Spectral Types Of Photoreceptors Research Articles

Ancestral photoreceptor diversity as the basis of visual behaviour.

Animal colour vision is based on comparing signals from different photoreceptors. It is generally assumed that processing different spectral types of photoreceptor mainly serves colour vision. Here I propose instead that photoreceptors are parallel feature channels that differentially support visual-motor programmes like motion vision behaviours, prey capture and predator evasion. Colour vision may have emerged as a secondary benefit of these circuits, which originally helped aquatic vertebrates to visually navigate and segment their underwater world. Specifically, I suggest that ancestral vertebrate vision was built around three main systems, including a high-resolution general purpose greyscale system based on ancestral red cones and rods to mediate visual body stabilization and navigation, a high-sensitivity specialized foreground system based on ancestral ultraviolet cones to mediate threat detection and prey capture, and a net-suppressive system based on ancestral green and blue cones for regulating red/rod and ultraviolet circuits. This ancestral strategy probably still underpins vision today, and different vertebrate lineages have since adapted their original photoreceptor circuits to suit their diverse visual ecologies.

Trichromatic vision in toads: evidence from preference for colour objects during mate choice

Abstract Input of different spectral types of photoreceptors in amphibian colour vision has been assessed by studying the behaviour of male toads Bufo bufo and B. gargarizans in a laboratory. This method is based on the males’ innate reaction of approaching and clasping any visual object during the breeding season. A pair of colour stimuli made of paper or displayed on a LCD monitor has been selected to match the toad’s RGB colour space so that they differ by excitation of only a single spectral class of retinal photoreceptors. With pairwise presentation, the males are found to prefer a more ‘bluish’, or a less ‘reddish’, or a less ‘greenish’ stimulus from each pair. A microspectrophotometry of isolated rod and cone photoreceptors and an observation of behavioural responses in toads have revealed a trichromatic mesopic visual system based on a positive input from blue-sensitive photoreceptors and negative inputs from red-sensitive cones and green-sensitive rods. It is supposed that the observed colour preference and involvement of different chromatic mechanisms determine social interactions of anurans during mate choice.

Evidence for UV-green dichromacy in the basal hymenopteran Sirex noctilio (Siricidae)

A precondition for colour vision is the presence of at least two spectral types of photoreceptors in the eye. The order Hymenoptera is traditionally divided into the Apocrita (ants, bees, wasps) and the Symphyta (sawflies, woodwasps, horntails). Most apocritan species possess three different photoreceptor types. In contrast, physiological studies in the Symphyta have reported one to four photoreceptor types. To better understand the evolution of photoreceptor diversity in the Hymenoptera, we studied the Symphyta Sirex noctilio, which belongs to the superfamily Siricoidea, a closely related group of the Apocrita suborder. Our aim was to (i) identify the photoreceptor types of the compound eye by electroretinography (ERG), (ii) characterise the visual opsin genes of S. noctilio by genomic comparisons and phylogenetic analyses and (iii) analyse opsin mRNA expression. ERG measurements revealed two photoreceptor types in the compound eye, maximally sensitive to 527 and 364 nm. In addition, we identified three opsins in the genome, homologous to the hymenopteran green or long-wavelength sensitive (LW) LW1, LW2 and ultra-violet sensitive (UV) opsin genes. The LW1 and UV opsins were found to be expressed in the compound eyes, and LW2 and UV opsins in the ocelli. The lack of a blue or short-wavelength sensitive (SW) homologous opsin gene and a corresponding receptor suggests that S. noctilio is a UV-green dichromate.

Foliage Intensity is an Important Cue of Habitat Location for Empoasca onukii.

For many herbivorous insects, vision is more important than olfaction in the prealighting stage of host habitat location. Tea leafhoppers, Empoasca onukii (Hemiptera, Cicadellidae), are serious pests that preferentially inhabit the tender leaves of tea plants across China. Here, we investigated whether tea leafhoppers could distinguish foliage colors associated with different leaf ages and use this visual cue to guide suitable habitat location from short distances. Similar to honeybees, the adult E. onukii has an apposition type of compound eye, and each ommatidium has eight retinular cells, in which three spectral types of photoreceptors are distributed, with peak sensitivities at 356 nm (ultraviolet), 435 nm (blue), and 542 nm (green). Both changes in spectral intensity and hue of reflectance light of the host foliage were correlated with varying leaf age, and the intensity linearly decreased with increasing leaf age. Behavioral responses also showed that adult E. onukii could discriminate between the simulated colors of host foliage at different leaf ages without olfactory stimuli and selected the bright colors that strongly corresponded to those of tender leaves. The results suggest that, compared with the spectral composition (hue), the intensity of light reflectance from leaves at different ages is more important for adult leafhoppers when discriminating host foliage and could guide them to tender leaves at the top of tea shoots.

