Spectral responses and chromatic processing in the dragonfly lamina

The dragonfly Hemicordulia tau has five spectral classes of photoreceptor which drive five lamina monopolars, m1-m5. The monopolars encode spectral information. Here, spectral coding by m2, m4 and m5 are described. m2 is the most sensitive to dim light. m4 and m5 are less sensitive than m2, and so we call them photopic cells. The effects of selective adaptation of receptor inputs to m4 and m5 are unusual. For example, in m4 adaptation of the green receptor suppresses the UV input, but green sensitivity is unaffected, while green adaptation of m5 increases its green sensitivity. In m5 the dark adapted spectral tuning resembles the 520 nm receptor, but on adaptation to 430 nm light this narrows markedly. Adaptation either of green or of UV receptor input to m2 and m4 modifies the time course of responses both to green and to UV, implying that changes in the time courses of monopolar responses with adaptation state do not directly reflect receptor responses (Fig. 2). Finally, the antagonistic surround of m2 is UV sensitive, and of m4 green sensitive (Fig. 3).Abbreviations LMC large monopolar cell - LVF long visual fibre - rf receptive field - SVF short visual fibre     

Lateral ocellar nerve projections in the dragonfly brain

Summary The central projections of the lateral ocellar neurons of the dragonfly were examined using whole nerve cobalt iontophoresis, supplemented by sectioning of the nerve and brain for inspection in the light and electron microscopes. At E.M. level the presence of cobalt in filled axon profiles and cell bodies was confirmed by analysis of X-ray energy spectra in the microscope.The pathways, cell body sites and terminal arborizations of four large (7–25 m diameter) lateral ocellar neurons are described. Two of these fibers arborize in the ipsilateral posterior neuropil of the protocerebrum and two cross the brain and arborize in the contralateral posterior neuropil. Within each half of the posterior neuropil, two spatially separated regions of ocellar input have been identified. These regions receive median ocellar input plus input from either the ipsi- or contralateral ocellus, but not both. The arborizations of the contralateral fibers are more extensive than those of the ipsilateral fibers.One of the contralateral neurons crosses the brain in the region of the protocerebral bridge giving off a collateral in that region before descending to the posterior neuropil. This collateral arborizes almost immediately in a region receiving input from arborizations of a number of small ocellar neurons (those less than 5 m in diameter) from the ipsilateral ocellar nerve, together with small neurons from the median ocellar nerve, forming a region in each half of the brain which receives input from all three ocelli. The small lateral ocellar neurons associated with these arborizations have cell bodies adjacent to the lateral ocellar tracts.This work was supported in part by National Institute of Health Grants 2 RO1 EY-00777 and 1 KO4 EY-00040     

The number and arrangement of elements in the lamina cartridge of the dragonfly Sympetrum rubicundulum

Summary Five monopolar cells and two long visual fibres are a consistent component of the lamina cartridge of the ventral half of the eye of the dragonfly Sympetrum rubicundulum. They communicate with the chiasm via a cartridge axon bundle comprising a minimum of ten fibres. The arrangement of these elements is documented with respect to the ommatidial photoreceptor axon bundle innervating them. These relationships are described both within the lamina cortex and in the cross-section of the underlying cartridge.     

The dorsal eye of the dragonfly Sympetrum: specializations for prey detection against the blue sky

Dragonflies of the genus Sympetrum have compound eyes conspicuously divided into dorsal and ventral regions. Using anatomical, optical, electrophysiological, in-vivo photochemical and microspectrophotometrical methods, we have investigated the design and physiology of the dorsal part which is characterized by a pale yellow-orange screening pigment and extremely large facets. The upper part of the yellow dorsal region is a pronounced fovea with interommatidial angles approaching 0.3°, contrasting to the much larger values of 1.5°–2° in the rest of the eye. The dorsal eye part is exclusively sensitive to short wavelengths (below 520 nm). It contains predominantly blue-receptors with a sensitivity maximum at 420 nm, and a smaller amount of UV-receptors. The metarhodopsin of the blue-receptors absorbs maximally at 535 nm. The yellow screening pigment transmits longwavelength light (cut-on 580 nm), which increases the conversion rate from metarhodopsin to rhodopsin (see Fig. 11a). We demonstrate that because of the yellow pigment screen nearly all of the photopigment is in the rhodopsin state under natural conditions, thus maximizing sensitivity. Theoretical considerations show that the extremely long rhabdoms (1.1 mm) in the dorsal fovea are motivated for absorption reasons alone. A surprising consequence of the long rhabdoms is that the sensitivity gain, caused by pumping photopigment into the rhodopsin state, is small. To explain this puzzling fact we present arguments for a mechanism producing a gradient of rhodopsin concentration along the rhabdom, which would minimize saturation of transduction units, and hence improve the signal-to-noise ratio at high intensities. The latter is of special importance for the short integration time and high contrast sensitivity these animals need for spotting small prey at long distances.Abbreviations ERG electroretinogram - R rhodopsin - M metarhodopsin     

Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors

Birds have four spectrally distinct types of single cones that they use for colour vision. It is often desirable to be able to model the spectral sensitivities of the different cone types, which vary considerably between species. However, although there are several mathematical models available for describing the spectral absorption of visual pigments, there is no model describing the spectral absorption of the coloured oil droplets found in three of the four single cone types. In this paper, we describe such a model and illustrate its use in estimating the spectral sensitivities of single cones. Furthermore, we show that the spectral locations of the wavelengths of maximum absorbance (_max) of the short- (SWS), medium- (MWS) and long- (LWS) wavelength-sensitive visual pigments and the cut-off wavelengths (_cut) of their respective C-, Y- and R-type oil droplets can be predicted from the _max of the ultraviolet- (UVS)/violet- (VS) sensitive visual pigment.     

Characterisation of columnar neurons and visual signal processing in the medulla of the locust optic lobe by system identification techniques

We describe visual responses of seventeen physiological classes of columnar neuron from the retina, lamina and medulla of the locust (Locusta migratoria) optic lobe. Many of these neurons were anatomically identified by neurobiotin injection. Characterisation of neuronal responses was made by moving and flash stimuli, and by two system identification techniques: 1. The first-order spatiotemporal kernel was estimated from response to a spatiotemporal white-noise stimulus; 2. A set of kernels to second order was derived by the maximal-length shift register (M-sequence) technique, describing the system response to a two-channel centre-surround stimulus. Most cells have small receptive fields, usually with a centre diameter of about 1.5°, which is similar to that of a single receptor in the compound eye. Linear response components show varying spatial and temporal tuning, although lateral inhibition is generally fairly weak. Second-order nonlinearities often have a simple form consistent with a static nonlinear transformation of the input from the large monopolar cells of the lamina followed by further linear filtering.Abbreviations LMC large monopolar cell - LVF long visual fibre - RF receptive field - SMC small monopolar cell - SVF short visual fibre     

Identificaton of UV,green and red receptors,and their projection to lamina in the cabbage butterfly,Pieris rapae

Summary The photoreceptors in the compound eye of a cabbage butterfly, Pieris rapae, were examined by conventional and intracellular-labeling electron microscopy by the use of the cobalt(III)-lysine complex as an ionized marker. Five types of spectral sensitivity were recorded intracellularly in electrophysiological experiments. They peaked at about 340, 380, 480, 560 and 620 nm, respectively. One of the distal retinula cells (R2) was a UV receptor, whereas the R4 distal retinula cell was a green receptor. The basal retinula cell, R9, was found to be a red receptor; it was localized near the basement membrane, having a bilobed cell body with an individual nucleus in each lobe. A small number of rhabdomere microvilli were present in a narrow cytoplasmic bridge connecting the two lobes. The axons of six retinula cells (R3–R8) in each ommatidium terminated at the cartridge in the lamina (short visual fiber), whereas those of the other three retinula cells, R1, R2 and R9, extended to the medulla (long visual fiber). The information from the UV and red receptors is therefore probably delivered directly to the medulla neurons, independent of that from the other spectral receptor types.     

Localization of the pupil trigger in insect superposition eyes

Summary In the superposition eyes of the sphingid moth Deilephila and the neuropteran Ascalaphus, adjustment to different intensities is subserved by longitudinal migrations of screening pigment in specialized pigment cells. Using ophthalmoscopic techniques we have localized the light-sensitive trigger that controls pigment position.In both species, local illumination of a small spot anywhere within the eye glow of a dark-adapted eye evokes local light adaptation in the ommatidia whose facets receive the light. Details of the response pattern demonstrate that a distal light-sensitive trigger is located axially in the ommatidium, just beneath the crystalline cone, and extends with less sensitivity deep into the clear zone. The distal trigger in Deilephila was shown to be predominantly UV sensitive, and a UV-absorbing structure, presumably the distal trigger, was observed near the proximal tip of the crystalline cone.In Ascalaphus we also found another trigger located more proximally, which causes local pigment reaction in the ommatidia whose rhabdoms are illuminated (the centre of the eye glow). The light-sensitive trigger for this response appears to be the rhabdom itself.     

