two spectral classes of single cones, one sensitive in the green presumably expressing an RH2 opsin gene and the second sensitive in the blue expressing an SWS2 opsin gene. In immature glass eels, entering into rivers from the sea, the cones contain mixtures of rhodopsins and porphyropsins, whereas the fully freshwater yellow eels have cone pigments that are almost pure porphyropsins with peak sensitivities at about 540–545 nm and 435–440 nm, respectively. However, during the early stages of metamorphosis, the pigments switch to rhodopsins with the maximum sensitivity of the “green”-sensitive cone shifting to about 525 nm, somewhat paralleling, but preceding the change in rods. During metamorphosis, the cones are almost completely lost.

The visual processing of humans is primarily reliant upon the sensitivity of cone photoreceptors to light during daylight conditions. This underscores the importance of understanding how cone photoreceptors maintain the ability to detect light. The vertebrate retina consists of a combination of both rod and cone photoreceptors. Subsequent to light exposure, both rod and cone photoreceptors are dependent upon the recycling of vitamin A to regenerate photopigments, the proteins responsible for detecting light. Metabolic processing of vitamin A in support of rod photopigment renewal, the so-called “rod visual cycle”, is well established. However, the metabolic processing of vitamin A in support of cone photopigment renewal remains a challenge for characterization in the recently discovered “cone visual cycle”. In this review we summarize the research that has defined the rod visual cycle and our current concept of the novel cone visual cycle. Here, we highlight the research that supports the existence of a functional cone-specific visual cycle: the identification of novel enzymatic activities that contribute to retinoid recycling, the observation of vitamin A recycling in cone-dominated retinas, and the localization of some of these activities to the Müller cell. In the opinions of the authors, additional research on the possible interactions between these two visual cycles in the duplex retina is needed to understand visual detection in the human retina.

8 pages, 8 figures, A unique retinal topography was found in the rufus snake eel, Ophichthus rufus, a burrowing fish that shows a preference for nocturnal habits. The cells in the ganglion-cell layer formed a high-density semicircular band that covered the dorso-rostral, temporal and ventro- rostral areas of the retina. Three regions of high acuity were identified in the ventro-temporal, ventrorostral and dorsal regions of the retina. This is the first time that multiple specialisations have been found in a benthic deep-water fish. The ventro-temporal and ventro- rostral visual axes were found at 48 and 54 from the retinal centre, subtending the dorsal field of view, while the dorsal axis was at 66 , subtending the ventral field of view. These characteristics may represent an adaptation to identify the mouth of the muddy burrows in which this species hides or where it looks for food. O. rufus has a duplex retina with numerous slender rod photoreceptors arranged in banks of four layers. This morphology is typical of deep-sea teleosts with a high visual sensitivity, which is useful in a dim-light environment. A few tiny cones were also present, probably enhancing acuity during the eel’s daily activity. The retina of O. rufus also possessed a well developed vascularisation, possibly to overcome the hypoxic conditions that may be found in the burrow. The characteristics of the retina of the rufus snake eel indicate singular visual capabilities that are discussed in relation to the burrowing life-style and to what is known of feeding habits of this fish, The author is especially grateful to M. Rufino and to L. Gil de Sola for providing the material during the MEDITS 2000 cruise, and to S. Lluch for helping in the retinal blood-vessel identification. The technicians of the Unidad Te´cnica de Microscopı´a Electro´ nica of the Barcelona University kindly prepared and processed the samples for the transmission electron microscope. The photographs of Fig. 1 belong to the UE project DGXIV-no. 96-063. Dr. R. Villanueva greatly improved the manuscript with his accurate criticism. Finally, the author would like to thank Dr. Rodgers for kindly reviewing the final English version, and two anonymous reviewers for their valuable comments on the manuscript. All the experiments comply with the current law (5/1995) of Spain