Visual cues of oviposition sites and spectral sensitivity of Cydia strobilella L.

We investigated whether the spruce seed moth (Cydia strobilella L., Tortricidae: Grapholitini), an important pest in seed orchards of Norway spruce (Picea abies (L.) Karst.), can make use of the spectral properties of its host when searching for flowers to oviposit on. Spectral measurements showed that the flowers, and the cones they develop into, differ from a background of P. abies needles by a higher reflectance of long wavelengths. These differences increase as the flowers develop into mature cones. Electroretinograms (ERGs) in combination with spectral adaptation suggest that C. strobilella has at least three spectral types of photoreceptor; an abundant green-sensitive receptor with maximal sensitivity at wavelength λmax=526nm, a blue-sensitive receptor with λmax=436nm, and an ultraviolet-sensitive receptor with λmax=352nm. Based on our spectral measurements and the receptor properties inferred from the ERGs, we calculated that open flowers, which are suitable oviposition sites, provide detectable achromatic, but almost no chromatic contrasts to the background of needles. In field trials using traps of different spectral properties with or without a female sex pheromone lure, only pheromone-baited traps caught moths. Catches in baited traps were not correlated with the visual contrast of the traps against the background. Thus, visual contrast is probably not the primary cue for finding open host flowers, but it could potentially complement olfaction as a secondary cue, since traps with certain spectral properties caught significantly more moths than others.

Sexual dimorphism in the compound eye of Heliconius erato: a nymphalid butterfly with at least five spectral classes of photoreceptor.

Most butterfly families expand the number of spectrally distinct photoreceptors in their compound eye by opsin gene duplications together with lateral filter pigments; however, most nymphalid genera have limited diversity, with only three or four spectral types of photoreceptor. Here, we examined the spatial pattern of opsin expression and photoreceptor spectral sensitivities in Heliconius erato, a nymphalid with duplicate ultraviolet opsin genes, UVRh1 and UVRh2 We found that the H. erato compound eye is sexually dimorphic. Females express the two UV opsin proteins in separate photoreceptors, but males do not express UVRh1. Intracellular recordings confirmed that females have three short wavelength-sensitive photoreceptors (λmax=356, ∼390 and 470 nm), while males have two (λmax=390 and ∼470 nm). We also found two long wavelength-sensitive photoreceptors (green, λmax∼555 nm, and red, λmax∼600 nm), which express the same LW opsin. The red cell's shifted sensitivity is probably due to perirhabdomal filtering pigments. Sexual dimorphism of the UV-absorbing rhodopsins may reflect the females' need to discriminate conspecifics from co-mimics. Red-green color vision may be used to detect differences in red coloration on Heliconius wings, or for host-plant identification. Among nymphalids so far investigated, only H. erato is known to possess five spectral classes of photoreceptor; sexual dimorphism of the eye via suppression of one class of opsin (here UVRh1 in males) has not - to our knowledge - been reported in any animal.

Spectral sensitivity of the compound eyes of Anomala corpulenta motschulsky (Coleoptera: Scarabaeoidea)

The scarab beetle, Anomala corpulenta Motschulsky (Coleoptera: Scarabaeoidea), is a widespread and destructive pest in China. Vision is one of the most important means of acquiring information about the external environment. In order to contribute to the understanding of the perception of visual stimuli in this species, the light sensitivity and spectral responses of the scarab beetle, A. corpulenta, were measured by using an electroretinogram (ERG) technique. In total, 14 monochromatic light intensities, between 340 and 605 nm, were applied to the compound eyes of A. corpulenta under varying levels of adaptation to dark and light conditions. The results showed that all light stimuli induced an ERG response, with varied amplitudes. The spectral sensitivity curve of dark-adapted eyes showed one major peak (~400 nm; near-ultraviolet), a secondary peak (from 498 to 562 nm; yellow-green) and the third peakat 460 nm. By contrast, in light-adapted eyes, only a near-UV peak was observed. From these results, we conclude that the compound eye of A. corpulenta is likely to have at least three spectral types of photoreceptor. Significance of differences were also recorded in the responses of male and female compound eyes, as well as diurnally and nocturnally. The amplitude of ERG in response to white-light stimuli varied with the light intensity: The stronger the luminance, the higher the ERG value. This suggests that the compound eye of A. corpulenta adapts quickly to changing light conditions, enabling A. corpulenta to maintain nocturnal activities.

