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The Journal of Neuroscience, June 1, 2003, 23(11):4527-4532
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Coexpression of Two Visual Pigments in a Photoreceptor Causes an Abnormally Broad Spectral Sensitivity in the Eye of the Butterfly Papilio xuthus
Kentaro Arikawa,1 Shin Mizuno,1 Michiyo Kinoshita,1 andDoekele G. Stavenga2 1 Graduate School of Integrated Science, Yokohama City University, Yokohama 236-0027, Japan, and 2 Department of Neurobiophysics, University of Groningen, 9747 AG, Groningen, The Netherlands
Abstract
Top
Abstract
Introduction
The compound eye of the butterfly Papilio xuthus consists of three different types of ommatidia, each containing nine photoreceptor cells (R1–R9). We have found previously that the R5–R8 photoreceptors of type II ommatidia coexpress two different mRNAs, encoding opsins of green- and orange-red-absorbing visual pigments (Kitamoto et al., 1998). Do these cells contain two functionally distinct visual pigments? First, we identified the sensitivity spectrum of these photoreceptors by using combined intracellular recording and dye injection. We thus found that the R5–R8 of type II ommatidia have a characteristic sensitivity spectrum extending over an excessively broad spectral range, from the violet to the red region; the photoreceptors are therefore termed broadband photoreceptors. The spectral shape was interpreted with a computational model for type II ommatidia, containing a UV visual pigment in cells R1 and R2, two green visual pigments in cells R3 and R4, a far-UV-absorbing screening pigment (3-hydroxyretinol) in the distal part of the ommatidium, and a red-screening pigment that surrounds the rhabdom. The modeling suggests that both visual pigments in the R5–R8 photoreceptors participate in phototransduction. This work provides the first compelling evidence that multiple visual pigments participate in phototransduction in single invertebrate photoreceptors.
Key words: vision; color; optical filters; insects; rhodopsin; signal transduction
Introduction
It is a generally accepted concept in vision research that single photoreceptors contain a single type of visual pigment. However, recent studies have demonstrated that some photoreceptors violate this dogma: they coexpress multiple visual pigments (Roehlich et al., 1994In the course of studies on the color vision of the butterfly Papilio xuthus, we discovered that some photoreceptors coexpress two mRNAs encoding different visual pigment opsins (Kitamoto et al., 1998
An ommatidium of Papilio contains nine photoreceptors (R1–R9) (see Fig. 1a). The rhabdomeres of the photoreceptors, harboring the visual pigments, together form the fused rhabdom, a cylindrical structure that acts as an optical waveguide. Clusters of either red or yellow pigment, lining the rhabdom (see Fig. 1b) (perirhabdomeral pigmentation), act as filters of light propagating along the rhabdom. According to the pigmentation, Papilio ommatidia can be divided into three types: type I are strongly red pigmented and nonfluorescent, type II are pale-red pigmented and emit a whitish fluorescence under UV light (see Fig. 1c), and type III are yellow pigmented and nonfluorescent (Arikawa and Stavenga, 1997
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Figure 1. Anatomy of the compound eye of P. xuthus; the dorsal side corresponds to the top edge of the micrographs. a, Diagram of three types of ommatidia (from left to right, types I–III). Each ommatidium contains nine photoreceptors, R1–R9 (1–9). R1–R4 are distal photoreceptors, which form the distal two-thirds of the rhabdom; R5–R8 are proximal photoreceptors, forming the proximal one-third of the rhabdom; and R9 is a basal cell. R1 and R2 contain distally purple pigment granules (distal pigment). Types I and II have red pigmentation around the rhabdom, whereas type III has yellow pigmentation (perirhabdomeral pigment). In type II, a fluorescing pigment, 3-hydroxyretinol, is concentrated in the distal portion of the photoreceptor layer (indicated by blue). b, Transverse, unstained section through the proximal tier of the retina, showing red (black