In the present EM study, we investigate the retina of Belone belone, a visually-orientated marine predator living close to the water surface. In the duplex retina, four morphologically different cone types are observed: unequal and equal double cones, long single cones and triple cones. In the light-adapted state, five different cone patterns occur: row, twisted row, square, pentagonal and hexagonal patterns. High double cone densities are found ventro-nasally, ventro-temporally and dorso-temporally. Throughout the retina the double cone/single cone ratio is 2 : 1, in the ventral part, however, a 1 : 1 ratio occurs. In the vitreous body we found a curtain-like intraocular septum dividing the retina into two morphologically different regions. In most areas of the dark-adapted retina the cone patterns are absent at the ellipsoid level, with long single cones standing more vitreally in the light path than double cones. The mosaics are retained, however, in the outer nuclear layer. Typical dark adaptation, i.e. the retinomotor movements of the retinal pigment epithelium and photoreceptors in response to the dark adaptation (light change) is not present in the peripheral ventral and parts of the central ventral area. In both regions we found a twisted row pattern of cones having a vitreal position. The findings are discussed with respect to the photic habitat and feeding habits of this species.

Photoreceptors in animals are generally of two kinds: the ciliary or c-type and the rhabdomeric or r-type. Although ciliary photoreceptors are found in many phyla, vertebrates seem to be unique in having two distinct kinds which together span the entire range of vision, from single photons to bright light. We ask why the principal photoreceptors of vertebrates are ciliary and not rhabdomeric, and how rods evolved from less sensitive cone-like photoreceptors to produce our duplex retina. We suggest that the principal advantage of vertebrate ciliary receptors is that they use less ATP than rhabdomeric photoreceptors. This difference may have provided sufficient selection pressure for the development of a completely ciliary eye. Although many of the details of rod evolution are still uncertain, present evidence indicates that (i) rods evolved very early before the split between the jawed and jawless vertebrates, (ii) outer-segment discs make no contribution to rod sensitivity but may have evolved to increase the efficiency of protein renewal, and (iii) evolution of the rod was incremental and multifaceted, produced by the formation of several novel protein isoforms and by changes in protein expression, with no one alteration having more than a few-fold effect on transduction activation or inactivation. This article is part of the themed issue ‘Vision in dim light’.

© 2015 Elsevier Ltd All rights reserved. Most vertebrates have a duplex retina containing rods for dim light vision and cones for bright lights and color detection. Photoreceptors like cones are present in many invertebrate phyla as well as in chordata, and rods evolved from cones [1, 2], but the sequence of events is not well understood. Since duplex retinas are present in both agnatha and gnathostomata, which diverged more than 400 million years ago, some properties of ancestral rods may be inferred from a comparison of cells in these two groups. Lamprey have two kinds of photoreceptors, called "short" and "long" [3-9], which seem to be rods and cones; however, the outer segments of both have an identical cone-like morphology of stacks of lamellae without a continuous surrounding plasma membrane [3, 4, 6, 7]. This observation and other aspects of the cellular and molecular biology of the photoreceptors have convinced several investigators [2, 10-12] that "the features of 'true' rod transduction in jawed vertebrates, which permit the reliable detection of single photons of light, evolved after the separation of gnathostomes from lampreys" [12]. To test this hypothesis, we recorded from photoreceptors of the sea lamprey Petromyzon marinus and show that their rods have a single-photon sensitivity similar to that of rods in other vertebrates. Thus, photoreceptors with many of the features of rods emerged before the split between agnatha and gnathostomata, and a rod-like outer segment with cytosolic disks surrounded by a plasma membrane is not necessary for high-sensitivity visual detection.

Morphology of the photoreceptor cells and tapetum of the Japanese anchovy Engraulis japonicus was studied by histologically and by chemical analysis. The Japanese anchovy has a duplex retina. The cones form parallel rows consisting of alternately placed long cones and bifid cones. Both types of cones are intimately associated and form triple units that are regularly spaced along the row of cones. The rods are grouped and stacked. This fish has a retinal tapetum lucidum composed of guanine and hypoxanthine. Three structures of the tapetum lucidum were recognized: platelet, diamond and rod types. Photomechanical changes include movements of the photoreceptor cells and the retinal tapetum. The retina of the Japanese anchovy is thought to be highly sensitive and well adapted to a dim light environment.

