Craig W. Hawryshyn

Thyroxine Induces a Precocial Loss of Ultraviolet Photosensitivity in Rainbow Trout (Oncorhynchus mykiss, Teleostei)

Small (< 30 g) juvenile rainbow trout (Oncorhynchus mykiss) possess retinal photoreceptor mechanisms sensitive to ultraviolet (UV), short (S), middle (M) and long (L) wavelengths. During normal development, the sensitivity peak of the UV cone mechanism (360 nm) shifts towards the S-wavelengths (to an intermediate lambda max of 390 nm) until, at approx. 60 g, individuals are no longer sensitive in the UV (only a S-wavelength peak at 430 nm remains). This shift in spectral sensitivity is associated with the loss of small accessory corner cones from the retinal photoreceptor cell mosaic. Treating small (< 30 g) rainbow trout with thyroid hormone induced a precocial loss of UV photosensitivity and an associated change in the retinal photoreceptor cell mosaic, identical to the events that occur during normal development.

The developmental trajectory of ultraviolet photosensitivity in rainbow trout is altered by thyroxine

Small (< 30 g) juvenile rainbow trout (Oncorhynchus mykiss) possess retinal photoreceptor mechanisms sensitive to ultraviolet (UV), short (S), middle (M), and long (L) wavelengths. During normal development, UV photosensitivity is lost progressively until, by approx. 60 g, individuals are no longer sensitive in the UV. This shift in spectral sensitivity is associated with the disappearance of small accessory corner cones (ACCs) from the retinal photoreceptor cell mosaic: the UV cone mechanism is lost. Exposing small (< 16 g) rainbow trout to the thyroid hormone thyroxine (T4) for a period of 6 weeks induced a precocial loss of the UV cone mechanism that was indistinguishable from the events that occur during normal development. Six weeks after termination of hormone treatment, the same individuals that had lost their UV photosensitivity after exposure to T4 once again possessed a peak in spectral sensitivity at 360 nm. ACCs had reappeared in the retinae of these fish. After 6 weeks of exposure to thyroxine, large (> 90 g) juvenile rainbow trout, which had lost their UV photoreceptor mechanism during normal development, were once again UV photosensitive and ACCs were found in their retinae. These results imply that the UV photoreceptor mechanism, although lost at one point during development, can reappear at another time during the life history of the same individual. Thyroid hormones appear to be involved in both the loss and reappearance of UV photosensitivity.

Cone photoreceptor topography in the retina of sexually mature Pacific salmonid fishes

We examined the retinal cone topography in sexually mature individuals from four species of Pacific salmonid fishes by using semithin plastic sections. We identified variations in cone density and cone arrangements and noted the presence of putative ultraviolet (UV) cones. Putative UV cones were found over an area extending dorsotemporally from the center of the retina. Because most of the putative UV cones are believed to disappear in early ontogeny, their presence over a large proportion (15–20%) of the surface area of the adult retina suggests that they may be reincorporated prior to or at sexual maturity, at least in rainbow trout.

Is the Use of Underwater Polarized Light by Fish Restricted to Crepuscular Time Periods

We measured the spectral distributions of the underwater total and polarized light fields in the upper photic zone of meso-eutrophic waters (i.e., blue-green waters containing medium to high chlorophyll a concentrations). Per cent polarization levels during the day were always lower than 40%, but at crepuscular times these values could increase to 67%. A corresponding change occurred in the spectral distribution, with proportionately more shorter wavelength photons contributing to the total spectrum during crepuscular periods. Electrophysiological recordings from the optic nerve of rainbow trout subjected to light stimuli of varying polarization percentages show that the animals threshold for detecting polarized light is between 63 and 72%. These physiological findings suggest that the use of water-induced polarized light cues by rainbow trout and similar percomorph fish should be restricted to crepuscular time periods.