arrowhead; type I or II ommatidium) or yellow (white arrowhead; type III ommatidium) pigmentation around the rhabdom. c, UV-induced fluorescence caused by 3-hydroxyretinol marks the type II ommatidia (from eye in intact, living animal). d, e, In situ hybridization of PxL2 (green-absorbing visual pigment) (d) and PxL3 (orange-red-absorbing visual pigment) (e) mRNA in adjacent sections through the proximal tier. R5–R8 are exclusively labeled with either the PxL2 probes (solid circles; type III) or the PxL3 probe (dotted circles; type I). R5–R8 of type II ommatidia are labeled by both PxL2 and PxL3 probes (dashed circles). The table is a summary of the characteristics of the three ommatidial types. In addition to the perirhabdomeral pigmentation and the autofluorescence, it presents the spectral sensitivity of the photoreceptors [S( )] and the visual pigment opsins expressed in the ventral half of the eye. V, Violet; B, blue; DG, double-peakedgreen; SG, single-peakedgreen; R, red; BB, broadband. The sensitivity spectrum of R9 photoreceptors is an open question; it probably peaks in the orange wavelength range, but electrophysiological data are lacking so far. For details of S(
We found five classes of spectral receptors in the Papilio retina, peaking in the UV, violet, blue, green, and red wavelength regions (Arikawa et al., 1987
In our early recordings, we had encountered units with broad sensitivity spectra. We initially considered that they might originate from multiple photoreceptors, artificially coupled because of low-quality penetrations. However, detailed analysis of the units, combining electrophysiology, histology, and computational modeling, provided evidence that the recordings were in fact from single R5–R8 photoreceptors of type II ommatidia. In this report, we present the results that led to this conclusion, and we will argue that both PxL2 and PxL3 are physiologically active in these photoreceptors.
Materials and Methods
Animals. Spring-form males of the Japanese yellow swallowtail butterfly P. xuthus were used within 3 d of emergence. The butterflies were reared on fresh citrus leaves at 25°C under an 8/16 hr light/dark cycle. The pupae were stored at 4°C for at least 3 months and then allowed to emerge at 25°C.We restricted the following analysis to the ventral two-thirds of the retina, because in the dorsal one-third, the cornea fluoresces under UV illumination, which obscures the ommatidial fluorescence in type II ommatidia. Type II ommatidia are presumably absent in the dorsal region (Arikawa and Stavenga, 1997
Electrophysiology. A butterfly whose wings and legs were removed was fixed on a plastic stage with its dorsal side up and then mounted in the electrophysiological setup in a Faraday cage. A silver wire inserted in the stump of an antenna served as the indifferent electrode. To insert a glass micropipette into the eye, a hole covering
10–20 facets was made in the dorsal region of the eye with a razor blade.
Monochromatic light stimuli were provided by a 500 W xenon arc lamp through 22 narrow-band interference filters ranging from 300 to 700 nm. The intensity of the light stimulus was attenuated with neutral-density filters and an optical wedge with a range of 4 log units. The light was focused on the tip of an optical fiber that led the light into the cage. The other end of the optical fiber was attached to a Cardan arm perimeter device, where it provided a point source of light (1.6° in diameter). The quantum flux of each monochromatic stimulus was measured by a radiometer (model 470D; Sanso, Tokyo, Japan), and the maximum quantum flux of each monochromatic stimulus at the corneal surface was adjusted with another optical wedge to 5.0 x 1011 photons·cm-2·sec-1 (
A glass micropipette filled with 5% Lucifer yellow aqueous solution (resistance,
) was inserted into the retina through the hole made in the cornea. A successful penetration of a photoreceptor cell was deduced from a resting potential of approximately -50 mV and responsivity to dim light. The optical axis of the responding unit was located by moving the tip of the optical fiber until dim white light flashes produced a maximal response.