SummaryTo maintain resting potentials in darkness, rod and cone photoreceptors incur a significant energy cost. But in brighter light, rods become energetically ‘cheaper’ than cones, which might explain the evolution of the vertebrate duplex retina.

Catadromous fishes migrate between ocean and freshwater during particular phases of their life cycle. The dramatic environmental changes shape their physiological features, e.g. visual sensitivity, olfactory ability, and salinity tolerance. Anguilla marmorata, a catadromous eel, migrates upstream on dark nights, following the lunar cycle. Such behavior may be correlated with ontogenetic changes in sensory systems. Therefore, this study was designed to identify changes in spectral sensitivity and opsin gene expression of A. marmorata during upstream migration. Microspectrophotometry analysis revealed that the tropical eel possesses a duplex retina with rod and cone photoreceptors. The λmax of rod cells are 493, 489, and 489 nm in glass, yellow, and wild eels, while those of cone cells are 508, and 517 nm in yellow, and wild eels, respectively. Unlike European and American eels, Asian eels exhibited a blue-shifted pattern of rod photoreceptors during upstream migration. Quantitative gene expression analyses of four cloned opsin genes (Rh1f, Rh1d, Rh2, and SWS2) revealed that Rh1f expression is dominant at all three stages, while Rh1d is expressed only in older yellow eel. Furthermore, sequence comparison and protein modeling studies implied that a blue shift in Rh1d opsin may be induced by two known (N83, S292) and four putative (S124, V189, V286, I290) tuning sites adjacent to the retinal binding sites. Finally, expression of blue-shifted Rh1d opsin resulted in a spectral shift in rod photoreceptors. Our observations indicate that the giant mottled eel is color-blind, and its blue-shifted scotopic vision may influence its upstream migration behavior and habitat choice.

The eye of Rhinomugil corsula has a duplex retina differentiated into dorsal and ventral halves, with the ventral retina 116·4 μm thicker than the dorsal retina. The rods of the ventral retina are relatively longer, with longer outer segments. The nuclei of the outer nuclear layer of the dorsal and ventral halves are in four and six to seven rows respectively. The rod outer segment bears a single incision. The mitochondria of cone and rod inner segments has a vitreal-scleral gradient. Single and double cones are present in both halves, with triple cones in the dorsal half only. The outer segments of double cones are equal and united. The single cones have two connecting cilia. The cone cells are arranged in a square mosaic with four double cones and five single cones to each unit in the dorsal half, and in a rhombic pattern in the ventral half.

Differentiation of visual cells inBufo melanostictus begins after hatching at gill bud stage. It is indicated by emergence of cytoplasmic buds from the outer nuclear layer of the retina. Each bud contains an apically located vacuole which soon disappears from all cells. Cones and rods start differentiating simultaneously but the majority of early cells are rods. Single cones, red rods and double cones can be identified by the stage when the operculum is formed. Up to the beginning of hindlimb morphogenesis rods remain the most numerous but later single cones attain approximate numerical equality with rods and the tadpole retina becomes a truly duplex retina. Red rods of tadpoles are structurally different from those of adult. As in the accessory members of double cones a paraboloid develops in the myoid region of the inner segment of red rods also and persists throughout larval life. During metamorphosis green rods appear, cone outer segments become sharply pointed, myoid develops in the red rods replacing the paraboloid which disappears along with its glycogen but there is no change in the double cones. After metamorphosis number and size of red rods increase greatly transforming the duplex retina of the tadpole into a predominantly rod retina adapted for scoptopic vision of the nocturnal adult.

Ontogenetic changes in the visual cell layer of the duplex retina during growth of the eye of the deep-sea teleost Gempylus serpens, the snake mackerel, are illustrated by comparing the retina of a small specimen with that of a previously studied adult fish. The small specimen has tightly packed cones spanning the whole width of the visual cell layer and small rods situated in its vitread part. Over most of the retina the cone population consists of single cones arranged in a very regular hexagonal mosaic. The temporalmost retina has a cone population consisting mainly of twin cones arranged in meridional rows. Growth of the eye is associated with an increase in the thickness of the visual cell layer and the density of rods and a total elimination of the densely packed single cones, the retina of the adult fish possessing only a temporally located population of double cones. The radical differences between the retina of the small and adult snake mackerel are probably associated with the different light regimes encountered by small and large specimens.

