Retinal cone photoreceptors of the deer mouse Peromyscus maniculatus : development, topography, opsin expression and spectral tuning

A quantitative analysis of photoreceptor properties was performed in the retina of the nocturnal deer mouse, Peromyscus maniculatus, using pigmented (wildtype) and albino animals. The aim was to establish whether the deer mouse is a more suitable model species than the house mouse for photoreceptor studies, and whether oculocutaneous albinism affects its photoreceptor properties. In retinal flatmounts, cone photoreceptors were identified by opsin immunostaining, and their numbers, spectral types, and distributions across the retina were determined. Rod photoreceptors were counted using differential interference contrast microscopy. Pigmented P. maniculatus have a rod-dominated retina with rod densities of about 450.000/mm(2) and cone densities of 3000 - 6500/mm(2). Two cone opsins, shortwave sensitive (S) and middle-to-longwave sensitive (M), are present and expressed in distinct cone types. Partial sequencing of the S opsin gene strongly supports UV sensitivity of the S cone visual pigment. The S cones constitute a 5-15% minority of the cones. Different from house mouse, S and M cone distributions do not have dorsoventral gradients, and coexpression of both opsins in single cones is exceptional (<2% of the cones). In albino P. maniculatus, rod densities are reduced by approximately 40% (270.000/mm(2)). Overall, cone density and the density of cones exclusively expressing S opsin are not significantly different from pigmented P. maniculatus. However, in albino retinas S opsin is coexpressed with M opsin in 60-90% of the cones and therefore the population of cones expressing only M opsin is significantly reduced to 5-25%. In conclusion, deer mouse cone properties largely conform to the general mammalian pattern, hence the deer mouse may be better suited than the house mouse for the study of certain basic cone properties, including the effects of albinism on cone opsin expression

Bat Eyes Have Ultraviolet-Sensitive Cone Photoreceptors

Mammalian retinae have rod photoreceptors for night vision and cone photoreceptors for daylight and colour vision. For colour discrimination, most mammals possess two cone populations with two visual pigments (opsins) that have absorption maxima at short wavelengths (blue or ultraviolet light) and long wavelengths (green or red light). Microchiropteran bats, which use echolocation to navigate and forage in complete darkness, have long been considered to have pure rod retinae. Here we use opsin immunohistochemistry to show that two phyllostomid microbats, Glossophaga soricina and Carollia perspicillata, possess a significant population of cones and express two cone opsins, a shortwave-sensitive (S) opsin and a longwave-sensitive (L) opsin. A substantial population of cones expresses S opsin exclusively, whereas the other cones mostly coexpress L and S opsin. S opsin gene analysis suggests ultraviolet (UV, wavelengths <400 nm) sensitivity, and corneal electroretinogram recordings reveal an elevated sensitivity to UV light which is mediated by an S cone visual pigment. Therefore bats have retained the ancestral UV tuning of the S cone pigment. We conclude that bats have the prerequisite for daylight vision, dichromatic colour vision, and UV vision. For bats, the UV-sensitive cones may be advantageous for visual orientation at twilight, predator avoidance, and detection of UV-reflecting flowers for those that feed on nectar

Ontogenetic Development of Weberian Ossicles and Hearing Abilities in the African Bullhead Catfish

BACKGROUND: The weberian apparatus of otophysine fishes facilitates sound transmission from the swimbladder to the inner ear to increase hearing sensitivity. It has been of great interest to biologists since the 19(th) century. No studies, however, are available on the development of the weberian ossicles and its effect on the development of hearing in catfishes. METHODOLOGY/PRINCIPAL FINDINGS: We investigated the development of the weberian apparatus and auditory sensitivity in the catfish Lophiobagrus cyclurus. Specimens from 11.3 mm to 85.5 mm in standard length were studied. Morphology was assessed using sectioning, histology, and X-ray computed tomography, along with 3D reconstruction. Hearing thresholds were measured utilizing the auditory evoked potentials recording technique. Weberian ossicles and interossicular ligaments were fully developed in all stages investigated except in the smallest size group. In the smallest catfish, the intercalarium and the interossicular ligaments were still missing and the tripus was not yet fully developed. Smallest juveniles revealed lowest auditory sensitivity and were unable to detect frequencies higher than 2 or 3 kHz; sensitivity increased in larger specimens by up to 40 dB, and frequency detection up to 6 kHz. In the size groups capable of perceiving frequencies up to 6 kHz, larger individuals had better hearing abilities at low frequencies (0.05-2 kHz), whereas smaller individuals showed better hearing at the highest frequencies (4-6 kHz). CONCLUSIONS/SIGNIFICANCE: Our data indicate that the ability of otophysine fish to detect sounds at low levels and high frequencies largely depends on the development of the weberian apparatus. A significant increase in auditory sensitivity was observed as soon as all weberian ossicles and interossicular ligaments are present and the chain for transmitting sounds from the swimbladder to the inner ear is complete. This contrasts with findings in another otophysine, the zebrafish, where no threshold changes have been observed

Cone opsin expression in adult pigmented and albino deer mice.

