S cones: Evolution, retinal distribution, development, and spectral sensitivity

Hunt, David M.; Peichl, Leo

doi:10.1017/s0952523813000242

Cited by 80 publications

(81 citation statements)

References 248 publications

(550 reference statements)

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“…The takeaway is that the SC does not use color or S-cone input to guide saccades. This conclusion is surprising because both the SC and S-cones are evolutionarily ancient, and the SC has a central role in visually guided orienting behavior (2,11).…”

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confidence: 83%

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Express saccades and superior colliculus responses are sensitive to short-wavelength cone contrast

Hall

Colby

2016

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

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A key structure for directing saccadic eye movements is the superior colliculus (SC). The visual pathways that project to the SC have been reported to carry only luminance information and not color information. Short-wavelength-sensitive cones (S-cones) in the retina make little or no contribution to luminance signals, leading to the conclusion that S-cone stimuli should be invisible to SC neurons. The premise that S-cone stimuli are invisible to the SC has been used in numerous clinical and human psychophysical studies. The assumption that the SC cannot use S-cone stimuli to guide behavior has never been tested. We show here that express saccades, which depend on the SC, can be driven by S-cone input. Further, express saccade reaction times and changes in SC activity depend on the amount of S-cone contrast. These results demonstrate that the SC can use S-cone stimuli to guide behavior. We conclude that the use of S-cone stimuli is insufficient to isolate SC function in psychophysical and clinical studies of human subjects.S-cone | SC | macaque D ecades of oculomotor research have led to an incongruous conclusion: The oculomotor system does not use color information to guide the eyes (1, 2). However, it is natural to direct one's gaze to objects defined by color. Color vision in primates evolved because of the tremendous benefit of being able to discriminate colors and direct our actions accordingly (3, 4). The superior colliculus (SC) is a brainstem structure with a central role in the transformation of visual sensory signals into saccadic eye movements (2). Visual projections to the SC lack color opponent responses and appear to be dominated by luminance information (5-9). Luminance signals arise almost exclusively from long-and medium-wavelength-sensitive cones (L-and M-cones) in the retina, but not short-wavelength-sensitive cones (S-cones) (10). Instead, S-cones evolved to contribute to color vision (11). The takeaway is that the SC does not use color or S-cone input to guide saccades. This conclusion is surprising because both the SC and S-cones are evolutionarily ancient, and the SC has a central role in visually guided orienting behavior (2, 11).The proposition that the SC cannot detect S-cone stimuli has been leveraged to test SC function in diverse clinical and human psychophysical studies (12, 13). The scope of these investigations has ranged from mechanisms of blindsight (14-16), interhemispheric transfer in patients without a corpus callosum (17), face processing (18), and visual development (19) to inhibition of return (20), nasotemporal asymmetry (21), and the gap effect (22). The rationale for these experiments comes from an influential study by Sumner et al. (23), who noted that previous physiological and anatomical experiments had failed to find S-cone input to the SC. The idea is to present subjects with either a luminance or S-cone stimulus on separate trials of a visual or oculomotor task. If behavior [usually saccadic reaction time (RT)] is different in response to the S-cone stimulus, the ...

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confidence: 83%

“…Luminance signals arise almost exclusively from long-and medium-wavelength-sensitive cones (L-and M-cones) in the retina, but not short-wavelength-sensitive cones (S-cones) (10). Instead, S-cones evolved to contribute to color vision (11). The takeaway is that the SC does not use color or S-cone input to guide saccades.…”

mentioning

confidence: 99%

Express saccades and superior colliculus responses are sensitive to short-wavelength cone contrast

Hall

Colby

2016

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

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“…3E). Tetrapod SWS1 pigments, however, apparently shifted from UV into violet or blue sensitivity independently on multiple occasions in each lineage (Yokoyama et al, 2016;Hunt and Peichl, 2014). The ancestral amphibian, reptile and mammal presumably all expressed a UV SWS1, and modern reptiles have no reported violet SWS1 opsins (de Lanuza and Font, 2014).…”