Retinal whole-mount preparations from the eyes of the North American paddlefish, Polyodon spathula, were examined with a combination of bright field and differential interference contrast microscopy. The entire retina was mapped and population counts of rod and cone photoreceptors were made at regular intervals throughout the retina. The retina is dominated by rods, but a significant percentage (ca. 38%) of the photoreceptors are cones. Mean cone packing density for the entire retina is 6,402±1,216 cones/mm2. There is a small (16%) but statistically significant difference between cone packing density in the dorsal retina (6,674±1,168 cones/mm2) and the ventral retina (5,745±1,076 cones/mm2). There is no region of unusually high cone concentration that might be construed as a fovea or a visual streak. Mean rod packing density for the entire retina is 10,271±1,205 rods/mm2. Except in the far periphery, where rods are less numerous, the density of rods is fairly uniform throughout the retina. The data are discussed with regard to paddlefish habitat and behavior. J. Exp. Zool. 301A:674–681, 2004. © 2004 Wiley-Liss, Inc.

With the exception of the stellate sturgeon, which has only cones, all acipenseriform species studied have a duplex retina. The retina is dominated by rods, but about 20% of the photoreceptors are cones. The rods are structurally similar to those of vertebrates in general. Most rods have outer segments that are broad and long, but at least one species has a very rare, very slender rod as well. Cones are also typical in structure, and they too are rather robust. With one exception, the inner segment of each cone houses a colorless oil droplet, the function of which is unknown. Packing density of both rods and cones is relatively low, indicating that both scotopic and photopic acuity is less than that of other nocturnal creatures. The visual pigment in the rods of all species studied has a peak absorbance near 540 nm. All species studied have multiple cone pigments and, therefore, the photoreceptor basis for wavelength discrimination. However, one cannot yet say whether or not any sturgeon or paddlefish has color vision. All visual pigments are based on the vitamin A2 chromophore, and there is no evidence that there is a shift to the vitamin A 1 chromophore with change of habitat or with age. At least one species does change its cone pigment complement with age. Larval white sturgeon up to 10 weeks of age have only green-sensitive cones; after 10 weeks, blue-sensitive and red-sensitive cones are also present.

In the duplex retina of the catfish Clarias batrachus(Linnaeus, 1758), the apical processes of the pigment epithelial cells have been found by transmission electron microscopy to be in intimate contact with the calycal processes around the basal portion of the photoreceptor outer segments. It is hypothesized that the retinal pigment epithelium effectively transports synthesized products and metabolites to the photoreceptor inner segments via the anatomical zone of the apical–calycal processes interface in this species.

The retina of the catfish Clarias butrachus (L.), supposed to possess an all-rod retina, is found on re-investigation to contain both rods and cones. The retina is characterized by a prominent tapetum and multiple optic papillae.

1. Detection thresholds for two-dimensional Gabor functions of varying spatial and temporal frequency were used to investigate the post-receptoral sensitivity across the retina of the typical and complete achromat. 2. Under photopic conditions there is no evidence for post-receptoral cone function at any retinal eccentricity investigated. Sensitivity saturates in a way consistent with known psychophysical and electrophysiological measures of rod saturation. This occurs in a unitary fashion across the retina. 3. Under scotopic conditions the regional fall-off in spatio-temporal sensitivity is similar for the achromat and duplex retina. This suggests that the rods in the achromat make normal neural connections. 4. Taken together this supports the contention that the typical and complete achromat is a functional rod monochromat and hence can be used to explore the sensitivity of the isolated rod post-receptoral mechanism under mesopic conditions where its sensitivity is optimal. This is where its contribution is most difficult to isolate in the duplex retina. 5. For the human rod mechanism, mesopic post-receptoral sensitivity for all spatio-temporal stimuli is optimal in the central region of the retina and falls off as a function of eccentricity. 6. For localized stimuli, peripheral spatial sensitivity is reduced evenly at all spatial frequencies compared with that of the central retina. A similar displacement of the spatial sensitivity function of the rod mechanism occurs as illuminance is reduced. 7. For localized stimuli, temporal acuity of the rod mechanism is around 20-25 Hz irrespective of retinal position. As the illuminance is further lowered dynamics of the rod pathway are reduced irrespective of retinal position and the sensitivity function maintains a bandpass shape. 8. The regional distribution sensitivity of the rod mechanism changes as illuminance is reduced from mesopic to scotopic levels.