<p>Double immunofluorescence labeling for S and M opsin in flatmounted retinae, the focus is on the opsin-containing cone outer segments. <b>Top</b>: There is a sparse population of S opsin-expressing cones in the wildtype and a more numerous one in the albino. <b>Middle</b>: The populations of M opsin-expressing cones are similar in both genotypes. <b>Bottom</b>: Merge of the top and middle images shows that S and M cones form separate populations in the wildtype, whereas many cones coexpress both opsins in the albino (yellowish colors); cone examples are arrowed. The scale bar applies to all images. </p

Postnatal development of cone opsin expression.

<p>The four colored blocks show the development of cone properties along the dorso-ventral axis of the retina from postnatal day P7 to adulthood. Each block contains a 3D diagram summarizing the progression of a property across the retina and over time, and the individual diagrams for each time point. For each time point, the cones were counted in three wildtype retinae double-immunolabeled for M and S opsin, data points give mean values and SEM. Top block (grey): Total cone density shows a decline with age, because of retinal areal growth. Second block (blue): Density of S opsin-expressing cones. At P7 nearly all cones express S opsin, during subsequent retinal maturation the number of S opsin-expressing cones drops dramatically to adult values. Third block (green): The density of M opsin-expressing cones is low at P7 and is highest in the central retina that leads maturation. During subsequent maturation, the number of M opsin-expressing cones increases to adult values. Bottom block (orange): Density of cones coexpressing M and S opsin, comprising practically all M opsin-expressing cones at P7 and a decreasing proportion of the cones at later stages. All vertical axes give cone densities (cones/mm²), eccentricities are given as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080910#pone-0080910-g005" target="_blank">Figure 5</a>.</p

Maps of cone densities in adult pigmented and albino deer mice.

<p>The two columns each show three maps of the same retina, giving total cone density (<i>top</i>), S cone density (<i>middle</i>), and M cone density (<i>bottom</i>). Densities at the isodensity lines are cones/mm². The small circles in the center of the retinae indicate the optic nerve head. D, dorsal; V, ventral.</p

Quantitative comparison of cone densities and opsin expression in adult wildtype and albino deer mice.

<p>The local densities of cones expressing M opsin, S opsin, or both, were determined along the dorso-ventral axis of the retina in three wildtype and three albino retinae, they are given as mean and SEM. The abscissa of each graph gives eccentricity as percentage of the distance between the optic nerve head (located at 0%) and the ventral (V) or dorsal (D) margin of the retina (located at 100%), respectively. Total cone density and the density of M opsin-expressing cones are similar in both genotypes and show a density decline from central to peripheral retina. In contrast, the density of S opsin-expressing cones is much higher in the albino than in the wildtype. This is because of the large proportion of albino cones that coexpress both opsins. ★★★, differences statistically significant at p<0,001 (two-way ANOVA & Bonferroni’s post-hoc test). </p

Photoreceptor differences between pigmented and albino deer mice.

<p>(<b>A</b>) <i>Top</i>: flat view of photoreceptor inner segments in wildtype and albino animals, showing the larger IS diameter and lower density of the albino photoreceptors, differential interference contrast images. <i>Bottom</i>: cones in the same fields, combined immunofluorescence labeling for M and S opsin. The scale bar applies to all images. (<b>B</b>) Quantification of the photoreceptor densities in wildtype and albino. Counts were made at several positions across the retina (wildtype: 11 positions in 1 retina; albino: 6 positions in 2 retinae of 2 individuals; data given as mean and SEM. ★★★, difference statistically significant at p<0,001 (t-test).</p

Thyroid Hormone Signaling in the Mouse Retina.

Thyroid hormone is a crucial regulator of gene expression in the developing and adult retina. Here we sought to map sites of thyroid hormone signaling at the cellular level using the transgenic FINDT3 reporter mouse model in which neurons express β-galactosidase (β-gal) under the control of a hybrid Gal4-TRα receptor when triiodothyronine (T3) and cofactors of thyroid receptor signaling are present. In the adult retina, nearly all neurons of the ganglion cell layer (GCL, ganglion cells and displaced amacrine cells) showed strong β-gal labeling. In the inner nuclear layer (INL), a minority of glycineric and GABAergic amacrine cells showed β-gal labeling, whereas the majority of amacrine cells were unlabeled. At the level of amacrine types, β-gal labeling was found in a large proportion of the glycinergic AII amacrines, but only in a small proportion of the cholinergic/GABAergic 'starburst' amacrines. At postnatal day 10, there also was a high density of strongly β-gal-labeled neurons in the GCL, but only few amacrine cells were labeled in the INL. There was no labeling of bipolar cells, horizontal cells and Müller glia cells at both stages. Most surprisingly, the photoreceptor somata in the outer nuclear layer also showed no β-gal label, although thyroid hormone is known to control cone opsin expression. This is the first record of thyroid hormone signaling in the inner retina of an adult mammal. We hypothesize that T3 levels in photoreceptors are below the detection threshold of the reporter system. The topographical distribution of β-gal-positive cells in the GCL follows the overall neuron distribution in that layer, with more T3-signaling cells in the ventral than the dorsal half-retina