We recorded from nearly dark-adapted photoreceptors. To minimize the effect of light adaptation during the experiment, we used light flashes that were limited to 30 msec in duration. This is the shortest light stimulus that still produces a receptor potential with an amplitude of the initial transient component that is the same as that elicited by longer (e.g., 1 sec) stimuli.
The receptor potentials were recorded through a preamplifier (MEZ-7200; Nihon-kohden, Tokyo, Japan) connected to an oscilloscope (VC-11; Nihon-kohden). First, the spectral type of the unit was determined by a series of monochromatic flashes with an intensity of 5.0 x 109
Recorded units were subjected to additional analysis only when the Vmax was >40 mV. Amplitudes of the spectral responses were extrapolated to the V–log I function of a given unit to transform the amplitudes into photon numbers required for the responses. The normalized reciprocal of the relative photon numbers then yielded the sensitivity.
The recorded broadband units were marked by Lucifer yellow. We delivered Lucifer yellow from the tip of the electrode by applying a hyperpolarizing DC of 2–5 nA for 5–10 min. The animal was then unmounted from the Faraday cage and positioned under an epifluorescence microscope (BX-60; Olympus Optical, Tokyo, Japan). The ommatidium containing the Lucifer yellow-injected unit was identified and photographed under violet excitation (dichroic cube U-MNBV; excitation bandpass filter at 420 nm and emission cutoff filter at 470 nm). Subsequently, the excitation light was switched to UV (dichroic cube U-MWU; excitation bandpass filter at 350 nm and emission cutoff at 420 nm) to correlate the stained ommatidium with the array of fluorescing ommatidia.
Histology. After the electrophysiology and the fluorescence microscopy, the compound eye containing the Lucifer yellow-injected unit was processed for light-microscopic histology. The eye was isolated and fixed at room temperature for 30 min in 4% paraformaldehyde in 0.1 M sodium cacodylate buffer at pH 7.4 and then dehydrated with an acetone series and embedded in Spurr's resin. Sections (10–14 µm thick) were cut with a rotary microtome. The sections were first observed under the epifluorescence microscope with violet excitation to localize the unit within the ommatidium, and subsequently normal transmission light was used to identify the color of the ommatidial pigmentation.
Modeling. The computational model used for calculating the sensitivity spectrum of the R5–R8 cells (see Figs. 2, 4) was essentially identical to that of Arikawa et al. (1999a
where I(z,
(
j is the peak absorbance coefficient of visual pigment j,
j and
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Figure 2. Measurements of photoreceptor sensitivity spectra. a, Typical recording from a broadband unit. Receptor potentials elicited by a series of equiquantal monochromatic flashes of 20 nm step (from 300 to 700 nm for the first set and from 700 to 300 nm for the second set) and response–stimulus intensity relationships at 560 and 460 nm over a range of 2.5 x 102
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Figure 4. Calculated (R1 and R2, dotted curve; R3 and R4, dashed curve; R5–R8 at polarization 0°, solid curve) and recorded (violet receptor, open circles; single-peaked green receptor, triangles; broadband receptor, filled circles) sensitivity spectra of the photoreceptor classes in type II ommatidia.