The eye of the deep-sea teleost Lestidiops affinis has been examined primarily by light microscopy and found to possess a duplex retina consisting of two main divisions, a pure-cone and a pure-rod region, with a narrow zone of transition, possessing both cones and rods, joining the two. The pure-cone region is located in the temporal (caudal) part of the retina subserving binocular vision in the rostral direction. It has an area temporalis retinae with particularly long and densely packed single cones arranged in a regular hexagonal mosaic. Joined (double or twin) cones have not been recognized with certainty in the pure-cone region. The pure-rod region, comprising the larger part of the retina, contains rods grouped in bundles separated by retinal pigment epithelium (RPE) processes with pigmented cores. The synaptic endings of the rods are arranged in separate clusters in the outer plexiform layer, there being apparently a separate rod pedicle cluster beneath (vitread to) each rod bundle. Structural comparisons with certain other deep-sea teleosts suggest the likely presence of a retinal tapetum in L. affinis, i.e. each single cone or rod bundle is situated in a reflecting pit formed by the RPE, with a discrete reflector apposed to the tip of each cone outer segment and the tips of the outer segments of each square-cut rod bundle.

Retinal structure was examined in 50-mm long leptocephalus larvae and in glass eel to elver juvenile stages. Larvae were found to have a single rodlike photoreceptor, while all postmetamorphic stages displayed a duplex retina. Retinal cell densities or ratios were not found to change with ontogeny in juveniles. Maintenance of juveniles in constant light or constant darkness resulted in a significant increase in numbers of rods and a decrease in numbers of inner nuclear layer cells, respectively. Retinomotor responses were present in all juvenile eels examined. The functional significance of retinal structure is discussed in relation to the different habitats occupied by successive life-history stages.

The absolute scotopic limen for light intensity was measured for three 10-mo-old female coyotes. The methodology was similar to that used by Blough in determining psychophysical thresholds in pigeons. Three coyotes were operantly conditioned to depress one of two foot treadles, left or right, depending on the condition of the stimulus light. Scotopic adaptation curves for each coyote were generated. Nonlinear regression curves were then fitted to the raw data. The mean scotopic thresholds did not differ significantly. However, time to the curves' asymptotes did differ significantly for one of the coyotes. The adaptation curves showed a distinct rod-cone "break," and retinal histology confirmed that the coyote has a duplex retina with a preponderance of rods. In addition, electroretinographic analysis showed the relative contributions of rods and cones at various light intensities and indicated a rod-cone break at approximately 15 min. Scotopic spectral sensitivity curves were also generated. The coyotes' scotopic visual threshold is exceeded by the natural illumination available under many nocturnal conditions. The results are discussed in relation to the ecology of the species.

