- Email: [email protected]
Evolution of Visual Processing in the Human Retina
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Spotlight
Evolution of Visual Processing in the Human Retina Trevor D. Price1,* and Rebia Khan1 Motion detection in humans is based on luminance differences, now shown likely to be processed by a specialized set of cone cells, separate from the cone cells that process color. Humans appear to have evolved a mechanism analogous to that proposed for the double cones of other vertebrates, lost as vision simplified in our nocturnal ancestors. Color, Motion, and Pattern
Loss of Single and Double Cones red ranges, making them tetrachromats). Second, so-called double cones are in Our Ancestors From about 270 million to 65 million years ago, the lineage leading to humans was probably nocturnal (Figure 1), and it was only following extinction of the dinosaurs, that mammals radiated extensively into diurnal habitats [2]. Modern mammals retain many legacies attributed to the long period of nocturnality in their history [2,3], including whiskers, high olfactory sensitivity, and high-frequency hearing, but some of the most striking lie in the visual system [3]. First, color perception was reduced, with only two types of photoreceptor cells involved in color vision (termed cone cells) present in most mammals – one that contains pigment absorbing in the UV[61_TD$IF][0-blue range of the spectrum and the other in the red–green range. By contrast, other diurnal vertebrate species – and the inferred mammalian ancestor – have more than two classes of cone cell involved in color detection (most birds have four, absorbing in the UV, blue, green, and
found in reptiles, birds, amphibians, fish, monotremes, and marsupials, but are absent in placental mammals [4]. Double cones consist of a larger principle cone and a smaller accessory cone, which are coupled. While the double cones appear to be involved in color detection in at least some fish [5], in terrestrial species, including birds and marsupials, they are thought to be dedicated to achromatic tasks including motion detection and pattern recognition [5]. Why have double cones been lost in the placental mammals? Besides the cones, the retina contains photoreceptor cells termed rods, which are present in nearly all vertebrate species and work in low light conditions to process achromatic signals. Rods therefore perform essentially similar functions to the double cones, which work in daylight. In the low light conditions experienced by one of our distant ancestors, we suggest rods outperformed double cones so the double cones were lost.
Visual processing includes the detection of movement, pattern, and color, and integrating all these inputs into a coherent picture of the natural world. However, different perceptual inputs trade off. Notably, separating slightly different colors of objects in natural scenes (we can distinguish at least 7000 [1]) requires summing photons incident on a small patch of the retina across both time and space to reduce inherent error, whereas detection of movement and pattern by definition requires low integration across time and space, respectively. As species have encountered different enemies and prey, and also come to occupy different light environments, so the visual system has evolved within the constraints of this trade-off. As lineages pass through multiple different environments, the visual system has been altered to create a legacy of past adaptations that affect the subsequent course of evolution (historical contingency), and hence how this fundamental trade-off has been resolved. These principles are exemplified by the evolutionary route that has led to the Figure 1. Timeline of Evolution along the Human Lineage from 300 Mya. Adapted from [2,6]. way humans process visual signals.
Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
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The presence of both single and double cones in most taxa illustrates the value of separating color detection from pattern and motion detection, right down to the level of the retina. As placental mammals emerged into diurnal habitats without double cones, the cone cell containing long wavelength (red to green) absorbing pigment now performs the function of motion and pattern detection. Accordingly, these cells comprise 90% of all cone cells. In dichromats, some color perception is achieved by comparing the output from the short-wavelength cone cells to that from the long-wavelength cones, and the basic tasks of color and motion and pattern detection remain largely separated.
Improved Color Vision in Primates
of how the different requirements for color, motion and pattern detection have been resolved given the two cone cell classes. In a remarkable study, Sabesan et al. [9] have shown that in fact the longand medium-wavelength-sensitive cone cells are themselves likely to be split into two classes: those that respond to achromatic signals and those that are used for color detection.
