Green-sensitive Photoreceptors Research Articles

Ommatidial type‐specific interphotoreceptor connections in the lamina of the swallowtail butterfly, Papilio xuthus

The eye of the butterfly Papilio xuthus contains a random array of three types of ommatidia (types I-III), each bearing nine photoreceptors, R1-R9. Of the six spectral classes of photoreceptors identified, types I, II, and III ommatidia contain four, three, and two classes, respectively: the ommatidia are thus spectrally heterogeneous. The photoreceptors send their axons to the lamina where, together with some large monopolar cells (LMCs), the nine from a single ommatidium contribute to a module called a lamina cartridge. We recently reported that among different photoreceptor axon terminals visualized by confocal microscopy, the number and length of axon collaterals differ for different spectral receptors, suggesting that lamina circuits are specific for each ommatidial type. Here we studied the distribution of synapse-like structures in the cartridges, first characterizing a photoreceptor by measuring its spectral sensitivity and then injecting Lucifer yellow (LY). We subsequently histologically identified the type of ommatidium to which the injected photoreceptor belonged, cut serial ultrathin sections of the entire lamina, labeled these with anti-LY immunocytochemistry, and then localized synapse-like structures. We found numerous interphotoreceptor contacts both within and between cartridges, the combination of which was again specific for the ommatidial type. R3 and R4, which are green-sensitive photoreceptors in all ommatidia, have thick axons lacking collaterals. We found that these cells exclusively make contacts with LMCs and not with photoreceptors. We therefore presume that R3 and R4 construct a system for motion vision, whereas other randomly distributed spectral types provide inputs for color vision.

Adult stemmata of the butterfly Vanessa cardui express UV and green opsin mRNAs

Adult stemmata are distinctive insect photoreceptors located on the posterior surfaces of the optic lobes. They originate as larval eyes that migrate inward during metamorphosis. We used a combination of light microscopy and in situ hybridization to examine their anatomical organization in the butterfly Vanessa cardui and to test for the presence of visual pigments, the light sensitive components of the visual transduction pathway. The bilateral cluster of six internal stemmata is located near the ventral edge of the lamina. They retain the dark screening pigment and overlying crystalline cones of the larval stemmata. We found two opsin mRNAs expressed in the stemmata that are also expressed, respectively, in UV-sensitive and green-sensitive photoreceptor cells in the compound eye. A third mRNA that is expressed in blue-sensitive photoreceptor cells of the compound eye was not expressed in the stemmata. Our results reinforce the idea that the adult stemmata are not merely developmental remnants of larval eyes, but remain functional, possibly as components of the circadian input channel.

Reflection of Near-Ultraviolet Radiation From Flowers of Australian Native Plants

Eighty-six species of Australian native plants were assessed in the near-ultraviolet (UV-A) (320-400 nm) and visible regions of the electromagnetic spectrum. Relationships between flower colour, size, symmetry and UV-A reflection were examined. The frequency of species in this sample that reflected UV-A radiation was found to be consistent with major overseas studies. A quantitative photographic study of the spectral reflection from the yellow flower of Hibbertia obtusifolia DC. (Dilleniaceae) was conducted for radiation with wavelengths of 280-800 nm. How an insect with UV-A-, blue- and green-sensitive photoreceptors might see H. obtusifolia as a two-coloured flower, and how this could aid a floral visitor's orientation is discussed.

Voltage-activated outward currents in adult and nymphal locust photoreceptors

The membrane properties of dark-adapted green sensitive photoreceptors of adult and nymphal desert locust (Schistocerca gregaria) were investigated in situ with single electrode (discontinuous) current and voltage clamp techniques. The photoreceptors had a resting potential of about -70 mV. The membrane rectified strongly in response to depolarizing current pulses at and above the resting potential. Two outward currents could be distinguished on the basis of different kinetics. The first, a transient current, was inactivating between-40 mV and -100 mV, and activated above -90 mV. The second, a sustained current had a similar activation range. The inactivating current could be blocked by application of 50 mM TEA into the retinal extracellular space. Both currents were expressed in nymphal photoreceptors already in the 1st instar larva and have similar properties as in the adults, although the behaviour of adults and nymphs is different. The conductances underlying these currents could be shown to modify the frequency response of the photoreceptor membrane.

