The spectral sensitivity of eye movements in response to light flashes inDaphnia magna

Summary The crustaceanDaphnia magna responds to a flash of light with a ventral rotation of its compound eye; this behavior is termed eye flick. We determined the spectral sensitivity for the threshold of eye flick in response to light flashes having three different spatial characteristics: (1) full-field, extending 180° from dorsal to ventral in the animal's field of view; (2) dorsal, 30° wide and located in the dorsal region of the visual field; (3) ventral, same as dorsal but located ventrally. All three stimuli extended 30° to the right and to the left of the animal's midplane. We found that spectral sensitivity varies with the spatial characteristics of the stimulus. For full-field illumination, the relative sensitivity was maximal at 527 nm and between 365 nm and 400 nm, with a significant local minimum at 420 nm. For the dorsal stimulus, the relative sensitivity was greatest at 400 nm, but also showed local maxima at 440 nm and 517 nm. For the ventral stimulus, the relative sensitivity maxima occurred at the same wavelengths as those for the full-field stimulus. At wavelengths of 570 nm and longer, the responses to both dorsal and ventral stimuli showed lower relative sensitivity than the full-field stimulus. No circadian or other periodic changes in threshold spectral sensitivity were observed under our experimental conditions. Animals which had their nauplius eyes removed by means of laser microsurgery had the same spectral sensitivity to full-field illumination as normal animals. Our results are discussed in terms of our current knowledge of the spectral classes of photoreceptors found in theDaphnia compound eye.     

The Components of the Visual System of a Dragonfly

In this study of the electroretinograms of dragonflies (adults and nymphs) the objectives were to determine the number of classes of photoreceptors present in the visual system and to allocate these to particular morphological regions. There are probably five classes of photoreceptors present with peak sensitivities near 550, 530, 518, 420, and < 380 mµ. The dorsal ocelli contain two classes (518 mµ and < 380 mµ). The ventral (anterior) ommatidia of the adult compound eye contain at least two classes (near 518 mµ and < 380 mµ) and probably a third class (near 550 mµ). The dorsal ommatidia of the adult compound eye contain one class (420 mµ) and possibly another class (< 380 mµ). The compound eye of the nymph contains one class (530 mµ) and possibly another class (420 mµ).     

Blue and double-peaked green receptors depend on ommatidial type in the eye of the Japanese yellow swallowtail Papilio xuthus

The compound eye of the butterfly Papilio xuthus is composed of three spectrally distinct types of ommatidia. We investigated the blue and double-peaked green receptors that are encountered distally in type I and III ommatidia, by means of intracellular recordings, in vivo fluorescence microscopy, and histology. The blue receptors are R1 and/or R2 photoreceptors; they contain the same mRNA encoding the opsin of the blue-absorbing visual pigment. However, here we found that the sensitivity in the UV wavelength region strongly depends on the ommatidial type; the blue receptors in type I ommatidia have a distinctly depressed UV sensitivity, which is attributed to lateral filtering in the fused rhabdom. In the main, fronto-ventral part of the eye, the R3 and R4 photoreceptors of all ommatidia contain the same set of two mRNAs encoding the opsins of green-absorbing visual pigments, PxL1 and PxL2. The spectral sensitivities are double-peaked, but the UV sensitivity of the R3 and R4 photoreceptors in type I ommatidia appears to be reduced, similar to that of the co-localized blue receptors.     

The POL area of the honey bee's eye: behavioural evidence

ABSTRACT. The uppermost dorsal part of the honey bee's compound eye contains a group of c. 150 specialized ommatidia. The photoreceptors of these ommatidia are characterized by a number of anatomical and physiological peculiarities which suggest that they have functional significance for the detection of polarized skylight. Here, we show by painting out different parts of the eye and recording the bee's behavioural responses that the specialized photoreceptors at the dorsal margin of the eye are indeed necessary for detecting polarized skylight and deriving compass information from celestial e-vector patterns. Hence, this group of specialized ommatidia can be called the POL area of the bee's compound eye.     

