Why different regions of the retina have different spectral sensitivities: A review of mechanisms and functional significance of intraretinal variability in spectral sensitivity in vertebrates

Abstract

Vision is used in nearly all aspects of animal behavior, from prey and predator detection to mate selection and parental care. However, the light environment typically is not uniform in every direction, and visual tasks may be specific to particular parts of an animal's field of view. These spatial differences may explain the presence of several adaptations in the eyes of vertebrates that alter spectral sensitivity of the eye in different directions. Mechanisms that alter spectral sensitivity across the retina include (but are not limited to) variations in: corneal filters, oil droplets, macula lutea, tapeta, chromophore ratios, photoreceptor classes, and opsin expression. The resultant variations in spectral sensitivity across the retina are referred to as intraretinal variability in spectral sensitivity (IVSS). At first considered an obscure and rare phenomenon, it is becoming clear that IVSS is widespread among all vertebrates, and examples have been found from every major group. This review will describe the mechanisms mediating differences in spectral sensitivity, which are in general well understood, as well as explore the functional significance of intraretinal variability, which for the most part is unclear at best.

Intra-retinal variation of opsin gene expression in the guppy (Poecilia reticulata)

“…A number of other in situ hybridization and MSP studies in fish have reported intra-retinal variability in opsin expression and spectral absorption [for a recent review see Temple (Temple, 2011)]. For example, Takechi and Kawamura showed that longer wavelength opsins were expressed in ventral and peripheral regions of the retina in zebrafish (Takechi and Kawamura, 2005).…”

“…intra-retinal variation) could be advantageous for fish, given that the light hitting the dorsal retina is of different spectral composition from that hitting the ventral retina, as a result of the filtering properties of water and any dissolved organic solutes or suspended particulates in it that alter the spectral properties of light. Several species of fish have been shown to possess intra-retinal variation in spectral sensitivity, exhibiting different densities and/or distributions of various photoreceptor types, apparently to deal with varied visual tasks (Takechi and Kawamura, 2005;Allison et al, 2006;Veldhoen et al, 2006;Temple et al, 2010;Temple, 2011). This intra-retinal variation in opsin gene expression may also influence the behaviour of species that use colour in mate choice decisions (Temple, 2011).…”

“…Several species of fish have been shown to possess intra-retinal variation in spectral sensitivity, exhibiting different densities and/or distributions of various photoreceptor types, apparently to deal with varied visual tasks (Takechi and Kawamura, 2005;Allison et al, 2006;Veldhoen et al, 2006;Temple et al, 2010;Temple, 2011). This intra-retinal variation in opsin gene expression may also influence the behaviour of species that use colour in mate choice decisions (Temple, 2011). During mate selection, female guppies have been noted to investigate the male from an elevated position in the water column (Baerends et al, 1955), suggesting that illumination and the location of opsin expression in the retina may be important during mate selection in this species.…”

A second visual rhodopsin gene,rh1-2, is expressed in zebrafish photoreceptors and found in other ray-finned fishes

“…In adult fish, however, rh2-3 and rh2-4 expression expands to additional portions of the peripheral retina (Takechi and Kawamura, 2005), while the pattern of rh1-2 stays mostly the same. It is possible that even limited rh1-2 expression in the ventral peripheral retina, which produces a slightly blue-shifted pigment compared with rhodopsin, may be advantageous for detecting the spectrum of down-welling light, a phenomenon that has been noted in cone opsin duplicates (Temple, 2011). Overall, the fact that rh1-2 has both a different and more restrictive expression pattern than rh1 in the retina is not unusual, as a diversity of expression patterns seem to be a common feature of duplicated opsin genes in teleost fish (Hofmann and Carleton, 2009).…”

Three cone opsin genes determine the properties of the visual spectra in the Japanese anchovy Engraulis japonicus (Engraulidae, Teleostei)

“…It has been shown in many studies and comprehensive reviews (Chiao et al, 2000;Kusmić and Gualtieri, 2000;Lythgoe, 1979;Temple, 2011) that aquatic animals, particularly fish, exhibit numerous adaptations and specializations of their visual systems to match the ambient light properties of the environment. In fish, as in other lower vertebrates studied thus far, specialized mechanisms have been developed at the periphery of the visual system (i.e.…”