scholarly journals Red-green opponency in the long visual fibre photoreceptors of brushfoot butterflies (Nymphalidae)

2021 ◽  
Vol 288 (1961) ◽  
Author(s):  
Gregor Belušič ◽  
Marko Ilić ◽  
Andrej Meglič ◽  
Primož Pirih

In many butterflies, the ancestral trichromatic insect colour vision, based on UV-, blue- and green-sensitive photoreceptors, is extended with red-sensitive cells. Physiological evidence for red receptors has been missing in nymphalid butterflies, although some species can discriminate red hues well. In eight species from genera Archaeoprepona, Argynnis, Charaxes, Danaus, Melitaea, Morpho, Heliconius and Speyeria , we found a novel class of green-sensitive photoreceptors that have hyperpolarizing responses to stimulation with red light. These green-positive, red-negative (G+R–) cells are allocated to positions R1/2, normally occupied by UV and blue-sensitive cells. Spectral sensitivity, polarization sensitivity and temporal dynamics suggest that the red opponent units (R–) are the basal photoreceptors R9, interacting with R1/2 in the same ommatidia via direct inhibitory synapses. We found the G+R– cells exclusively in butterflies with red-shining ommatidia, which contain longitudinal screening pigments. The implementation of the red colour channel with R9 is different from pierid and papilionid butterflies, where cells R5–8 are the red receptors. The nymphalid red-green opponent channel and the potential for tetrachromacy seem to have been switched on several times during evolution, balancing between the cost of neural processing and the value of extended colour information.

Author(s):  
Camilla R. Sharkey ◽  
Jorge Blanco ◽  
Maya M. Leibowitz ◽  
Daniel Pinto-Benito ◽  
Trevor J. Wardill

AbstractDrosophila melanogaster has long been a popular model insect species, due in large part to the availability of genetic tools and is fast becoming the model for insect colour vision. Key to understanding colour reception in Drosophila is in-depth knowledge of spectral inputs and downstream neural processing. While recent studies have sparked renewed interest in colour processing in Drosophila, photoreceptor spectral sensitivity measurements have yet to be carried out in vivo. We have fully characterised the spectral input to the motion and colour vision pathways, and directly measured the effects of spectral modulating factors, screening pigment density and carotenoid-based ocular pigments. All receptor sensitivities had significant shifts in spectral sensitivity compared to previous measurements. Notably, the spectral range of the Rh6 visual pigment is substantially broadened and its peak sensitivity is shifted by 92 nm from 508 to 600 nm. We propose that this deviation can be explained by transmission of long wavelengths through the red screening pigment and by the presence of the blue-absorbing filter in the R7y receptors. Further, we tested direct interactions between photoreceptors and found evidence of interactions between inner and outer receptors, in agreement with previous findings of cross-modulation between receptor outputs in the lamina.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Camilla R. Sharkey ◽  
Jorge Blanco ◽  
Maya M. Leibowitz ◽  
Daniel Pinto-Benito ◽  
Trevor J. Wardill

Abstract Drosophila melanogaster has long been a popular model insect species, due in large part to the availability of genetic tools and is fast becoming the model for insect colour vision. Key to understanding colour reception in Drosophila is in-depth knowledge of spectral inputs and downstream neural processing. While recent studies have sparked renewed interest in colour processing in Drosophila, photoreceptor spectral sensitivity measurements have yet to be carried out in vivo. We have fully characterised the spectral input to the motion and colour vision pathways, and directly measured the effects of spectral modulating factors, screening pigment density and carotenoid-based ocular pigments. All receptor sensitivities had significant shifts in spectral sensitivity compared to previous measurements. Notably, the spectral range of the Rh6 visual pigment is substantially broadened and its peak sensitivity is shifted by 92 nm from 508 to 600 nm. We show that this deviation can be explained by transmission of long wavelengths through the red screening pigment and by the presence of the blue-absorbing filter in the R7y receptors. Further, we tested direct interactions between inner and outer photoreceptors using selective recovery of activity in photoreceptor pairs.


2020 ◽  
Author(s):  
Marjorie A. Liénard ◽  
Gary D. Bernard ◽  
Andrew A. Allen ◽  
Jean-Marc Lassance ◽  
Siliang Song ◽  
...  