Diversity of the Photoreceptors and Spectral Opponency in the Compound Eye of the Golden Birdwing, Troides aeacus formosanus

The compound eye of the Golden Birdwing, Troides aeacus formosanus (Papilionidae, Lepidoptera), is furnished with three types of ommatidia, which are clearly different in pigmentation around the rhabdom. Each ommatidium contains nine photoreceptors, whose spectral sensitivities were analyzed electrophysiologically. We identified nine spectral types of photoreceptor with sensitivities peaking at 360 nm (UV), 390 nm (V), 440 nm (B), 510 nm (BG), 540 nm (sG), 550 nm (dG), 580 nm (O), 610 nm (R), and 630 nm (dR) respectively. The spectral sensitivities of the V, O, R and dR receptors did not match the predicted spectra of any visual pigments, but with the filtering effects of the pigments around the rhabdom, they can be reasonably explained. In some of the receptors, negative-going responses were observed when they were stimulated at certain wavelengths, indicating antagonistic interactions between photoreceptors.

Nocturnal colour vision – not as rare as we might think

The dual retina of humans and most vertebrates consists of multiple types of cone for colour vision in bright light and one single type of rod, leaving these animals colour-blind at night. Instead of comparing the signals from different spectral types of photoreceptors, they use one highly sensitive receptor, thus improving the signal-to-noise ratio. However, nocturnal moths and geckos can discriminate colours at extremely dim light intensities when humans are colour-blind, by sacrificing spatial and temporal rather than spectral resolution. The advantages of colour vision are just as obvious at night as they are during the day. Colour vision is much more reliable than achromatic contrast, not only under changing light intensities, but also under the colour changes occurring during dusk and dawn. It can be expected that nocturnal animals other than moths and geckos make use of the highly reliable colour signals in dim light.

Evidence for trichromacy in the green peach aphid, Myzus persicae (Sulz.) (Hemiptera: Aphididae)

The green peach aphid, Myzus persicae (Hemiptera: Aphididae) is an important phytophagous pest of greenhouse and field crops. In the host finding process visual cues are of paramount importance. In order to contribute to the understanding of the perception of visual stimuli in this species, we measured the electroretinogram of alate female summer migrants of M. persicae. The spectral sensitivity was measured in 10 nm steps under both dark and light adaptation from 320 to 640 nm. The dark adapted spectral sensitivity curve showed one maximum in the green region around 530 nm and a distinct shoulder between 500 and 510 nm. In presence of adapting light, a secondary blue–green peak (490 nm) and a third peak in the near UV (330–340 nm) were observed. From these results we conclude that M. persicae has three spectral types of photoreceptors.

Animal colour vision--behavioural tests and physiological concepts.

Over a century ago workers such as J. Lubbock and K. von Frisch developed behavioural criteria for establishing that non-human animals see colour. Many animals in most phyla have since then been shown to have colour vision. Colour is used for specific behaviours, such as phototaxis and object recognition, while other behaviours such as motion detection are colour blind. Having established the existence of colour vision, research focussed on the question of how many spectral types of photoreceptors are involved. Recently, data on photoreceptor spectral sensitivities have been combined with behavioural experiments and physiological models to study systematically the next logical question: 'what neural interactions underlie colour vision?' This review gives an overview of the methods used to study animal colour vision, and discusses how quantitative modelling can suggest how photoreceptor signals are combined and compared to allow for the discrimination of biologically relevant stimuli.