Microvillar orientation in the photoreceptors of the ant Cataglyphis bicolor

Polarization sensitivity in arthropod photoreceptors is crucially dependent on the arrangement of the microvilli within the rhabdom. Here, we present an electron-microscopical study in which the degree of microvillar alignment and changes in the cross-sectional areas of the rhabdoms along their length were studied in the compound eye of the desert ant, Cataglyphis bicolor. Serial cross-sections through the retina were taken and the orientation of the microvilli was determined in the photoreceptors of individually identified ommatidia. The reconstructions of microvillar alignment were made in the three anatomically and functionally distinct regions of the Cataglyphis compound eye: the dorsal rim area (DRA), the dorsal area (DA), and the ventral area (VA). The following morphological findings are consistent with polarization sensitivities measured previously by intracellular recordings. (1) The microvilli of the DRA photoreceptors are aligned in parallel along the entire length of the cell from the distal tip of the rhabdom down to its proximal end, near the basement membrane. The microvilli of the retinular cells R1 and R5 are always parallel to each other and perfectly perpendicular, with only minor deviation, to the microvillar orientation of the remaining receptor cells. (2) In the DA and VA regions of the eye, the microvillar tufts of the small receptors R1, R3, R5, R7, and R9 change their direction repetitively every 1-4 7m for up to 90°. In contrast, the large receptor cells R2, R4, R6, and R8 maintain their microvillar orientation rigidly. (3) In the DRA ommatidia, the cross-sectional areas of the rhabdomeres do not change along the length of the rhabdom, but substantial changes occur in the DA and VA ommatidia.     

Coexpression of spectrally distinct rhodopsins in Aedes aegypti R7 photoreceptors

The retina of the mosquito Aedes aegypti can be divided into four regions based on the non-overlapping expression of a UV sensitive Aaop8 rhodopsin and a long wavelength sensitive Aaop2 type rhodopsin in the R7 photoreceptors. We show here that another rhodopsin, Aaop9, is expressed in all R7 photoreceptors and a subset of R8 photoreceptors. In the dorsal region, Aaop9 is expressed in both the cell body and rhabdomere of R7 and R8 cells. In other retinal regions Aaop9 is expressed only in R7 cells, being localized to the R7 rhabdomere in the central and ventral regions and in both the cell body and rhabdomere within the ventral stripe. Within the dorsal-central transition area ommatidia do not show a strict pairing of R7-R8 cell types. Thus, Aaop9 is coexpressed in the two classes of R7 photoreceptors previously distinguished by the non-overlapping expression of Aaop8 and Aaop2 rhodopsins. Electroretinogram analysis of transgenic Drosophila shows that Aaop9 is a short wavelength rhodopsin with an optimal response to 400-450 nm light. The coexpressed Aaop2 rhodopsin has dual wavelength sensitivity of 500-550 nm and near 350 nm in the UV region. As predicted by the spectral properties of each rhodopsin, Drosophila photoreceptors expressing both Aaop9 and Aaop2 rhodopsins exhibit a uniform sensitivity across the broad 350-550 nm light range. We propose that rhodopsin coexpression is an adaptation within the R7 cells to improve visual function in the low-light environments in which Ae. aegypti is active.     

Photoreceptor spectral sensitivities of the Small White butterfly <Emphasis Type="Italic">Pieris rapae crucivora</Emphasis> interpreted with optical modeling

The compound eye of the Small White butterfly, Pieris rapae crucivora, has four classes of visual pigments, with peak absorption in the ultraviolet, violet, blue and green, but electrophysiological recordings yielded eight photoreceptors classes: an ultraviolet, violet, blue, double-peaked blue, green, blue-suppressed-green, pale-red and deep-red class. These photoreceptor classes were identified in three types of ommatidia, distinguishable by the different eye shine spectra and fluorescence; the latter only being present in the eyes of males. We present here two slightly different optical models that incorporate the various visual pigments, the light-filtering actions of the fluorescent, pale-red and deep-red screening pigment, located inside or adjacent to the rhabdom, and the reflectance spectrum of the tapetum that abuts the rhabdom proximally. The models serve to explain the photoreceptor spectral sensitivities as well as the eye shine.     

