The retinal topography of three species of coleoid cephalopod: significance for perception of polarized light

Talbot, Christopher M.; Marshall, N. Justin

doi:10.1098/rstb.2010.0254

Cited by 33 publications

(36 citation statements)

References 44 publications

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“…The horizontal slit pupil of shallow water octopus (Fig. S1F) species intercepts a similar ray bundle when imaging the bottom, acting as an arc-like pupil for images formed on the upper portion of the retina that has an enhanced density of photoreceptors (40).…”

Section: Resultsmentioning

confidence: 99%

Spectral discrimination in color blind animals via chromatic aberration and pupil shape

Stubbs

2016

Proc. Natl. Acad. Sci. U.S.A.

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We present a mechanism by which organisms with only a single photoreceptor, which have a monochromatic view of the world, can achieve color discrimination. An off-axis pupil and the principle of chromatic aberration (where different wavelengths come to focus at different distances behind a lens) can combine to provide "colorblind" animals with a way to distinguish colors. As a specific example, we constructed a computer model of the visual system of cephalopods (octopus, squid, and cuttlefish) that have a single unfiltered photoreceptor type. We compute a quantitative image quality budget for this visual system and show how chromatic blurring dominates the visual acuity in these animals in shallow water. We quantitatively show, through numerical simulations, how chromatic aberration can be exploited to obtain spectral information, especially through nonaxial pupils that are characteristic of coleoid cephalopods. We have also assessed the inherent ambiguity between range and color that is a consequence of the chromatic variation of best focus with wavelength. This proposed mechanism is consistent with the extensive suite of visual/behavioral and physiological data that has been obtained from cephalopod studies and offers a possible solution to the apparent paradox of vivid chromatic behaviors in color blind animals. Moreover, this proposed mechanism has potential applicability in organisms with limited photoreceptor complements, such as spiders and dolphins.spectral discrimination | chromatic aberration | color vision | pupil shape | cephalopod W e show in this paper that, under certain conditions, organisms can determine the spectral composition of objects, even with a single photoreceptor type. Through computational modeling, we show a mechanism that provides spectral information using an important relationship: the position of sharpest focus depends on the spectral peak of detected photons. Mapping out contrast vs. focal setting (accommodation) amounts to obtaining a coarse spectrum of objects in the field of view, much as a digital camera attains best focus by maximizing contrast vs. focal length. We note that a similar phenomenon has been advanced as a possible explanation for color percepts in red/green color-blind primates (1); however, primates have not evolved the off-axis pupil shape found in nearly all shallow water cephalopods that enhances this effect.The only other known mechanism of color discrimination in organisms involves determining the spectrum of electromagnetic radiation using differential comparisons between simultaneous neural signals arising from photoreceptor channels with differing spectral acceptances. Color vision using multiple classes of photoreceptors on a 2D retinal surface comes at a cost: reduced signal to noise ratio in low-light conditions and degraded angular resolution in each spectral channel. Thus, many lineages that are or were active in low-light conditions have lost spectral channels to increase sensitivity (2).Octopus, squid, and cuttlefish (coleoid cephalopods) have l...

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Section: Resultsmentioning

confidence: 99%

Spectral discrimination in color blind animals via chromatic aberration and pupil shape

Stubbs

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Interestingly, the retinas of both crustaceans and cephalopods, which make up a substantial proportion of pelagic visual predators, are known to possess orthogonally arranged rhabdoms [49,50]. Where known, these are generally arranged with half the rhabdoms oriented vertically and the other half horizontally (see [51]), precisely the required orientation for the contrast-enhancement mechanisms we invoke here, and one that provides a parsimonious solution to viewing polarized light [52]. These animals are also capable of rotational eye movements that could theoretically optimize the signal difference between channels in the same way as we did by rotating the camera systems.…”

Section: Discussion (A) Laboratory-based Versus In Situ Imagerymentioning

confidence: 99%

Polarization sensitivity as a contrast enhancer in pelagic predators: lessons fromin situpolarization imaging of transparent zooplankton

Johnsen

Marshall

Widder

2011

Phil. Trans. R. Soc. B

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Because light in the pelagic environment is partially polarized, it has been suggested that the polarization sensitivity found in certain pelagic species may serve to enhance the contrast of their transparent zooplankton prey. We examined its potential during cruises in the Gulf of Mexico and Atlantic Ocean and at a field station on the Great Barrier Reef. First, we collected various species of transparent zooplankton and micronekton and photographed them between crossed polarizers. Many groups, particularly the cephalopods, pelagic snails, salps and ctenophores, were found to have ciliary, muscular or connective tissues with striking birefringence. In situ polarization imagery of the same species showed that, while the degree of underwater polarization was fairly high (approx. 30% in horizontal lines of sight), tissue birefringence played little to no role in increasing visibility. This is most likely due to the low radiance of the horizontal background light when compared with the downwelling irradiance. In fact, the dominant radiance and polarization contrasts are due to unpolarized downwelling light that has been scattered from the animal viewed against the darker and polarized horizontal background light. We show that relatively simple algorithms can use this negative polarization contrast to increase visibility substantially.

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“…Rapid and presumably saccadic eye and/or body repositioning towards objects of interest are noted in octopus, squid and cuttlefish [28,29]. This would be expected from such voracious predators that also show a visually guided ballistic tentacular strike similar to, although orders of magnitude slower than, that of stomatopods.…”

Section: (B) Comparison With Arthropods and Other Invertebratesmentioning

confidence: 99%

Shrimps that pay attention: saccadic eye movements in stomatopod crustaceans

Marshall

Land

Cronin

2014

Phil. Trans. R. Soc. B

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Discovering that a shrimp can flick its eyes over to a fish and follow up by tracking it or flicking back to observe something else implies a 'primate-like' awareness of the immediate environment that we do not normally associate with crustaceans. For several reasons, stomatopods (mantis shrimp) do not fit the general mould of their subphylum, and here we add saccadic, acquisitional eye movements to their repertoire of unusual visual capabilities. Optically, their apposition compound eyes contain an area of heightened acuity, in some ways similar to the fovea of vertebrate eyes. Using rapid eye movements of up to several hundred degrees per second, objects of interest are placed under the scrutiny of this area. While other arthropod species, including insects and spiders, are known to possess and use acute zones in similar saccadic gaze relocations, stomatopods are the only crustacean known with such abilities. Differences among species exist, generally reflecting both the eye size and lifestyle of the animal, with the larger-eyed more sedentary species producing slower saccades than the smaller-eyed, more active species. Possessing the ability to rapidly look at and assess objects is ecologically important for mantis shrimps, as their lifestyle is, by any standards, fast, furious and deadly.

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The retinal topography of three species of coleoid cephalopod: significance for perception of polarized light

Cited by 33 publications

References 44 publications

Spectral discrimination in color blind animals via chromatic aberration and pupil shape

Spectral discrimination in color blind animals via chromatic aberration and pupil shape

Polarization sensitivity as a contrast enhancer in pelagic predators: lessons fromin situpolarization imaging of transparent zooplankton

Shrimps that pay attention: saccadic eye movements in stomatopod crustaceans

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