Interneuronal and glial-neuronal gap junctions in the lamina ganglionaris of the compound eye of the housefly,Musca domestics

Summary The cell-body layer of the lamina ganglionaris of the housefly, Musca domestica, contains the perikarya of five types of monopolar interneuron (L1–L5) along with their enveloping neuroglia (Strausfeld 1971). We confirm previous reports (Trujillo-Cenóz 1965; Boschek 1971) that monopolar cell bodies in the lamina form three structural classes: Class I, Class II, and midget monopolar cells. Class-I cells (L1 and L2) have large (8–15 m) often crescentshaped cell bodies, much perinuclear cytoplasm and deep glial invaginations. Class-II cells (L3 and L4) have smaller perikarya (4–8 m) with little perinuclear cytoplasm and no glial invaginations. The midget monopolar cell (L5) resides at the base of the cell-body layer and has a cubshaped cell body. Though embedded within a reticulum of satellite glia, the L1–L4 monopolar perikarya and their immediately proximal neurites frequently appose each other directly. Typical arthropod (-type) gap junctions are routinely observed at these interfaces. These junctions can span up to 0.8 m with an intercellular space of 2–4 nm. The surrounding nonspecialized interspace is 12–20 nm. Freezefracture replicas of monopolar appositions confirm the presence of -type gap junctions, i.e., circular plaques (0.15–0.7 m diam.) of large (10–15 nm) E-face particles. Gap junctions are present between Class I somata and their proximal neurites, between Class I and Class II somata and proximal neurites, and between Class II somata. Intercartridge coupling may exist between such monopolar somata. The cell body and proximal neurite of L5 were not examined. We also find that Class I and Class II somata are extensively linked to their satellite glia via gap junctions. The gap width and nonjunctional interspace between neuron and glia are the same as those found between neurons. The particular arrangement and morphology of lamina monopolar neurons suggest that coupling or low resistance pathways between functionally distinct neurons and between neuron and glia are probably related to the metabolic requirements of the nuclear layer and may play a role in wide field signal averaging and light adaptation.     

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 10nm 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.     

Spectral organization of the eye of a butterfly,Papilio

Journal of Comparative Physiology A - This review outlines our recent studies on the spectral organization of butterfly compound eyes, with emphasis on the Japanese yellow swallowtail butterfly,...     

Spectral sensitivities of photoreceptors and their role in colour discrimination in the green-backed firecrown hummingbird (<Emphasis Type="Italic">Sephanoides sephaniodes</Emphasis>)

We studied the photopic spectral sensitivity in the green-backed firecrown, Sephanoides sephaniodes, a South American hummingbird, and its possible ecological relationship with preferred flowers and body colouration. Avian colour vision is in general tetrachromatic with at least four types of cones, which vary in sensitivity from the near ultraviolet (UV) to the red wavelength range. Hummingbirds represent an important family of birds, yet little is known about their eye sensitivity, especially about the role of photoreceptors and their oil droplet complements. The photopic electroretinogram shows a main sensitivity peak at 560 nm and a secondary peak in the UV, and may be explained by the presence of four single cones (lambda (max) at ~370, 440, 508 and 560 nm), and a double cone (lambda (max) at 560 nm) screened by oil droplets. The flowers preferred by the firecrown are those in which the red-green wavelength region predominates and have higher contrast than other flowers. The crown plumage of males is highly iridescent in the red wavelength range (peak at 650 nm) and UV; when plotted in a high-dimensional tetrachromatic space, it falls in a "red + UV" purple hue line, suggesting a potential significant communication signal for sexual differentiation.     