AbstractColour vision is largely mediated by changes in number, expression, and spectral properties of rhodopsins, but the genetic mechanisms underlying adaptive shifts in spectral sensitivity remain largely unexplored. Using in vivo photochemistry, optophysiology, and in vitro functional assays, we link variation in eye spectral sensitivity at long wavelengths to species-specific absorbance spectra for LW opsins in lycaenid butterflies. In addition to loci specifying an ancestral green-absorbing rhodopsin with maximum spectral sensitivity (λmax) at 520-530 nm in Callophrys sheridanii and Celastrina ladon, we find a novel form of red-shifted LW rhodopsin at λmax = 565-570 nm in Arhopala japonica and Eumaeus atala. Furthermore, we show that Ca. sheridanii and Ce. ladon exhibit a smaller bathochromic shift at BRh2 (480-489 nm), and with the ancestral LW rhodopsin, cannot perceive visible red light beyond 600 nm. In contrast, molecular variation at the LW opsin in A. japonica and E. atala is coordinated with tuning of the blue opsin that also shifts sensitivity to longer wavelengths enabling colour discrimination up to 617 nm. We then use E. atala as a model to examine the interplay between red and blue spectral sensitivity. Owing to blue duplicate expression, the spatial distribution of opsin mRNAs within an ommatidium defines an expanded retinal stochastic mosaic of at least six opsin-based photoreceptor classes. Our mutagenesis in vitro assays with BRh1 (λmax = 435 nm) chimeric blue rhodopsins reveal four main residues contributing to the 65 nm bathochromic shift towards BRh2 (λmax = 500 nm). Adaptations in this four-opsin visual system are relevant for discrimination of conspecific reflectance spectra in E. atala. Together, these findings illustrate how functional changes at multiple rhodopsins contribute to the evolution of a broader spectral sensitivity and adaptation in visual performance.Significance StatementRhodopsins are photosensitive protein molecules that absorb specific wavelengths of incoming light and convey colour information in the visual system. We show that molecular evolution in a green insect opsin gene resulted in a shift in its maximal absorbance peak, enabling some lycaenid butterflies to use spectral energy of longer wavelengths (LW) to discriminate colours in the red spectrum better than relatives bearing ancestral green LW rhodopsins. Lycaenids also evolved a duplicate blue opsin gene, and we illustrate an example where species equipped with red LW rhodopsins shifted their blue sensitivity peak to longer wavelengths due to changes in several blue-tuning residues that have evolved repeatedly in different insect lineages. We demonstrate how changes at multiple vision genes in the insect eye effectively create a coordinated mechanism expanding spectral sensitivity for visually guided behaviours such as selecting host plants and mates.


2017 ◽  
Vol 4 (3) ◽  
pp. 161009 ◽  
Author(s):  
Pierre-Paul Bitton ◽  
Ulrike K. Harant ◽  
Roland Fritsch ◽  
Connor M. Champ ◽  
Shelby E. Temple ◽  
...  

The light environment in water bodies changes with depth due to the absorption of short and long wavelengths. Below 10 m depth, red wavelengths are almost completely absent rendering any red-reflecting animal dark and achromatic. However, fluorescence may produce red coloration even when red light is not available for reflection. A large number of marine taxa including over 270 fish species are known to produce red fluorescence, yet it is unclear under which natural light environment fluorescence contributes perceptively to their colours. To address this question we: (i) characterized the visual system of Tripterygion delaisi, which possesses fluorescent irides, (ii) separated the colour of the irides into its reflectance and fluorescence components and (iii) combined these data with field measurements of the ambient light environment to calculate depth-dependent perceptual chromatic and achromatic contrasts using visual modelling. We found that triplefins have cones with at least three different spectral sensitivities, including differences between the two members of the double cones, giving them the potential for trichromatic colour vision. We also show that fluorescence contributes increasingly to the radiance of the irides with increasing depth. Our results support the potential functionality of red fluorescence, including communicative roles such as species and sex identity, and non-communicative roles such as camouflage.