Transplantation of transgenic photoreceptors to RD mouse retina

Photoreceptors of nocturnal geckos are transmuted cones that acquired rod morphological and physiological properties but retained cone-type phototransduction proteins. We have used microspectrophotometry and microfluorometry of solitary isolated green-sensitive photoreceptors of Tokay gecko to study the initial stages of the visual cycle within these cells. These stages are the photolysis of the visual pigment, the reduction of all-trans retinal to all-trans retinol, and the clearance of all-trans retinol from the outer segment (OS) into the interphotoreceptor space. We show that the rates of decay of metaproducts (all-trans retinal release) and retinal-to-retinol reduction are intermediate between those of typical rods and cones. Clearance of retinol from the OS proceeds at a rate that is typical of rods and is greatly accelerated by exposure to interphotoreceptor retinoid-binding protein, IRBP. The rate of retinal release from metaproducts is independent of the position within the OS, while its conversion to retinol is strongly spatially non-uniform, being the fastest at the OS base and slowest at the tip. This spatial gradient of retinol production is abolished by dialysis of saponin-permeabilized OSs with exogenous NADPH or substrates for its production by the hexose monophosphate pathway (NADP + glucose-6-phosphate or 6-phosphogluconate, glucose-6-phosphate alone). Following dialysis by these agents, retinol production is accelerated by several-fold compared to the fastest rates observed in intact cells in standard Ringer solution. We propose that the speed of retinol production is set by the availability of NADPH which in turn depends on ATP supply within the outer segment. We also suggest that principal source of this ATP is from mitochondria located within the ellipsoid region of the inner segment.

Green-sensitive cone photoreceptors are selectively labeled by Procion yellow dye in goldfish retina

Selective labeling of intravitreal Procion yellow dye by presumed blue-sensitive cone photoreceptors has been demonstrated in primate retina. To determine whether Procion yellow is selective for this cone type in an unrelated vertebrate species, labeling by this dye was studied in goldfish retina, where cone pigment type can be directly inferred from photoreceptor morphology. At low vitreal concentrations of the dye (less than 0.4%), only cone outer segments were labeled. At vitreal concentrations of 0.4-0.5%, the inner segments of short-double cones and a subset of long single cones (presumed green-sensitive cones) were selectively stained. At still higher vitreal concentrations (0.6-0.7%), the inner segments of short-single cones and miniature short-single cones (presumed blue-sensitive cones) showed evidence of Procion label, but were not as heavily labeled. The inner segments of long-double cones and a subset of long-single cones (presumed red-sensitive cones) did not label at any of these concentrations. These results show that Procion yellow is not a selective marker for blue-sensitive cones in the goldfish retina. In addition, stained rod and cone nuclei were observed at each dye concentration, including those concentrations at which no inner segments were labeled.

Visual edge detection in the honeybee and its chromatic properties

Free-flying bees were trained to collect a reward of sugar-water at one of several discs placed horizontally on a contrasting background. In sub­sequent tests the reward was removed and the behaviour of the bees was observed and recorded on video-tape while they landed on the experi­mental arrangement in search of the reward. The spatial distribution of the landings was analysed to measure the detectability of the discs and attractiveness of their boundaries, as com­pared to the interior regions. The results reveal that, while landing on figures, bees pay special attention to the edges. Even though the reward is placed at a randomly chosen location within the figure during training, the bees show a distinct preference for landing near the boundary of the figure. The bees’ preference for edges is restricted to figures with bound­aries that provide contrast to the green-sensitive receptors. When the boundaries contain no green contrast, the edge preference disappears. In this situation, landings continue to occur mainly within the figure, but they tend to be distributed randomly over its entire surface. Thus, whereas colour information can mediate the detection of objectsper se, the detection of edges, at least in the context of landing on a figure, is a colour-blind performance that is driven primarily by signals from the bee’s green-sensitive photoreceptors. This finding has interesting parallels in primate vision, where edge detection is also colour-blind. On the basis of these findings, we propose that edges provide cues that play an important role in guiding landing manouevres towards objects of interest, such as flowers.