We have modeled the rhabdom as a circular cylinder. On the basis of detailed anatomy, the assumptions were as follows. The total length of the rhabdom is 500 µm; a distal layer of 260 µm is fully occupied by the R1–R4 photoreceptors; in a transition zone of 70 µm, the R1–R4 rhabdomeres reduce in size, whereas the participation of the R5–R8 cells increases; the latter cells fully occupy the proximal 140 µm; the basal 30 µm is taken up by the R9 photoreceptor; and each of the R1–R4 and R5–R8 occupy one-quarter of the rhabdomere cross-sections in the distal and proximal layers, respectively. The fluorescing, UV-absorbing 3-hydroxyretinol is homogeneously distributed in the distal 70 µm, with an absorption coefficient of 0.2 µm-1. The red-screening pigment is present in cells R3–R8, with an absorption coefficient of 0.005 µm-1. The visual pigment peak wavelengths are 365 nm (PxUV), 530 nm (PxL1), 515 nm (PxL2), and 575 nm (PxL3); the photoreceptors R1 and R2 both contain exclusively PxUV; R3 and R4 contain equal amounts of PxL1 and PxL2; R5–R8 contain PxL2 and PxL3 in a concentration ratio of 3:1 (see below); and R9 contains both PxL1 and PxL2. The visual pigment spectra are described by template formulas (Stavenga et al., 1993
A relative amount of PxL2 and PxL3 of 3:1 was chosen, because this ratio gave satisfactory outcomes in the computer simulations. We have noticed that the in situ hybridization results did not necessarily match this choice: the labeling density of PxL2 is comparable with or maybe even weaker than that of PxL3 (Fig. 1d,e). However, taking equal concentrations of PxL2 and PxL3 yielded a much too high sensitivity in the long-wavelength range in the simulations. This may imply that the labeling density of in situ hybridization does not provide a direct measure of the expressed visual pigment concentration in photoreceptors. Another possible cause of the discrepancy is the limited accuracy of the predicted absorption peak wavelength of the PxL2 and PxL3 visual pigments. We predicted absorption peaks of 515 nm for PxL2 and 575 nm for PxL3 only by model calculation (Arikawa et al., 1999a
Results
The proximal photoreceptors of the fluorescent type II ommatidia express a broadband spectral sensitivity
In the course of previous studies on the photoreceptors of P. xuthus, we sometimes encountered units with abnormally broad sensitivity spectra, but we could not unequivocally prove that the recordings were from single photoreceptors. We therefore designed the experimental procedure described below.With the electrode advancing in the retina, we searched for units with broad sensitivity spectra. Broadband units were detected only when the electrode track ran through the proximal tier of the ventral retina. Figure 2a shows a typical recording trace, which contains two series of spectral responses (300–700 nm; with equiquantal monochromatic flashes) and V–log I functions (recorded at 560 and 440 nm in this case). Figure 2b is a set of V–log I functions recorded from a single broadband unit at 420, 440, 540, and 620 nm, with the best fits of the Naka–Rushton function. The maximum response amplitude, Vmax, and the exponent, n, are virtually identical for the different recording wavelengths (for values, see Fig. 2 legend). The sensitivity spectrum presented in Figure 2c shows the average of 10 cells from nine butterflies.
We identified and localized all of the recorded units histologically, as follows, to determine whether the units correspond to single photoreceptors. After the electrophysiological recordings, we delivered Lucifer yellow from the electrode tip by applying a hyperpolarizing DC. The minor amount of Lucifer yellow that may have leaked into the recorded photoreceptor during the spectral measurements before applying the current did not perturb the sensitivity spectra, because the spectra of known spectral receptors encountered in the course of the present study were identical to those of our previous recordings with 3 M KCl-filled electrodes (Arikawa et al., 1987
The ommatidium containing the Lucifer yellow-injected unit was subsequently localized by fluorescence microscopy, applying violet epi-illumination (Fig. 3a). By switching the excitation light to UV, we found that the ommatidium emitted whitish fluorescence, proving that the unit was a member of a type II ommatidium (Fig. 3b). The eyes were then further processed for histology to identify the receptor type. In the particular case of Figure 3c, showing a transverse section through the proximal tier of the ommatidia, the unit appeared to be a single R8 photoreceptor. Regular transmission microscopy of the same frame revealed that the Lucifer yellow-injected photoreceptor contained red pigment (Fig. 3d), in agreement with the previous observation that type II ommatidia are red pigmented (Arikawa and Stavenga, 1997
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Figure 3. Lightmicroscopicidentificationofthelocationofabroadbandunit.Thedorsalside of the eye, which was identified by the hole made in the cornea for electrode insertion (data not shown), corresponds to the top edge of all micrographs. The direction allows us to identify the photoreceptor number unambiguously (Fig. 1a). a, The ommatidium containing the Lucifer yellow-injected unit (arrowhead). b, UV excitation showing that the ommatidium was of type II (arrowhead). c, Section of the eye observed under violet excitation. The unit was a proximal photoreceptor R8 (arrowhead). d, Regular transmission microscopy revealed that the ommatidium of the labeled photoreceptor (arrowhead) contained red pigment. Scale bars: a, b, 100 µm; c, d, 10 µm.