Degeneration and regeneration of ultraviolet cone photoreceptors during development in rainbow trout

Ultraviolet‐sensitive (UVS) cones disappear from the retina of salmonid fishes during a metamorphosis that prepares them for deeper/marine waters. UVS cones subsequently reappear in the retina near sexual maturation and the return migration to natal streams. Cellular mechanisms of this UVS cone ontogeny were investigated using electroretinograms, in situ hybridization, and immunohistochemistry against opsins during and after thyroid hormone (TH) treatments of rainbow trout (Oncorhynchus mykiss). Increasing TH levels led to UVS cone degeneration. Labeling demonstrated that UVS cone degeneration occurs via programmed cell death and caspase inhibitors can inhibit this death. After the cessation of TH treatment, UVS cones regenerated in the retina. Bromodeoxyuridine (BrdU) was applied after the termination of TH treatment and was detected in the nuclei of cells expressing UVS opsin. BrdU was found in UVS cones but not other cone types. The most parsimonious explanation for the data is that UVS cones degenerated and UVS cones were regenerated from intrinsic retinal progenitor cells. Regenerating UVS cones were functionally integrated such that they were able to elicit electrical responses from second‐order neurons. This is the first report of cones regenerating during natural development. Both the death and regeneration of cones in retinae represent novel mechanisms for tuning visual systems to new visual tasks or environments. J. Comp. Neurol. 499:702–715, 2006.

Optic Nerve Response and Retinal Structure in Rainbow Trout of Different Sizes

This study presents evidence of ultraviolet (UV) sensitive, ON center ganglion cells in the fish retina. We determined the spectral sensitivity of ON and OFF responses from the optic nerve mass potential in small (18.0 - 28.5 g) and large (59.5-835 g) rainbow trout, with special reference to UV sensitivity. Under a mid+long-wavelength adapting background, the ON response of small fish revealed the presence of a UV cone mechanism (lambda max 390 nm) which was absent in large specimens. Under similar background conditions, the OFF response of both small and large fish showed one sensitivity peak, dominated by inputs from an M-cone mechanism. An almost complete absence of the accessory corner cones from the retinal mosaic was correlated with the loss of UV sensitivity.

Ontogeny of ultraviolet-sensitive cones in the retina of rainbow trout (Oncorhynchus mykiss)

In order to facilitate emerging models of retinal development, we developed electroretinogram and in situ hybridization protocols to examine the ontogeny of photoreceptors in the retina of a land‐locked salmonid, the rainbow trout (Oncorhynchus mykiss). We cloned cDNA fragments corresponding to the rod opsin and each of the four cone opsin gene families, which we utilized to produce riboprobes. We established the specificity of the in situ hybridization protocol by examining subcellular signal localization and through double‐labeling experiments. We confirm the assumption that the accessory corner cones in the square mosaic are the ultraviolet wavelength‐sensitive (UVS) cone photoreceptor (i.e., they express an SWS1 opsin) and observed UVS cones throughout the retina of small trout. Larger fish have a decrease in sensitivity to short wavelength light stimuli and the distribution of UVS cones in the mature retina is limited to the dorsal‐temporal quadrant. These larger fish also possess differentiated UVS cones in the peripheral germinal zone (PGZ), including within areas peripheral to mature retina lacking UVS cones. These data are consistent with the loss of putative UVS cones from the PGZ of a migratory salmonid of another genus, and thus the disappearance of UVS cones appears to be general to the Family Salmonidae, regardless of life history strategy. The generation, differentiation, and subsequent loss of UVS cones in the smolt PGZ is a dramatic example of the supposition that the mechanisms of PGZ development recapitulate the retinal embryogenesis of that species. J. Comp. Neurol. 461:294–306, 2003.

Intraspecific variation of spectral sensitivity in threespine stickleback (Gasterosteus aculeatus) from different photic regimes

To examine the influence of the spectral characteristics of underwater light on spectral sensitivity of the ON and OFF visual pathways, compound action potential recordings were made from retinal ganglion cells of threespine stickleback from different photic regimes. In fish from a red-shifted photic regime (λP50 680 nm for downwelling light at 1m), peak sensitivity of both the ON and OFF pathways was limited to long wavelength light (λmax 600–620). In contrast, the ON pathway of fish from a comparatively blue-shifted (λP50 566 nm) photic regime exhibited sensitivity to medium (λmax 540–560) and long (λmax 600 nm) wavelengths, while the OFF pathway exhibited peak sensitivity to only medium (λmax 540 nm) wavelength light. In a third population, where the the ambient light is moderately red-shifted (λP50 629 nm), the ON pathway once again exhibited only a long wavelength sensitivity peak at 620 nm, while the OFF pathway exhibited sensitivity to both medium (λmax 560 nm) and long (λmax 600–620 nm) wavelength light. These findings suggest that the photic environment plays an integral role in shaping spectral sensitivity of the ON and OFF pathways.