1988 ◽  
Vol 136 (1) ◽  
pp. 35-52
Author(s):  
R. MENZEL ◽  
E. STEINMANN ◽  
J. DE SOUZA ◽  
W. BACKHAUS

The spectral sensitivity of single photoreceptors of Osmia rufa was determined by a fast voltage-clamp technique. Three receptor types were found whose spectral sensitivity functions followed a rhodopsin-like photopigment absorption function with λmax values at 348nm (ultraviolet receptor), 436nm (blue receptor) and 572nm (green receptor). The λmax of the green receptor in Osmia rufa is shifted to much longer wavelengths compared with other insect species. Discrimination of colour signals was tested after training a bee at the entrance to its nest. The colour signals were filter discs (70 mm in diameter) with a hole (10 mm in diameter) in the centre and the bees quickly learned to use the coloured disc as a marker of the nest entrance. Tests were dual forced-choice tests with two coloured discs closely positioned next to each other. 94 different tests were each repeated 5–15 times and were performed after training to 12 different colour signals. A photoreceptor model was used to calculate the loci of the colour signals in a three-dimensional colour space and in a chromaticity diagram. The perceptual distance between the colour loci was calculated as line elements (minimum number of just noticeable difference, jnd-steps), which were based on the noiseproperties of the photoreceptors. The discrimination determined by the behavioural tests correlated very well with the jnd-steps. The correlation was better for the line elements in the colour plane than in the colour space. Osmia rufa was compared with the honeybee Apis mellifera and the stingless bee Melipona quadrifasciata. There is no difference in colour selection between Osmia and Apis, whereas Melipona discriminates less well in the violet-blue region. The model calculation was used to compare the chromaticity diagrams and the spectral discrimination functions of the three species. It is concluded that the receptor model used in this study predicts the discrimination behaviour of the three bee species very well. Therefore, comparative studies on colour vision in flowervisiting insects may be based on spectral measurements of the photoreceptors, and in many cases this reduces the extent of laborious behavioural studies.


2019 ◽  
Author(s):  
Richard W. Brill ◽  
Andrij Z. Horodysky ◽  
Allen R. Place ◽  
Mary E.M. Larkin ◽  
Renate Reimschuessel

AbstractDietary insufficiencies have been well documented to decrease growth rates and survival (and therefore overall production) in fish aquaculture. By contrast, the effects of dietary insufficiencies on the sensory biology of cultured fish remains largely unstudied. Diets based solely on plant protein sources could have advantages over fish-based diets, because of the cost and ecological effects of the latter, but lack the amino acid taurine. Adequate levels of taurine are, however, necessary for the development of a fully functional visual system in mammals. As part of ongoing studies to determine the suitability of plant-based diets, we investigated the effects of normal and reduced taurine dietary levels on retinal anatomy and function in European sea bass (Dicentrarchus labrax). We could not demonstrate any effects of dietary taurine level on retinal anatomy, nor the functional properties of luminous sensitivity or temporal resolution (measured as flicker fusion frequency). We did, however, find an effect on spectral sensitivity. The peak of spectral sensitivity of individuals fed a 5% taurine diet was rightward shifted (i.e., towards longer wavelengths) relative to that of fish fed a 0% or 1.5 % taurine diet. This difference in in spectral sensitivity was due to a relatively lower level of middle wavelength pigment (maximum absorbance ≈500 nm) in fish fed a 5% taurine diet. Changes in spectral sensitivity resulting from diets containing different taurine levels are unlikely to be detrimental to fish destined for market but could be in fishes that are being reared for stock enhancement programs.


1992 ◽  
Vol 8 (3) ◽  
pp. 243-249 ◽  
Author(s):  
Joseph C. Besharse ◽  
Paul Witkovsky

AbstractTo test the hypothesis that light-evoked cone contraction in eye cups from Xenopus laevis is controlled through a direct mechanism initiated by the cone's own photopigment, we conducted spectral-sensitivity experiments. We estimate that initiation of contraction of red absorbing cones (611 nm) is 1.5 log units more sensitive to green (533 nm) than red (650 nm) light stimuli. The difference is comparable to that predicted from the spectral-sensitivity function of the green absorbing, principal rod (523 nm). Furthermore, 480-nm and 580-nm stimuli which are absorbed nearly equally by the principal rod have indistinguishable effects on cone contraction. We also found that light blockade of nighttime cone elongation is much more sensitive to green than to red light stimuli. Our observations are inconsistent with the hypothesis tested, and suggest that light-regulated cone motility is controlled through an indirect mechanism initiated primarily by the green absorbing, principal rod.