Identifying Achromatic and Chromatic Signals Sabesan et al. stimulated single middleand long-wavelength cone cells of two humans and asked the individuals to report what they saw [9]. To do this, they had to overcome numerous technical challenges. Getting accurate locations for cone cells is difficult because the eye moves even while viewing a stationary object. Furthermore, because any light aimed at the retina has to go through the whole eyeball, optic aberrations make it difficult to get accurate images of the
retina or stimulate it at a cellular level. Through high-speed retinal tracking and adaptive optics that corrected for light aberration, Sabesan et al. targeted 273 cone cells in two test individuals, having first mapped the cells and identified their type [7]. For many of the cells stimulated, the test individuals reported seeing white light rather than color. Indeed, the majority (77% of the middle- and 66% of the long-wavelength-sensitive cones) fell in the achromatic category. Individual cone cells produced similar responses when tested multiple times, even in trials months apart [9] (Figure 2). Sabesan et al. reasonably interpreted these results to show that two classes of middle- and long-wavelength cone cells in the human retina are separately wired to perform achromatic and chromatic tasks. Separation of the achromatic and chromatic channels is reminiscent of the division in the retina into double and single cones
Most mammals are dichromats, but we and our immediate primate relatives are trichromats, resulting from a duplication of the long-wavelength-sensitive opsin gene, now dated to 30 million years ago [6], establishing middle- alongside long-wavelength-sensitive cone cells. Together these continue to make up 90% of our cone cells [7], but the relative proportions of middle- and long-wavelength cells can be highly variable between individuals. The difference in peak wavelength of absorbance of these cone cell classes is small (only 30 nm, compared with the short- to middlewavelength absorbance difference of 100 nm). One consequence is that comparison of outputs from the middleand long-wavelength class of cone cells enables especially fine discrimination in the red–green part of the spectrum – an experimentally demonstrated outcome is improved detection of colored fruits against green leaves [8]. Primates con- Figure 2. Color Responses of Cones in a Small Part of the Retina of a Human Individual (from [9]). tinue to use summed outputs from both Cone cells in the retina absorb in the short wavelengths (indicated here in blue), medium wavelengths (green), or longer wavelengths (red). Retinal make-up was first mapped using bleaching experiments that exposed the middle- and long-wavelength- each cell to a monochromatic light [7]. Targeted cones have a center that shows the cone type, and outer circle absorbing cones for motion and pattern that gives the fraction of times the individual reported a red, green, or white sensation when the cone was detection, presumably because they pre- stimulated (nontargeted cones are out of focus). Each cone was stimulated 20 times per trial. Sixty cones were targeted in at least two trials, which were sometimes many months apart. Note that for most cones a single viously formed the single class of longsensation predominates. A lack of complete concordance in responses for a given cone cell is attributed to wavelength-absorbing cells that were known experimental error, because on occasion an adjacent cone cell is stimulated [9]. Scale bar is 11.5 mm. used in this way. This raises the question Reproduced with permission of the American Association for the Advancement of Science.
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Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
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different. The results also have important implications for the separation of achromatic and chromatic processes in the evolution of vision. They suggest that the placental mammal system has repurposed its color perception system to do the task ancestral double cones once did. The gerrymandering of existing systems to achieve this ancestral separation suggests that there is an inherent value These findings have many implications for in keeping distinct paths for chromatic our understanding of the evolution of and achromatic detection. color vision in animals. Some models assume that cone abundance is a critical 1Department of Ecology and Evolution, University of variable in determining color perception, Chicago, Chicago IL 60637, USA because the more cells involved, the *Correspondence: [email protected] (T.D. Price). greater should be the sensitivity [10]. http://dx.doi.org/10.1016/j.tree.2017.09.001 The red–green channel in humans has greater sensitivity than the blue channel References 1. Marin-Franch, I. and Foster, D.H. (2010) Number of per[10], but it now may be that the number of ceptually distinct surface colors in natural scenes. J. Vis. 10, 1–7 cone cells involved in color detection is no
inferred for our ancient ancestors. Although not previously suspected, it is consistent with the inherent conflict between resolution and sensitivity. The evolution of trichromacy in primates 30 million years ago certainly improved color perception, but might well have come at a cost of reduced spatial and temporal resolution.