Identical observations were made for all of the broadband-sensitive units analyzed in the present study (i.e., the broadband units were invariably identified as belonging to the set of proximal photoreceptors, R5–R8, of the fluorescent type II ommatidia).
Modeling of the broadband sensitivity spectrum
In modeling the broadband sensitivity spectra, we have calculated the fraction of light entering the rhabdom of type II ommatidia that is absorbed by the visual pigments as well as by the screening pigments to be in the wavelength range of 300–700 nm. We have assumed that both PxL2 and PxL3 visual pigments in R5–R8 photoreceptors contribute to the spectral sensitivity in an identical manner (i.e., each absorbed photon by one or the other visual pigment contributes equally to phototransduction or opens the same number of channels). Figure 2c shows the results of the model calculations of the normalized absorption spectra of the R5–R8 receptors, together with the average of the broadband sensitivity spectra. We calculated the spectra for incident light with different polarization angles (i.e., 0, 90, 35, and 125°, respectively). The calculated and measured spectra closely match at the short and the long wavelengths, but the spectra vary in the wave-length range of 480–580 nm. The variation can be attributed primarily to the polarization sensitivity of the distal photoreceptors, R1–R4, which act as a polarization-dependent absorption filter for the proximal photoreceptors, R5–R8. For example, the R3 and R4 cells are single-peaked green receptors, peaking at 520 nm with maximum polarization sensitivity at 90°. When the ommatidium is stimulated with 90° polarized light, the light is strongly absorbed by R3 and R4, thus reducing the light reaching the proximal tier and lowering the response of proximal photoreceptors in the middle wavelength region.Figure 4 presents the calculated and recorded spectra of the proximal as well as distal photoreceptors in type II ommatidia. The R1 and R2 photoreceptors, which contain PxUV, a visual pigment absorbing maximally at 360 nm, become violet receptors, with sensitivity spectrum peaking at 400 nm, because of the abundant 3-hydroxyretinol concentrated in the distal part, which acts as a UV filter for the underlying photoreceptors (Arikawa et al., 1999b
-band as a result of the UV filter, confirming our previous study on the type II ommatidium (Arikawa et al., 1999b
One might argue that the fluorescence of 3-hydroxyretinol could excite the photoreceptors in type II ommatidia. However, the recordings clearly indicate that this is not the case: the photoreceptors in type II ommatidia have virtually no sensitivity in the UV wavelength region (Fig. 4) in which the absorption of 3-hydroxyretinol exists. Although the fluorescence seems very prominent in micrographs (Fig. 1c), it requires extremely bright illumination provided by a focused mercury lamp of an epifluorescence microscope. Because of the low quantum yield, fluorescence will therefore have a negligible contribution to photoreceptor excitation.