Ovipositing butterflies use a red receptor to see green

Swallowtail butterflies of the species Papilio aegeus oviposit on the leaves of Rutaceae plants in Australia. They possess receptor types with sensitivity peaks around 390 nm (violet receptor) and 610 nm (red receptor), in addition to the receptor types common in insects with sensitivity peaks at 360 nm (ultraviolet receptor), 440 nm (blue receptor) and 540 nm (green receptor). Multiple- and dual-choice experiments show that females of P. aegeus prefer to oviposit on substrata that look green to humans. A class of simple models is developed to describe this choice behaviour in terms of linear interactions between the different spectral types of photoreceptors. The green receptor has a positive influence, whereas the blue (and possibly the ultraviolet and violet) receptor and the red receptor have negative influences on the choice behaviour. Colour choice for oviposition is thus guided by a single chromatic mechanism. Caterpillars of P. aegeus grow faster on young leaves which, according to the model, should be preferred by females for oviposition. The importance of the red receptor for the discrimination between different green leaves is discussed in ecological and comparative contexts. Finally, in an evolutionary perspective, the possibility is discussed that colour vision systems like those of honeybees might have evolved as a combination of two or more such chromatic mechanisms.

Identification of photoreceptor locations in the compound eye of Coccinella septempunctata Linnaeus (Coleoptera, Coccinellidae)

Three spectral types of photoreceptor with sensitivity maxima in the 360 nm (u.v. light), 420 nm (blue light) and 520 nm (green light) were characterized in the compound eye of Coccinella septempunctata Linnaeus by intracellular electro-physiological recording. All three different spectral types of photoreceptor were found to respond to polarized light with an average polarization sensitivity (PS) value around 4.0. Referring the longitudinal direction ( Y-axis) of the compound eye as 0°, the e-vector of polarized light giving maximal sensitivity were 45° for the u.v. receptor, 75° for the blue receptor, 45 and 135° for the green receptor. These values were compared to the angles between the Y-axis of the compound eye and the microvillar directions in the rhabdomeres of eight retinula cells. It was concluded that all six peripheral retinula cells (Nos 1–6) were green receptors and that the two central retinula cells (Nos 7 and 8) were u.v. and blue receptors, respectively.

Spectral sensitivities of photoreceptors and lamina monopolar cells in the dragonfly, Hemicordulia tau

Five spectral types of photoreceptors with peak sensitivities at 330 nm, 410 nm, 460 nm, 525 nm and 630 nm were recorded from the ventral eye of the dragonfly, Hemicordulia tau. Often the 525 nm photoreceptors presented broader, and the 630 nm photoreceptors narrower, spectral sensitivities than would be excepted of a photopigment with the same peak sensitivity. Four types of lamina monopolar cells (cell types 1–4) were recognised from their dark-adapted spectral sensitivities and their anatomy. The anatomical identification allows tentative assignation to the monopolar cell classification from Sympetrum rubicundulum obtained using Golgi staining (Meinertzhagen and Armett-Kibel 1982). When dark-adapted, the monopolar cells had peak spectral sensitivities that were similar to single photoreceptors or appeared to pool receptor outputs, but in some cases spectral sensitivity changed markedly upon adaptation to white and to chromatic light, in one case (cell type 2) apparently ‘switching off’ a UV-sensitive input.

Electrical inhibition in the retina of the butterflyPapilio

1. Four spectral types of photoreceptors have been characterized by double electrode recordings, with one electrode inside the cell and the other immediately outside. The colour types are: UV — peak sensitivity at 390 nm, blue — 450 nm, green — 540 nm and red — 610 nm. Recordings from the red receptors presented here are the first complete electrophysiological confirmations of the microspectrophotometrically measured red receptors in the retina of butterflies (Bernard 1979). 2. Differential recording (extracellular subtracted from intracellular) shows that the hyperpolarizing afterpotential (HAP) is eliminated when a unit is stimulated at peak wavelength, and greatly reduced during off-peak stimulation. This implies that the HAP is at least partially due to passive lateral electrical inhibition, in addition to the ionic conductance changes previously postulated. 3. The change from a point source stimulus to a diffuse extended source increases both the extracellular and the intracellular hyperpolarizations (at off-peak wavelengths), and reduces the intracellular depolarization, but differential recordings show that the transmembrane potential does not change. 4. The existence of the secondary peak (UV) in green-peak cells and its changes in response to various stimuli are adequately explained by a rhodopsin with a β-peak and by interactions between the photoreceptors. 5. Differential recording brings most of the spectral sensitivities to the curves predicted by the Dartnall nomograms. The remaining discrepancies can be attributed to the inadequacy of the placement of the extracellular electrode. 6. A model of electrical lateral inhibition is presented that accounts for the observed effects. The model is an extended version of the one presented by Shaw (1975).