Spectral sensitivities of retinular cells measured in intact,living flies by an optical method

Summary The spectral sensitivity of the peripheral retinular cells R1–6 in nine species of intact flies was determined using non-invasive, optical measurements of the increase in reflectance that accompanies the pupillary response. Our technique is to chronically illuminate a localized region of the eye with a long wavelength beam, adjusted to bring pupillary scattering above threshold, then, after stabilization, to stimulate with monochromatic flashes. A criterion increase in scattering is achieved at each wavelength by adjusting flash intensity. Univariance of the pupillary response is demonstrated by Fig. 3.Action spectra measured with this optical method are essentially the same as the published spectral sensitivity functions measured with intracellular electrophysiological methods (Fig. 4 forCalliphora, Fig. 5 forDrosophila, Fig. 7 forEristalis, and Fig. 8 forMusca). This holds for both the long wavelength peak and the high sensitivity in the UV as was consistently found in all investigated fly species.Spectral sensitivity functions for R1–6 of hover flies (family Syrphidae) are quite different in different regions of the same eye. There can also be substantial differences between the two sexes of the same species. The ventral pole of the eye of femaleAllograpta (Fig. 10) contains receptors with a major peak at 450 nm, similar to those ofEristalis. However, the dorsal pole of the same eye contains receptors with a major peak at 495 nm, similar to those ofCalliphom. Both dorsal and ventral regions of the maleToxomerus eye, and the ventral region of the female eye, contain only the 450 nm type of R1-6 (see Fig. 12). However, the dorsal region of the female eye also contains another spectral type of receptor that is maximally sensitive at long wavelength. Eyes of both sexes ofAllograpta (Figs. 10 and 11) contain a mixture of spectral types of receptors R1-6.We thank Dr. Chris Maier of the Connecticut Agricultural Experiment Station, for determination of the Syrphidae. This work was supported by grants EY01140 and EY00785 from the National Eye Institute, U.S.P.H.S., (to GDB), by the Connecticut Lions Eye Research Foundation (to GDB), and by the Netherlands Organization for the Advancement of Pure Research (Z.W.O.), (to DGS).     

Sexual Dimorphism in the Compound Eye of Rhagophthalmus ohbai (Coleoptera: Rhagophthalmidae): II. Physiology and Function of the Eye of the Male

The eyes of male and female Rhagophthalmus ohbai are of very different sizes and possess approximately 3000 and 35 facets, respectively. In the male eye one can distinguish a smaller dorsal region with 500 facets and a larger ventral one with ca. 1800. Ultrastructural differences between them have been described earlier in this journal (Lau and Meyer-Rochow, 2006). Electrophysiological recordings from the two eye areas have now revealed that the ventral region is maximally sensitive to light of 600 nm wavelength, while the dorsal eye region responds maximally to light of 540–560 nm wavelengths. In the dorsal eye region sensitivity to UV-radiation at around 360 nm wavelength, being twice as high as that of the ventral eye region, amounted to ca. one quarter of peak wavelength sensitivity. The regional differences in spectral sensitivity seem to be a reflection of the different tasks of the two eye regions: looking downward to see the yellow light emitted by a female, sensitivity towards longer wavelengths would be advantageous, but looking upward into the twilight sky, sensitivity to shorter wavelength would be a more appropriate adaptation.     

Distribution of photoperiodic receptors in the compound eyes of the bean bug, Riptortus clavatus

  The bean bug, Riptortus clavatus shows a long-day photoperiodic response with respect to the control of adult diapause. The location of photoreceptors for photoperiodism was examined in this species by complete or partial removal of photoreceptor organs. Even after one compound eye or both ocelli were removed, the insects were sensitive to photoperiod. After both compound eyes were removed, however, the insects became reproductive regardless of the photoperiod. Therefore, photoreceptors for photoperiodism were not in the ocelli but in the compound eyes. To clarify whether ommatidia in compound eyes have a regional difference in reception of photoperiod, sensitivity to photoperiod was examined after one compound eye and a part of the contralateral one were removed. Only when the central region of compound eyes was removed did the insects lose sensitivity to photoperiod. It is concluded that the ommatidia in the central region of compound eyes play a principal role in the reception of photoperiod. Accepted: 23 September 1996     

Photoreceptor projection and termination pattern in the lamina of gonodactyloid stomatopods (mantis shrimp)