Evolution of color vision in pierid butterflies: blue opsin duplication,ommatidial heterogeneity and eye regionalization in <Emphasis Type="Italic">Colias erate</Emphasis>

This paper documents the molecular organization of the eye of the Eastern Pale Clouded Yellow butterfly, Colias erate (Pieridae). We cloned four cDNAs encoding visual pigment opsins, corresponding to one ultraviolet, two blue and one long wavelength-absorbing visual pigments. Duplication of the blue visual pigment class occurs also in another pierid species, Pieris rapae, suggesting that blue duplication is a general feature in the family Pieridae. We localized the opsin mRNAs in the Colias retina by in situ hybridization. Among the nine photoreceptor cells in an ommatidium, R1-9, we found that R3-8 expressed the long wavelength class mRNA in all ommatidia. R1 and R2 expressed mRNAs of the short wavelength opsins in three fixed combinations, corresponding to three types of ommatidia. While the duplicated blue opsins in Pieris are separately expressed in two subsets of R1-2 photoreceptors, one blue sensitive and another violet sensitive, those of Colias appear to be always coexpressed.     

Spectral sensitivity of the photonegative reaction of the blood-sucking bug Triatoma infestans (Heteroptera: Reduviidae)

We studied the spectral sensitivity of the visual system of the blood-sucking bug Triatoma infestans, one of the main vectors of Chagas Disease in South America. We quantified the photonegative reaction of this insect in a rectangular arena, half of which was kept dark and the other half illuminated with various intensities of different monochromatic lights (or broadband stimuli for λ>665 nm). As a behavioral parameter of the photonegative response, we measured the time each insect spent in the dark half of the arena. We found that low intensity levels (under 0.06 μW/cm²) of monochromatic lights of 397, 458, 499, and 555 nm evoked a statistically significant (i.e., different from that of control groups) photonegative reaction. Insects were less sensitive to monochromatic lights of 357 nm (UV) and 621 nm (dark orange), and to broadband stimuli in the red part of the spectrum (665–695 nm). These findings indicate that the visual system of T. infestans is sensitive to broader regions of the spectrum than those previously reported.     

Optic lobes of the larval and imaginal scorpionfly Panorpa vulgaris (Mecoptera,Panorpidae): A neuroanatomical study of neuropil organization,retinula axons,and lamina monopolar cells

Panorpa larvae possess stemmata (lateral ocelli), which have the structure of compound eyes, and stemma lamina and stemma medulla neuropils. A distinct lobula neuropil is lacking. The stemma neuropils have a columnar organization. They contain lamina monopolar cells, and both short and long visual fibers. All the identified larval monopolar neurons have radially arranged dendrites along the entire depth of the lamina neuropil and a single terminal arborization within the medulla (L1/L2-type). The terminals of visual fibers have short spiny lateral projections. Long fibers possess en passant synapses within the lamina. The same principles of organization of first and second order visual neuropils are found in Panorpa imagines. In contrast to the larvae, a lobula neuropil is present. Adults have monopolar cells of the L1-type that are similar to the L1-neurons found in Diptera. The columnar organization, the presence of short and long visual fibers, and lamina monopolar neurons are thus features common to both visual systems, viz., the larval (stemmata) and the imaginal (compound eyes).     

Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae)

Sexual communication between male and female fireflies involves the visual detection of species-specific bioluminescent signals. Firefly species vary spectrally in both their emitted light and in the sensitivity of the eye, depending on the time when each is active. Tuning of spectral sensitivity in three firefly species that occupy different photic niches was investigated using light and electron microscopy, microspectrophotometry, and intracellular recording to characterize the location and spectral absorption of the screening pigments that filter incoming light, the visual pigments that receive this filtered light, and the visual spectral sensitivity. Twilight-active species had similar pink screening pigments, but the visual pigment of Photinus pyralis peaked near 545 nm, while that of P. scintillans had a λ_max near 557 nm. The night-active Photuris versicolor had a yellow screening pigment that was uniquely localized, while its visual pigment was similar to that of P. pyralis. These results show that both screening and visual pigments vary among species. Modeling of spectral tuning indicates that the combination of screening and visual pigments found in the retina of each species provides the best possible match of sensitivity to bioluminescent emission. This combination also produced model sensitivity spectra that closely resemble sensitivities measured either with electroretinographic or intracellular techniques. Vision in both species of Photinus appears to be evolutionarily tuned for maximum discrimination of conspecific signals from spectrally broader backgrounds. Ph. versicolor, on the other hand, appears to have a visual system that offers a compromise between maximum sensitivity to, and maximum discrimination of, their signals. Accepted: 29 September 1999     

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