Discussion
In this study, we describe a novel type of photoreceptor featured in the Papilio retina with an abnormally broad sensitivity spectrum, accordingly termed broadband receptor. Anatomically, the broadband-sensitive cells are the proximal photoreceptors (R5–R8) in the type II ommatidia [i.e., the red-pigmented ommatidia that fluoresce under UV excitation (Figs. 1, 3)]. The photoreceptors were shown to express two mRNAs, encoding the visual pigment opsins PxL2 and PxL3 (Fig. 1d,e). The absorption characteristics of the corresponding visual pigments are spectrally quite different: the absorption peak wavelengths are in the green (515 nm) and orange-red (575 nm) regions, respectively (Arikawa et al., 1999aIn the modeling, we incorporated the light-filtering effects of a number of optical absorbers, namely 3-hydroxyretinol in the distal part of the type II ommatidia, the red-screening pigment surrounding the rhabdom, and the visual pigments in the distal photoreceptors R1–R4, of which the visual pigments in the R3 and R4 photoreceptors filter specifically in the green wavelength region. The calculated absorption spectra reasonably fit to the broadband sensitivity spectra in the short- and the long-wavelength regions. However, the modeling does not yet satisfactorily reproduce the bumpy profile of the sensitivity spectrum in the wavelength region between 480 and 580 nm (Fig. 2c). As described in Materials and Methods, we calculated the sensitivity spectrum by taking only the first-order waveguide mode into account. The second mode presumably contributes to the bumpy profile of the spectrum (Stavenga, 2003
To the best of our knowledge, the broadband receptor of P. xuthus is the first clear example of a class of invertebrate photoreceptors with multiple visual pigments functioning simultaneously. It extends the as-yet-limited list of similar vertebrate photoreceptors (Makino and Dodd, 1996
The biological function of the broadband receptor for butterfly vision must remain a matter of speculation. It seems unlikely that it plays a role in color vision, a function that is logically conferred to the R5–R8 photoreceptors of the type I ommatidia: they have a narrow-band sensitivity spectrum, distinctly peaking in the red (Arikawa and Uchiyama, 1996
Butterfly eyes have a strikingly heterogeneous organization, with specific sets of spectral detectors combined in different types of ommatidia. Although the overall lattice of ommatidia is of crystalline regularity, the different types are randomly arranged within that regular lattice (Arikawa and Stavenga, 1997
Footnotes
Received Oct. 15, 2002; revised Mar. 11, 2003; accepted Mar. 13, 2003.This work was supported by research grants from the Ministry of Education, Culture, Sports, Science and Technology and the Japan Science and Technology Corporation to K.A. Shin-ya Takemura participated in part of the electrophysiological experiments.
Correspondence should be addressed to Dr. Kentaro Arikawa, Graduate School of Integrated Science, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama 236-0027, Japan. E-mail: arikawa{at}yokohama-cu.ac.jp.
Copyright © 2003 Society for Neuroscience 0270-6474/03/234527-06$15.00/0
References
Applebury ML, Antoch MP, Baxter LC, Chun LL, Falk JD, Farhangfar F, Kage K, Krzystolik MG, Lyass LA, Robbins JT (2000) The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27: 513–523.[Web of Science][Medline]
Arikawa K, Stavenga DG (1997) Random array of colour filters in the eyes of butterflies. J Exp Biol 200: 2501–2506.[Abstract]
Arikawa K, Uchiyama H (1996) Red receptors dominate the proximal tier of the retina in the butterfly Papilio xuthus. J Comp Physiol [A] 178: 55–61.
Arikawa K, Inokuma K, Eguchi E (1987) Pentachromatic visual system in a butterfly. Naturwissenschaften 74: 297–298.[Web of Science]
Arikawa K, Scholten DGW, Kinoshita M, Stavenga DG (1999a) Tuning of photoreceptor spectral sensitivities by red and yellow pigments in the butterfly Papilio xuthus. Zool Sci 16: 17–24.
Arikawa K, Mizuno S, Scholten DGW, Kinoshita M, Seki T, Kitamoto J, Stavenga DG (1999b) An ultraviolet absorbing pigment causes a narrow-band violet receptor and a single-peaked green receptor in the eye of the butterfly Papilio. Vision Res 39: 1–8.[Medline]
Bandai K, Arikawa K, Eguchi E (1992) Localization of spectral receptors in the ommatidium of butterfly compound eye determined by polarization sensitivity. J Comp Physiol [A] 171: 289–297.