The apposition compound eyes of gonodactyloid stomatopods are divided into a ventral and a dorsal hemisphere by six equatorial rows of enlarged ommatidia, the mid-band (MB). Whereas the hemispheres are specialized for spatial vision, the MB consists of four dorsal rows of ommatidia specialized for colour vision and two ventral rows specialized for polarization vision. The eight retinula cell axons (RCAs) from each ommatidium project retinotopically onto one corresponding lamina cartridge, so that the three retinal data streams (spatial, colour and polarization) remain anatomically separated. This study investigates whether the retinal specializations are reflected in differences in the RCA arrangement within the corresponding lamina cartridges. We have found that, in all three eye regions, the seven short visual fibres (svfs) formed by retinula cells 1–7 (R1–R7) terminate at two distinct lamina levels, geometrically separating the terminals of photoreceptors sensitive to either orthogonal e-vector directions or different wavelengths of light. This arrangement is required for the establishment of spectral and polarization opponency mechanisms. The long visual fibres (lvfs) of the eighth retinula cells (R8) pass through the lamina and project retinotopically to the distal medulla externa. Differences between the three eye regions exist in the packing of svf terminals and in the branching patterns of the lvfs within the lamina. We hypothesize that the R8 cells of MB rows 1–4 are incorporated into the colour vision system formed by R1–R7, whereas the R8 cells of MB rows 5 and 6 form a separate neural channel from R1 to R7 for polarization processing.This research was supported by the Swiss National Science Foundation (PBSKB-104268/1), the Australian Research Council (LP0214956) and the American Air Force (AOARD/AFOSR) (F62562-03-P-0227).     

Anatomical and physiological evidence for polarisation vision in the nocturnal bee <Emphasis Type="Italic">Megalopta genalis</Emphasis>

The presence of a specialised dorsal rim area with an ability to detect the e-vector orientation of polarised light is shown for the first time in a nocturnal hymenopteran. The dorsal rim area of the halictid bee Megalopta genalis features a number of characteristic anatomical specialisations including an increased rhabdom diameter and a lack of primary screening pigments. Optically, these specialisations result in wide spatial receptive fields (Δρ = 14°), a common adaptation found in the dorsal rim areas of insects used to filter out interfering effects (i.e. clouds) from the sky. In this specialised eye region all nine photoreceptors contribute their microvilli to the entire length of the ommatidia. These orthogonally directed microvilli are anatomically arranged in an almost linear, anterior–posterior orientation. Intracellular recordings within the dorsal rim area show very high polarisation sensitivity and a sensitivity peak within the ultraviolet part of the spectrum.     

The structures of dorsal and ventral regions of a dragonfly retina

Summary The apposition eyes of the corduliid dragonfly Hemicordulia tau are each divided by pigment colour, facet size and facet arrangement into three regions: dorsal, ventral, and a posterior larval strip. Each ommatidium has two primary pigment cells, twenty-five secondary pigment cells, and eight receptor cells, all surrounded by tracheae which probably prevent light passing between ommatidia, and reduce the weight of the eye. Electron microscopy reveals that the receptor cells are of two types: small vestigial cells making virtually no contribution to the rhabdom, and full-size typical cells. The ventral ommatidia have a distal typical cell (oriented either horizontally or vertically), four medial typical cells, two proximal typical cells and one full-length vestigial cell. The dorsal ommatidia have only four full-length typical cells, and one distal and three vestigial full-length cells. The cross-section of dorsal rhabdoms is small and circular distally, but expands to a large three-pointed star medially and proximally. The tiered receptor arrangement in the ventral ommatidia is typical of other Odonata but the dorsal structure has not been fully described in other species. Specialised dorsal eye regions are typical of insects that detect others against the sky.     

The photoreceptor localization confirms the spectral heterogeneity of ommatidia in the male small white butterfly,<Emphasis Type="Italic"> Pieris rapae crucivora</Emphasis>

The compound eye of Pieris rapae crucivora contains ventrally three types of histologically distinct ommatidia. An ommatidium contains nine photoreceptors, four of which (R1-4) construct the distal tier of the rhabdom. We determined the sensitivity spectra of the R1-4 distal photoreceptors in each type of ommatidia by intracellular electrophysiology and identified UV, blue, double-peaked blue, green, and a green receptor with depressed sensitivity in the violet. We localized these receptors in each type of ommatidia by injecting dye after the recording. In type I ommatidia the R1 and R2 cells are UV and blue receptors. When R1 is UV sensitive, R2 is always blue sensitive, or vice versa. R3 and R4 in type I are both green receptors. In type II, R1 and R2 are both double-peaked blue receptors and R3 and R4 are both green receptors with depressed sensitivity in the violet. In type III, R1 and R2 are both UV, and R3 and R4 are green receptors. The double-peaked blue, and green receptors with depressed sensitivity in the violet in type II ommatidia have depressed sensitivity at 420 nm, which is probably due to the filtering effect of a fluorescing material present in the type II ommatidia. Spectral heterogeneity of ommatidia seems to be a common design of insect compound eyes.     