2. Gerkema, M.P. et al. (2013) The nocturnal bottleneck and the evolution of activity patterns in mammals. Proc. R. Soc. Lond. B 280, 20130508 3. Heesy, C.P. and Hall, M.I. (2010) The nocturnal bottleneck and the evolution of mammalian vision. Brain Behav. Evol. 75, 195–203 4. Bowmaker, J.K. (2008) Evolution of vertebrate visual pigments. Vision Res. 48, 2022–2041 5. Pignatelli, V. et al. (2010) Double cones are used for colour discrimination in the reef fish, Rhinecanthus aculeatus. Biol. Lett. 6, 537–539 6. dos Reis, M. et al. (2012) Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc. R. Soc. Lond. B 279, 3491–3500 7. Sabesan, R. et al. (2015) Characterizing the human cone photoreceptor mosaic via dynamic photopigment densitometry. PLoS One 10, e0144981 8. Caine, N.G. and Mundy, N.I. (2000) Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proc. R. Soc. Lond. B 267, 439–444 9. Sabesan, R. et al. (2016) The elementary representation of spatial and colour vision in the human retina. Sci. Adv. 2, e1600797 10. Vorobyev, M. and Osorio, D. (1998) Receptor noise as a determinant of colour thresholds. Proc. R. Soc. Lond. B Biol. Sci. 265, 351–358
Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
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Spotlight
Evolution of Visual Processing in the Human Retina Trevor D. Price1,* and Rebia Khan1 Motion detection in humans is based on luminance differences, now shown likely to be processed by a specialized set of cone cells, separate from the cone cells that process color. Humans appear to have evolved a mechanism analogous to that proposed for the double cones of other vertebrates, lost as vision simplified in our nocturnal ancestors. Color, Motion, and Pattern
Loss of Single and Double Cones red ranges, making them tetrachromats). Second, so-called double cones are in Our Ancestors From about 270 million to 65 million years ago, the lineage leading to humans was probably nocturnal (Figure 1), and it was only following extinction of the dinosaurs, that mammals radiated extensively into diurnal habitats [2]. Modern mammals retain many legacies attributed to the long period of nocturnality in their history [2,3], including whiskers, high olfactory sensitivity, and high-frequency hearing, but some of the most striking lie in the visual system [3]. First, color perception was reduced, with only two types of photoreceptor cells involved in color vision (termed cone cells) present in most mammals – one that contains pigment absorbing in the UV[61_TD$IF][0-blue range of the spectrum and the other in the red–green range. By contrast, other diurnal vertebrate species – and the inferred mammalian ancestor – have more than two classes of cone cell involved in color detection (most birds have four, absorbing in the UV, blue, green, and
found in reptiles, birds, amphibians, fish, monotremes, and marsupials, but are absent in placental mammals [4]. Double cones consist of a larger principle cone and a smaller accessory cone, which are coupled. While the double cones appear to be involved in color detection in at least some fish [5], in terrestrial species, including birds and marsupials, they are thought to be dedicated to achromatic tasks including motion detection and pattern recognition [5]. Why have double cones been lost in the placental mammals? Besides the cones, the retina contains photoreceptor cells termed rods, which are present in nearly all vertebrate species and work in low light conditions to process achromatic signals. Rods therefore perform essentially similar functions to the double cones, which work in daylight. In the low light conditions experienced by one of our distant ancestors, we suggest rods outperformed double cones so the double cones were lost.
Visual processing includes the detection of movement, pattern, and color, and integrating all these inputs into a coherent picture of the natural world. However, different perceptual inputs trade off. Notably, separating slightly different colors of objects in natural scenes (we can distinguish at least 7000 [1]) requires summing photons incident on a small patch of the retina across both time and space to reduce inherent error, whereas detection of movement and pattern by definition requires low integration across time and space, respectively. As species have encountered different enemies and prey, and also come to occupy different light environments, so the visual system has evolved within the constraints of this trade-off. As lineages pass through multiple different environments, the visual system has been altered to create a legacy of past adaptations that affect the subsequent course of evolution (historical contingency), and hence how this fundamental trade-off has been resolved. These principles are exemplified by the evolutionary route that has led to the Figure 1. Timeline of Evolution along the Human Lineage from 300 Mya. Adapted from [2,6]. way humans process visual signals.
Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
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TREE 2300 No. of Pages 3
The presence of both single and double cones in most taxa illustrates the value of separating color detection from pattern and motion detection, right down to the level of the retina. As placental mammals emerged into diurnal habitats without double cones, the cone cell containing long wavelength (red to green) absorbing pigment now performs the function of motion and pattern detection. Accordingly, these cells comprise 90% of all cone cells. In dichromats, some color perception is achieved by comparing the output from the short-wavelength cone cells to that from the long-wavelength cones, and the basic tasks of color and motion and pattern detection remain largely separated.
Improved Color Vision in Primates
of how the different requirements for color, motion and pattern detection have been resolved given the two cone cell classes. In a remarkable study, Sabesan et al. [9] have shown that in fact the longand medium-wavelength-sensitive cone cells are themselves likely to be split into two classes: those that respond to achromatic signals and those that are used for color detection.