2012 ◽  
Vol 25 (0) ◽  
pp. 179
Author(s):  
Vincent A. Billock ◽  
Brian H. Tsou

Information integration occurs at every sensory scale and although distinctions are made for integration between and within senses, integration at intermediate scales may exploit familiar mechanisms. Here, we explore this idea by applying a sensory integration mechanism to some poorly understood multispectral integration problems in human colour vision. Billock and Tsou (IMRF, 2011) used a binding-like neural synchronization mechanism to model intensity-dependent (inverse) enhancement of visual responses by auditory stimulation in cat. The same model also applies to mutual enhancement of visual and infrared responses in rattlesnake, suggesting that a similar mechanism could model integration of spectral information in human colour vision. For example, chromatic brightness is thought to be a vector-like nonlinear combination of luminance and chromatic channels; its neural correlate is unknown. We model its spectral sensitivity by pairwise excitatory synchronization between luminance (broadband) neurons and cortically rectified L+M- and S+M-L- LGN neurons. Similarly, the yellow lobe of the yellow-blue opponent channel is known to be a nonlinearly enhanced combination of long- and medium-wavelength-sensitive inputs, but no sensible neural model for this interaction has been advanced. We model the spectral sensitivity of ‘yellowness’ using excitatory synchronization between cortically rectified L+M+S- and M+L- LGN units. The inputs for both simulations were macaque neural firing rate data (DeValois et al., 1966). Fascinatingly, in both cases, multispectral integration in human colour vision was well modeled using the rattlesnake/cat neural synchronization equations without any use of fitting parameters. This is the first application of sensory integration concepts to human colour vision transformations.


2020 ◽  
Vol 223 (23) ◽  
pp. jeb230979
Author(s):  
Anna-Lee Jessop ◽  
Yuri Ogawa ◽  
Zahra M. Bagheri ◽  
Julian C. Partridge ◽  
Jan M. Hemmi

ABSTRACTColour signals, and the ability to detect them, are important for many animals and can be vital to their survival and fitness. Fiddler crabs use colour information to detect and recognise conspecifics, but their colour vision capabilities remain unclear. Many studies have attempted to measure their spectral sensitivity and identify contributing retinular cells, but the existing evidence is inconclusive. We used electroretinogram (ERG) measurements and intracellular recordings from retinular cells to estimate the spectral sensitivity of Gelasimus dampieri and to track diurnal changes in spectral sensitivity. G. dampieri has a broad spectral sensitivity and is most sensitive to wavelengths between 420 and 460 nm. Selective adaptation experiments uncovered an ultraviolet (UV) retinular cell with a peak sensitivity shorter than 360 nm. The species’ spectral sensitivity above 400 nm is too broad to be fitted by a single visual pigment and using optical modelling, we provide evidence that at least two medium-wavelength sensitive (MWS) visual pigments are contained within a second blue-green sensitive retinular cell. We also found a ∼25 nm diurnal shift in spectral sensitivity towards longer wavelengths in the evening in both ERG and intracellular recordings. Whether the shift is caused by screening pigment migration or changes in opsin expression remains unclear, but the observation shows the diel dynamism of colour vision in this species. Together, these findings support the notion that G. dampieri possesses the minimum requirement for colour vision, with UV and blue/green receptors, and help to explain some of the inconsistent results of previous research.


1972 ◽  
Vol 59 (5) ◽  
pp. 534-558 ◽  
Author(s):  
Gilbert D. McCann ◽  
David W. Arnett

Spectral and polarization sensitivity measurements were made at several levels (retina, first and third optic ganglion, cervical connective, behavior) of the dipteran visual nervous system. At all levels, it was possible to reveal contributions from the retinular cell subsystem cells 1 to 6 or the retinular cell subsystem cells 7 and 8 or both. Only retinular cells 1 to 6 were directly studied, and all possessed the same spectral sensitivity characterized by two approximately equal sensitivity peaks at 350 and 480 nm. All units of both the sustaining and on-off variety in the first optic ganglion exhibited the same spectral sensitivity as that of retinular cells 1 to 6. It was possible to demonstrate for motion detection and optomotor responses two different spectral sensitivities depending upon the spatial wavelength of the stimulus. For long spatial wavelengths, the spectral sensitivity agreed with retinular cells 1 to 6; however, the spectral sensitivity at short spatial wavelengths was characterized by a single peak at 465 nm reflecting contributions from the (7, 8) subsystem. Although the two subsystems exhibited different spectral sensitivities, the difference was small and no indication of color discrimination mechanisms was observed. Although all retinular cells 1 to 6 exhibited a preferred polarization plane, sustaining and on-off units did not. Likewise, motion detection and optomotor responses were insensitive to the polarization plane for long spatial wavelength stimuli; however, sensitivity to select polarization planes was observed for short spatial wavelengths.


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