Comparative study of temporal summation and response form in hymenopteran photoreceptors.

1. Temporal summation was measured in green-sensitive photoreceptors of seven hymenopteran species with various life styles: three bees, Melipona quadrifasciata quadrifasciata, Trigona spinnipes and Bombus morio; one wasp, Polistes canadensis; and three ants, Pseudomyrmex phyllophilus, Camponotus rufipes, and Atta sexdens rubropilosa. In all species approximate agreement with Bloch's law was confirmed. 2. Critical durations (tc), which varied from 10 ms (Pseudomyrmex) to 46 ms (Atta), are discussed in relation to the life styles of the species and to the mechanisms causing the differences. 3. The direct measures of critical duration obtained are compared to estimates made by convolution or integration of impulse responses measured here in one species and from published data. Linear convolution of typical impulse responses is shown to result in significant departures from Bloch's law, a fact that seems to have been overlooked in the literature. 4. The method used to measure temporal summation involved recording responses to 300-ms stimuli at various intensities; the form of these responses varied greatly from species to species. Possible causes of these variations are discussed.

Colour vision in butterflies

1. The retinula cells ofVanessa are similar in physiological properties, including spectral sensitivityS(λ) and negative electrical coupling, to those already described inPapilio, except that red-sensitive cells have not been found in either retina or lamina. 2. In the dark-adapted eye, with a stimulus of one colour, lamina ganglion cells yield only hyperpolarizations. 3. Some lamina ganglion cells (LMC's) have a broad flatS(λ) with angular sensitivity showing that they receive summed input from only one ommatidium. Others have narrowS(λ) and narrow field suggesting that primary receptors from single ommatidia interact on or before reaching them. Narrow peaks are near 500 or 550 nm, but not spread through the spectrum, suggesting colour specific behaviour rather than colour vision. 4. Vanessa itea, V. kershawi, Precis villida andHeteronympha merope all have optomotorS(λ) similar to the curves for green-sensitive photoreceptors, with broad peak between 500 and 550 nm. 5. Optomotor responses of butterflies fall off rapidly around 0.1 cd·m−2, whereas insects with superposition eyes are 100 times more sensitive. Calibrations suggest that the butterfly optomotor threshold is well above the photon flux that yields abundant bumps in the retinula cells. 6. There is difficulty in reconciling theS(λ) of the optomotor response with theS(λ) of any of the individual LMC's. 7. The physiological properties of receptors, LMC's and deep optic lobe units are brought together in a discussion of insect colour vision.

Change of synapse frequency in certain photoreceptors of the honeybee after chromatic deprivation

Bees reared under UV-light are less sensitive to long wavelength light in phototaxis experiments than are control bees. Electroretinogram measurements indicate that selective reduction in spectral sensitivity is related to smaller lamina potentials to green light. Histological investigation of synapse frequency of green sensitive photoreceptor terminals reveal a decrease in number of synapses due to the selective wavelength deprivation.

The Cockroach DCMD Neurone

ABSTRACT The projections and response properties of a bilateral pair of large visual interneurones in the cockroach Periplaneta are described. The cells are shown to be analogous to the DCMD neurones of locust (Rowell, 1971a). The organization of the afferent input to the cockroach DCMD was explored by examining the response to different types of visual stimuli. The afferent input is organized into an array of parallel channels. Response habitutation occurs within each channel independently of habituation in other channels. The dynamics of habituation and recovery from habituation were examined. A simple model based on these data is proposed that can predict the DCMD response to repetitive stimuli having a wide range of interstimulus intervals. The relation of this model to models of synaptic depression is discussed. Both u.v.-sensitive and green-sensitive photoreceptors in the eye provide input to the DCMD, but this cell remains unable to detect colour.