Morphological specializations of dorsal rim ommatidia in the compound eye of dragonflies and damselfies (Odonata)

We have examined the fine structure of dorsal rim ommatidia in the compound eye of the three odonate species Sympetrum striolatum, Aeshna cyanea and Ischnura elegans. These ommatidia exhibit several specializations: (1) the rhabdoms are very short, (2) there is no rhabdomeric twist, and (3) the rhabdoms contain only two, orthogonally-arranged microvillar orientations. The dorsal rim ommatidia of several other insect species are known to be anatomically specialized in a similar way and to be responsible for polarization vision. We suggest that the dorsal rim area of the odonate compound eye plays a similar role in polarization vision. Since the Odonata are a primitive group of insects, the use of polarized skylight for navigation may have developed early in insect phylogeny.     

Specialized ommatidia of the polarization-sensitive dorsal rim area in the eye of monarch butterflies have non-functional reflecting tapeta

Many insects exploit sky light polarization for navigation or cruising-course control. The detection of polarized sky light is mediated by the ommatidia of a small specialized part of the compound eye: the dorsal rim area (DRA). We describe the morphology and fine structure of the DRA in monarch butterflies (Danaus plexippus). The DRA consists of approximately 100 ommatidia forming a narrow ribbon along the dorsal eye margin. Each ommatidium contains two types of photoreceptor with mutually orthogonal microvilli orientations occurring in a 2:6 ratio. Within each rhabdomere, the microvilli are well aligned. Rhabdom structure and orientation remain constant at all retinal levels, but the rhabdom profiles, as seen in tangential sections through the DRA, change their orientations in a fan-like fashion from the frontal to the caudal end of the DRA. Whereas these properties (two microvillar orientations per rhabdom, microvillar alignment along rhabdomeres, ommatidial fan array) are typical for insect DRAs in general, we also report and discuss here a novel feature. The ommatidia of monarch butterflies are equipped with reflecting tapeta, which are directly connected to the proximal ends of the rhabdoms. Although tapeta are also present in the DRA, they are separated from the rhabdoms by a space of approximately 55 μm effectively inactivating them. This reduces self-screening effects, keeping polarization sensitivity of all photoreceptors of the DRA ommatidia both high and approximately equal.     

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

Summary 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.     

Spectral sensitivity of the compound eye in butterflies (Heliconius)

Summary The spectral sensitivity of the compound eye in three butterfly species (Heliconius erato, H. numata, H, sara) was tested electrophysiologically in the wavelength region 310 to 650 nm. Sensitivity maxima were found at 370 to 390 nm, 450 to 470 nm, and 550 to 570 nm, for all species. The three sensitivity maxima are suggested to be due to different photoreceptor types effecting wave-length discrimination. An interspecies difference in spectral sensitivity was also found. The difference is suggested to be due to the relative number of photoreceptors of each type. In some of the present experiments a small discontinuity in sensitivity was found at 610 or 630 nm. It is probably caused by a selective reflection of these wavelengths from a tapetum.     

Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye

We made intracellular recordings from the photoreceptors of the polarisation-sensitive dorsal rim area of the cricket compound eye combined with dye marking. By measuring visual field sizes and optical axes in different parts of the dorsal rim area, we assessed the optical properties of the ommatidia. Due to the large angular sensitivities (median about 20°) and the high sampling frequency (about 1 per degree), the visual fields overlap extensively, such that a given portion of the sky is viewed simultaneously by a large number of ommatidia. By comparing the dye markings in the retina and in the optic lobe, the axon projections of the retinula cells were examined. Receptors R1, R2, R5 and R6 project to the lamina, whereas R7 projects to the medulla. The microvilli orientation of the two projection types differ by 90° indicating the two analyser channels that give antagonistic input to polarisation-sensitive interneurons. Using the retinal marking pattern as an indicator for the quality of the intracellular recordings, the polarisation sensitivity of the photoreceptors was re-examined. The polarisation sensitivity of recordings from dye-coupled cells was much lower (median: 4.5) than that of recordings in which only one cell was marked (median: 9.8), indicating that artefactual electrical coupling between photoreceptors can significantly deteriorate polarisation sensitivity. The physiological value of polarisation sensitivity in the cricket dorsal rim area is thus typically about 10. Accepted: 4 November 1999