Section: Spectral Tuning Of Uv Opsinsmentioning

confidence: 99%

Photoreception and vision in the ultraviolet

Cronin

Bok

2016

Journal of Experimental Biology

143

128

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Ultraviolet (UV) light occupies the spectral range of wavelengths slightly shorter than those visible to humans. Because of its shorter wavelength, it is more energetic (and potentially more photodamaging) than 'visible light', and it is scattered more efficiently in air and water. Until 1990, only a few animals were recognized as being sensitive to UV light, but we now know that a great diversity, possibly even the majority, of animal species can visually detect and respond to it. Here, we discuss the history of research on biological UV photosensitivity and review current major research trends in this field. Some animals use their UV photoreceptors to control simple, innate behaviors, but most incorporate their UV receptors into their general sense of vision. They not only detect UV light but recognize it as a separate color in light fields, on natural objects or living organisms, or in signals displayed by conspecifics. UV visual pigments are based on opsins, the same family of proteins that are used to detect light in conventional photoreceptors. Despite some interesting exceptions, most animal species have a single photoreceptor class devoted to the UV. The roles of UV in vision are manifold, from guiding navigation and orientation behavior, to detecting food and potential predators, to supporting high-level tasks such as mate assessment and intraspecific communication. Our current understanding of UV vision is restricted almost entirely to two phyla: arthropods and chordates (specifically, vertebrates), so there is much comparative work to be done.

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“…Additionally, UVS SWS1 pigments may allow for greater chromatic contrast than VS SWS1 pigments due to increased spectral separation from LWS [25][26][27]. The widespread presence of UVS pigments in various vertebrates and the likelihood that a UVS SWS1 is the ancestral condition [28] suggests UVS pigments may be optimal for most vertebrate species. If correct, this raises the question of why most mammals have VS SWS1 pigments.…”

Section: Introductionmentioning

confidence: 99%

Spectral shifts of mammalian ultraviolet-sensitive pigments (short wavelength-sensitive opsin 1) are associated with eye length and photic niche evolution

et al. 2015

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Retinal opsin photopigments initiate mammalian vision when stimulated by light. Most mammals possess a short wavelength-sensitive opsin 1 (SWS1) pigment that is primarily sensitive to either ultraviolet or violet light, leading to variation in colour perception across species. Despite knowledge of both ultraviolet-and violet-sensitive SWS1 classes in mammals for 25 years, the adaptive significance of this variation has not been subjected to hypothesis testing, resulting in minimal understanding of the basis for mammalian SWS1 spectral tuning evolution. Here, we gathered data on SWS1 for 403 mammal species, including novel SWS1 sequences for 97 species. Ancestral sequence reconstructions suggest that the most recent common ancestor of Theria possessed an ultraviolet SWS1 pigment, and that violet-sensitive pigments evolved at least 12 times in mammalian history. We also observed that ultraviolet pigments, previously considered to be a rarity, are common in mammals. We then used phylogenetic comparative methods to test the hypotheses that the evolution of violet-sensitive SWS1 is associated with increased light exposure, extended longevity and longer eye length. We discovered that diurnal mammals and species with longer eyes are more likely to have violet-sensitive pigments and less likely to possess UV-sensitive pigments. We hypothesize that (i) as mammals evolved larger body sizes, they evolved longer eyes, which limited transmittance of ultraviolet light to the retina due to an increase in Rayleigh scattering, and (ii) as mammals began to invade diurnal temporal niches, they evolved lenses with low UV transmittance to reduce chromatic aberration and/or photo-oxidative damage.

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S cones: Evolution, retinal distribution, development, and spectral sensitivity

Cited by 80 publications

References 248 publications

Express saccades and superior colliculus responses are sensitive to short-wavelength cone contrast

Express saccades and superior colliculus responses are sensitive to short-wavelength cone contrast

Photoreception and vision in the ultraviolet

Spectral shifts of mammalian ultraviolet-sensitive pigments (short wavelength-sensitive opsin 1) are associated with eye length and photic niche evolution

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