Polarized-light sensitivity in rainbow trout (Oncorhynchus mykiss): characterization from multi-unit responses in the optic nerve

Integrated spike activity of axons from the optic nerve was measured in an investigation of the e-vector sensitive mechanism underlying the ability of rainbow trout (Oncorhynchus mykiss) for orientation in downwelling, linearly-polarized light. In anaesthetized, immobilized fish, one eye was exposed to incremental light flashes which were superimposed over closely controlled background conditions. Under scotopic and various photopic conditions, intensity/response curves were generated from the on-response of the optic nerve. Relative sensitivity curves were then obtained as a function of e-vector direction for the 5 kinds of receptor cells in this trouts retina: rods, ultraviolet cones (UV), short wavelength cones (S), medium wavelength cones (M), and long wavelength cones (L).Under scotopic conditions, no sensitivity to e-vector was apparent: thus, rods do not mediate polarization sensitivity. Under photopic conditions, parr weighing 8–10 g exhibited e-vector sensitivity in two orthogonal channels. A UV stimulus (380 nm) on a white background evoked a three-peaked response (0°, 90°, and 180°) to the e-vector orientations presented in 30° increments between 0° and 180°. In contrast, when the background was illuminated with appropriate short and long wavelength cut-off filters, M-and L-cones showed maximum responses only to the horizontal (90°) plane whether they were stimulated at their α-absorption band or their β-absorption band in the near UV. Isolated UV-cones gave maximum responses to the vertical (0° and 180°) e-vector, thus corresponding to a second channel. The blue sensitive, S-cones, did not show evidence of polarization sensitivity. As well, no evidence of the polarization sensitivity was observed under UV isolating background conditions in larger individuals, 50–78 g smolts, although the other cone mechanisms responded as in smaller individuals.

Functional diversity in the color vision of cichlid fishes

BackgroundColor vision plays a critical role in visual behavior. An animals capacity for color vision rests on the presence of differentially sensitive cone photoreceptors. Spectral sensitivity is a measure of the visual responsiveness of these cones at different light wavelengths. Four classes of cone pigments have been identified in vertebrates, but in teleost fishes, opsin genes have undergone gene duplication events and thus can produce a larger number of spectrally distinct cone pigments. In this study, we examine the question of large-scale variation in color vision with respect to individual, sex and species that may result from differential expression of cone pigments. Cichlid fishes are an excellent model system for examining variation in spectral sensitivity because they have seven distinct cone opsin genes that are differentially expressed.ResultsTo examine the variation in the number of cones that participate in cichlid spectral sensitivity, we used whole organism electrophysiology, opsin gene expression and empirical modeling. Examination of over 100 spectral sensitivity curves from 34 individuals of three species revealed that (1) spectral sensitivity of individual cichlids was based on different subsets of four or five cone pigments, (2) spectral sensitivity was shaped by multiple cone interactions and (3) spectral sensitivity differed between species and correlated with foraging mode and the spectral reflectance of conspecifics. Our data also suggest that there may be significant differences in opsin gene expression between the sexes.ConclusionsOur study describes complex opponent and nonopponent cone interactions that represent the requisite neural processing for color vision. We present the first comprehensive evidence for pentachromatic color vision in vertebrates, which offers the potential for extraordinary spectral discrimination capabilities. We show that opsin gene expression in cichlids, and possibly also spectral sensitivity, may be sex-dependent. We argue that females and males sample their visual environment differently, providing a neural basis for sexually dimorphic visual behaviour. The diversification of spectral sensitivity likely contributes to sensory adaptations that enhance the contrast of transparent prey and the detection of optical signals from conspecifics, suggesting a role for both natural and sexual selection in tuning color vision.