Identifying Achromatic and Chromatic Signals Sabesan et al. stimulated single middleand long-wavelength cone cells of two humans and asked the individuals to report what they saw [9]. To do this, they had to overcome numerous technical challenges. Getting accurate locations for cone cells is difficult because the eye moves even while viewing a stationary object. Furthermore, because any light aimed at the retina has to go through the whole eyeball, optic aberrations make it difficult to get accurate images of the
retina or stimulate it at a cellular level. Through high-speed retinal tracking and adaptive optics that corrected for light aberration, Sabesan et al. targeted 273 cone cells in two test individuals, having first mapped the cells and identified their type [7]. For many of the cells stimulated, the test individuals reported seeing white light rather than color. Indeed, the majority (77% of the middle- and 66% of the long-wavelength-sensitive cones) fell in the achromatic category. Individual cone cells produced similar responses when tested multiple times, even in trials months apart [9] (Figure 2). Sabesan et al. reasonably interpreted these results to show that two classes of middle- and long-wavelength cone cells in the human retina are separately wired to perform achromatic and chromatic tasks. Separation of the achromatic and chromatic channels is reminiscent of the division in the retina into double and single cones
Most mammals are dichromats, but we and our immediate primate relatives are trichromats, resulting from a duplication of the long-wavelength-sensitive opsin gene, now dated to 30 million years ago [6], establishing middle- alongside long-wavelength-sensitive cone cells. Together these continue to make up 90% of our cone cells [7], but the relative proportions of middle- and long-wavelength cells can be highly variable between individuals. The difference in peak wavelength of absorbance of these cone cell classes is small (only 30 nm, compared with the short- to middlewavelength absorbance difference of 100 nm). One consequence is that comparison of outputs from the middleand long-wavelength class of cone cells enables especially fine discrimination in the red–green part of the spectrum – an experimentally demonstrated outcome is improved detection of colored fruits against green leaves [8]. Primates con- Figure 2. Color Responses of Cones in a Small Part of the Retina of a Human Individual (from [9]). tinue to use summed outputs from both Cone cells in the retina absorb in the short wavelengths (indicated here in blue), medium wavelengths (green), or longer wavelengths (red). Retinal make-up was first mapped using bleaching experiments that exposed the middle- and long-wavelength- each cell to a monochromatic light [7]. Targeted cones have a center that shows the cone type, and outer circle absorbing cones for motion and pattern that gives the fraction of times the individual reported a red, green, or white sensation when the cone was detection, presumably because they pre- stimulated (nontargeted cones are out of focus). Each cone was stimulated 20 times per trial. Sixty cones were targeted in at least two trials, which were sometimes many months apart. Note that for most cones a single viously formed the single class of longsensation predominates. A lack of complete concordance in responses for a given cone cell is attributed to wavelength-absorbing cells that were known experimental error, because on occasion an adjacent cone cell is stimulated [9]. Scale bar is 11.5 mm. used in this way. This raises the question Reproduced with permission of the American Association for the Advancement of Science.
2
Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
TREE 2300 No. of Pages 3
different. The results also have important implications for the separation of achromatic and chromatic processes in the evolution of vision. They suggest that the placental mammal system has repurposed its color perception system to do the task ancestral double cones once did. The gerrymandering of existing systems to achieve this ancestral separation suggests that there is an inherent value These findings have many implications for in keeping distinct paths for chromatic our understanding of the evolution of and achromatic detection. color vision in animals. Some models assume that cone abundance is a critical 1Department of Ecology and Evolution, University of variable in determining color perception, Chicago, Chicago IL 60637, USA because the more cells involved, the *Correspondence: [email protected] (T.D. Price). greater should be the sensitivity [10]. http://dx.doi.org/10.1016/j.tree.2017.09.001 The red–green channel in humans has greater sensitivity than the blue channel References 1. Marin-Franch, I. and Foster, D.H. (2010) Number of per[10], but it now may be that the number of ceptually distinct surface colors in natural scenes. J. Vis. 10, 1–7 cone cells involved in color detection is no
inferred for our ancient ancestors. Although not previously suspected, it is consistent with the inherent conflict between resolution and sensitivity. The evolution of trichromacy in primates 30 million years ago certainly improved color perception, but might well have come at a cost of reduced spatial and temporal resolution.
2. Gerkema, M.P. et al. (2013) The nocturnal bottleneck and the evolution of activity patterns in mammals. Proc. R. Soc. Lond. B 280, 20130508 3. Heesy, C.P. and Hall, M.I. (2010) The nocturnal bottleneck and the evolution of mammalian vision. Brain Behav. Evol. 75, 195–203 4. Bowmaker, J.K. (2008) Evolution of vertebrate visual pigments. Vision Res. 48, 2022–2041 5. Pignatelli, V. et al. (2010) Double cones are used for colour discrimination in the reef fish, Rhinecanthus aculeatus. Biol. Lett. 6, 537–539 6. dos Reis, M. et al. (2012) Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc. R. Soc. Lond. B 279, 3491–3500 7. Sabesan, R. et al. (2015) Characterizing the human cone photoreceptor mosaic via dynamic photopigment densitometry. PLoS One 10, e0144981 8. Caine, N.G. and Mundy, N.I. (2000) Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proc. R. Soc. Lond. B 267, 439–444 9. Sabesan, R. et al. (2016) The elementary representation of spatial and colour vision in the human retina. Sci. Adv. 2, e1600797 10. Vorobyev, M. and Osorio, D. (1998) Receptor noise as a determinant of colour thresholds. Proc. R. Soc. Lond. B Biol. Sci. 265, 351–358
Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
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