The specific aims of this study were to examine age differences in visual acuity among young adult (5 years), middle aged (12 years) and aged (22 years) rhesus monkeys in relation to foveal cone density in the diurnal duplex retina. Classically, acuity has been defined as the reciprocal of the least resolvable detail measured in minutes of visual angle. The minimum separable binocular acuity mean of the young adult group was 0.83 ± 0.11, middle age acuity mean was 0.86 ± 0.12, and the acuity mean of the aged monkeys was 2.0 – 0.70 minutes of visual angle. According to analysis of variance and multiple range tests for specific group means, the 0.83' acuity m mean of the young, and the 0.86' acuity mean of the middle age group did not differ significantly, whereas the 2.0' acuity mean of the old group differed significantly from the 2 younger age groups. Foveal cone density was determined morphometrically by assesmeent of cone inner segment width, and absolute cone inner segment number per 100 Am along the horizontal meridian of the pure cone, rod free 1° × 1° foveola. Foveal cone density decreased significantly from 44.16 per 100 Am in the middle age group to 39.00 per 100 Am in the old macaque group. Since the diurnal macaque is of the same taxonomic order as man, and the visual systems of the two species are directly comparable in terms of ac acuity and the central receptive field organization of the retino-geniculo-striate system, it may be concluded that the macaque may represent an attractive and valid model for studies of aging in photopic and scotopic vision of diurnal primates, including man.

A pure-cone retina has been reported in the larval stages of teleosts from three families, viz. the salmonOncorhynchusspp. by Ali (1959), the herringClupea harengusby Blaxter & Jones (1967) and plaicePleuronectes platessaby Blaxter (1968 a). There is also an absence of any retinomotor responses (movement of retinal masking pigment and changes in the relative positions of the visual cells) until the rods develop, which is usually at metamorphosis where this is clear-cut. Most adult teleosts are known to have a duplex retina.

1. When there is projected on the retina (man, monocularly) the shadow of a grid which forms a visual field in several distinct pieces (not including the fovea in the present tests), the ordinary properties of the flicker recognition contour (F vs. log I) as a function of the light-time cycle fraction (tL) can be markedly disturbed. In the present experiments flicker was produced by the rotation of a cylinder with opaque vertical stripes. In the absence of such a grid shadow the "cone" segments of the contours form a set in which Fmax. and the abscissa of inflection are opposite but rectilinear functions of tL, while the third parameter of the probability integral (σ'log I) remains constant. This is the case also with diverse other animals tested. In the data with the grid, however, analysis shows that even for low values of tL (up to 0.50) there occurs an enhancement of the production of elements of neural effect, so that Fmax. rises rather than falls as ordinarily with increase of tL, although σ'log I stays constant and hence the total number of acting units is presumed not to change. This constitutes valid evidence for neural integration of effects due to the illumination of separated retinal patches. Beginning at tL = 0.75, and at 0.90, the slope of the "cone" curve is sharply increased, and the maximum F is far above its position in the absence of the grid. The decrease of σ'log I (the slope constant) signifies, in terms of other information, an increase in the number of acting cone units. The abscissa of inflection is also much lowered, relatively, whereas without the grid it increases as tL is made larger. These effects correspond subjectively to the fact that at the end-point flicker is most pronounced, on the "cone" curve, along the edges of the grid shadow where contrast is particularly evident with the longer light-times. The "rod" portion of the F - log I contour is not specifically affected by the presence of the grid shadow. Its form is obtainable at tL = 0.90 free from the influence of summating "cone" contributions, because then almost no overlapping occurs. Analysis shows that when overlapping does occur a certain number of rod units are inhibited by concurrent cone excitation, and that the mean contribution of elements of neural action from each of the non-inhibited units is also reduced to an extent depending on the degree of overlap. The isolated "rod" curve at tL = 0.90 is quite accurately in the form of a probability integral. The data thus give a new experimental proof of the occurrence of two distinct but interlocking populations of visual effects, and experimentally justify the analytical procedures which have been used to separate them. 2. The changing form of the F - log I contour as a function of tL, produced in man when the illuminated field is divided into parts by a shadow pattern, is normally found with the bird Taeniopygia castenotis (Gould), the zebra finch. The retina has elements of one general structural type (cones), and the F - log I contour is a simplex symmetrical probability integral. The eye of this bird has a large, complex, and darkly pigmented pecten, which casts a foliated shadow on the retina. The change in form of the F - log I curve occurs with tL above 0,50, and at tL = 0.90 is quite extreme. It is more pronounced than the one that is secured in the human data with the particular grid we have used, but there is no doubt that it could be mimicked completely by the use of other grids. The increase of flicker acuity due to the pecten shadow is considerable, when the dark spaces are brief relative to the light. The evidence thus confirms the suggestion (Menner) drawn from comparative natural history that the visual significance of the avian pecten might be to increase the sensory effect of small moving images. It is theoretically important that (as in the human experiment) this may be brought about by an actual decrease of effective retinal area illuminated. It is also significant theoretically that despite the presence of shadows of pecten or of grid, and of the sensory influences thus introduced, the probability integral formulation remains effective.