Feiler R, Bjornson R, Kirschfeld K, Mismer D, Rubin GM, Smith DP, Socolich M, Zuker CS (1992) Ectopic expression of ultraviolet-rhodopsins in the blue photoreceptor cells of Drosophila: visual physiology and photochemistry of transgenic animals. J Neurosci 12: 3862–3868.[Abstract]
Glosmann M, Ahnelt PK (2002) A mouse-like retinal cone phenotype in the Syrian hamster: S opsin coexpressed with M opsin in a common cone photoreceptor. Brain Res 929: 139–146.[Medline]
Heiling AM, Herberstein ME, Chittka L (2003) Crab-spiders manipulate flower signals. Nature 421: 334.[Medline]
Jacobs GH, Fenwick JC, Calderone JB, Deeb SS (1999) Human cone pigment expressed in transgenic mice yields altered vision. J Neurosci 19: 3258–3265.
[Abstract/Free Full Text] Kitamoto J, Sakamoto K, Ozaki K, Mishina Y, Arikawa K (1998) Two visual pigments in a single photoreceptor cell: identification and histological localization of three mRNAs encoding visual pigment opsins in the retina of the butterfly Papilio xuthus. J Exp Biol 201: 1255–1261.[Abstract]
Kitamoto J, Ozaki K, Arikawa K (2000) Ultraviolet and violet receptors express identical mRNA encoding an ultraviolet-absorbing opsin: identification and histological localization of two mRNAs encoding short-wavelength-absorbing opsins in the retina of the butterfly Papilio xuthus. J Exp Biol 203: 2887–2894.[Abstract]
Lyubarsky AL, Falsini B, Pennesi ME, Valentini P, Pugh ENJ (1999) UV- and midwave-sensitive cone-driven retinal responses of the mouse: a possible phenotype for coexpression of cone photopigments. J Neurosci 19: 442–455.
[Abstract/Free Full Text] Makino CL, Dodd RL (1996) Multiple visual pigments in a photoreceptor of the salamander retina. J Gen Physiol 108: 27–34.
[Abstract/Free Full Text] Parry JW, Bowmaker JK (2002) Visual pigment coexpression in guinea pig cones: a microspectrophotometric study. Invest Ophthalmol Vis Sci 43: 1662–1665.
[Abstract/Free Full Text] Roehlich P, Vanveen T, Szel A (1994) Two different visual pigments in one retinal cone cell. Neuron 13: 1159–1166.[Web of Science][Medline]
Sakamoto K, Hisatomi O, Tokunaga F, Eguchi E (1996) Two opsins from the compound eye of the crab Hemigrapsus sanguineus. J Exp Biol 199: 441–450.[Abstract]
Shaaban SA, Corognale MA, Calderone JB, Huang J, Jacobs GH, Deeb SS (1998) Transgenic mice expressing a functional human photopigment. Invest Ophthalmol Vis Sci 39: 1036.
[Abstract/Free Full Text] Snyder AW, Menzel R, Laughlin SB (1973) Structure and function of the fused rhabdom. J Comp Physiol 87: 99–135.
Stavenga DG (2003) Angular and spectral sensitivity of fly photoreceptors. I. Integrated facet lens and rhabdomere optics. J Comp Physiol [A] 189: 1–17.
Stavenga DG, Smits RP, Hoenders BJ (1993) Simple exponential functions describing the absorbance bands of visual pigment spectra. Vision Res 33: 1011–1017.[Web of Science][Medline]
Townson SM, Chang BSW, Salcedo E, Chadwell LV, Pierce NE, Britt SG (1998) Honeybee blue-and ultraviolet-sensitive opsins: cloning, heterologous expression in Drosophila, and physiological characterization. J Neurosci 18: 2412–2422.
[Abstract/Free Full Text] Warrant EJ, Nilsson DE (1998) Absorption of white light in photoreceptors. Vision Res 38: 195–207.[Web of Science][Medline]
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