Electrical responses from the skate retina will only follow flicker up to frequencies of 5 hertz when intensities are below rod saturation. At greater luminances, the eye responds to rates as high as 30 hertz. As a result, a plot of critical flicker fusion as a function of intensity is a double branched curve. It seems that prolonged stimulation of skate rods, at high intensities, permits them to change their temporal response characteristics so that they follow high frequencies much as cones do in the duplex retina.

The electroretinographic (ERG) responses to single light flashes and to flickering lights were obtained in the tawny owl (Strix aluco). The waveform of the single-flash responses indicated that the owl possesses a duplex retina. Spectral sensitivity was determined with light flickering at a 6 and 25 Hz. The sensitivity curve obtained from the 6-Hz responses has a broad maximum between 500 and 525 nm. The 25-Hz sensitivity curve is narrow with a peak at about 600 nm. The sensitivity curves are compared with behaviorally measured sensitivity curves of the pigeon. A close agreement is found between 25-Hz curve and the pigeon red modulator.

The presence of cones in potto's retina has been proved beyond doubt although they are very restricted in number (1 cone for 300 rods). Morphologically speaking there is no point in calling these cones “rudimentary” except for their slender outer segment. There are red sensitive elements in that retina at wavelengths beyond the spectral sensitivity of visual purple and it is tempting to assume that these elements are cones. The ERG evoked from these elements by red light differs from that in response to white and blue light. They dark-adapt faster than the receptors sensitive to blue and white flashes. However in some of their properties, for example fusion frequency, these cones behave like rods in other species. As these few cones seem to activate the bipolar cells nearly as effectively as the numerous rods, it is suggested that these cones may be responsible for day vision in the potto.

Since the foveal photoreceptors in the duplex retina of adult human and other diurnal primates are closely associated with high visual acuity and spectral sensitivity, observations were made on the pre- and postnatal morphologic development of the macula and fovea in the retina of the diurnal rhesus monkey. Histologic findings on the level of development of the retina at birth revealed a macula with the characteristic foveal depression. Observations on the ultrastructural development of the foveal photoreceptors revealed that their outer and inner segments were relatively well differentiated even at birth. An examination of the prenatal morphogenesis of the photoreceptors in the eye of the fetus indicated that the initial differentiation of the receptors may take place as early as 100 to 125 days after conception. However, the receptors in the specialized fovea continued to develop for 1 to 2 months after birth, whereas the photoreceptors outside the central region of the retina had completed their fine structural development at birth. By the end of the second month after birth, the macular and foveal areas essential for high visual acuity and spectral sensitivity appeared structurally well completed. In general, major maturational changes observable after birth were apparent predominantly in the pigment epithelium of the retina.

Ring-billed gulls ( Larus delawarensis ) and gray gulls ( Larus modestus ) are two species active both by day and night. We have investigated the retinal adaptations that allow the diurnal and nocturnal behaviours of these two species. Electroretinograms and histological analyses show that both species have a duplex retina in which cones outnumber rods, but the number of rods appears sufficient to provide vision at night. Their retinas respond over the same scotopic dynamic range of 3.4 log cd m −2 , which encompasses all of the light levels occurring at night in their photic environment. The amplitudes of the scotopic saturated a- and b-wave responses as well as the photopic saturated b-wave response and the photopic sensitivity parameter S are however higher in ring-billed gulls than in gray gulls. Moreover, the process of dark adaptation is about 30 min faster in gray gulls than in ring-billed gulls. Our results suggest that both species have acquired in the course of their evolution functional adaptations that can be related to their specific photic environment.