Our Senses: An Immersive Experience - Rob DeSalle 2018
The Eyes Have It: The Limits of Sight in Humans
“The eye sees only what the mind is prepared to comprehend.”
—Henri Bergson, philosopher
Go to the theater or a concert, and you will most likely see a wide range of people with differing levels of visual acuity. There will be people with and without glasses. Those without glasses may be wearing contact lenses or have had corrective eye surgery. Some of those with eyewear might need very thick lenses, while others need glasses only to read the program. There will be people without glasses reading things far from the stage. There might even be a blind person or two in the crowd. All these are obvious vision differences among humans. Some exist because of accidents or because of environmental exposure or disease, and others are congenital. But there is a lot of other variation in seeing that you wouldn’t outwardly recognize at this performance. A small proportion of the men in the audience will not be able to discern between red and green, and some of the women might be seeing shades of red that only they are used to seeing. Some individuals might have tunnel vision (poor peripheral vision), and still others might need to limit the amount of light hitting their eyes and so wear sunglasses. All of this variation is related to how vision works (fig. 9.1).
Figure 9.1. Structure of the eye and the retina.
In the eye of a mammal, the path of light to the retina travels along a theoretical line called the visual axis. This is a straight line from the object being observed to the center of the fovea. Along the way to the retina, the light from the object travels through the following layers of compounds and structures. First, it passes through a tear film that covers the eye. This filmy coating protects, lubricates, and keeps the eye surface clear. Next is the cornea, which looks like a clear sheet of tissue but is quite complex, with several specialized layers. The cornea focuses more than half of the light entering the eye. The anterior chamber comes next. This structure is filled with fluid and abuts the following eye part along the visual axis, the iris, which assists in controlling the size of the pupil. The iris is pigmented and is what we refer to when we say a person has deep blue eyes or sexy green eyes or astonishing brown eyes. The next structure along the visual axis, the pupil, is a structure that can expand in diameter to allow more light in to the rest of the eye, or it can contract to restrict the amount of light going along the visual axis. The lens comes next. It is convex and helps to focus light along the visual axis on the retina. Between the lens and the retina is a large structure called the vitreous, through which the light on the visual axis has to pass before hitting the retina. The last structure of the eye in most mammals is the retina.
People with super vision are rarely reported, and these are of such dubious quality that they usually become Internet memes, complete with discussions of the veracity of the claims. Two recent cases are particularly interesting, because—whether they are true or not—they lead us to information about the limits of human vision.
The first super vision story concerns a woman from Germany named Veronica Seider. In the 1970s, Seider was heralded as the human with the best eyesight on the planet because she claimed to be able to see detail on objects more than a mile away. She reportedly could even identify people from that distance, and her vision was thought to be 20/2, perhaps even 20/1. Most humans have 20/20 vision (or 6/6, if you are used to the metric system), which means that they can see objects clearly at 20 feet. If someone has 20/200 vision, this means that an object would need to be 20 feet away for that individual to see detail that a 20/20 person would see at 200 feet. In other words, the 20/200 person has clear vision only one-tenth of most people. Seider’s 20/2 vision means that what she could see clearly at 20 feet would have to be viewed at 2 feet by an average person for it to be clear. So, her vision would be about ten to twenty times better than the average human vision, close to if not exceeding the visual acuity of some birds of prey that are at 20/2.
Baseball players who rely heavily on visual acuity when batting need to recognize the speed and spin of the ball well before it reaches the plate to judge where to swing the bat to make contact with the ball. For instance, it has been estimated that misjudging the speed of a pitch by a slight 2.5 miles per hour will result in a swing either 12 inches too soon or 12 inches too late. Different pitches look different to the great hitters. To me, a speeding baseball or a curveball or a forkball or a changeup all look like a blur no matter what is thrown at me (which is why my baseball career ended in high school). But to Wade Boggs or the great Ted Williams, a fastball looks white, a slider looks as if it has a red dot on it, and a curveball appears to have tumbling stripes. Some hitters attain a state of baseball nirvana called precise foveal fixation when hitting. This state is where the hitter is seeing the ball with such precision that judging where it will cross the plate is a snap, and being in this zone apparently does produce a euphoric response. The fovea is an incredibly tiny region of the retina where the most focused, distinct, and detailed vision is received, and it is responsible for foveal fixation. It is best described by the following well-known test. Look at the figures below and focus on the registration symbol (®) for a few seconds, and without losing the focus on that symbol, try to get a sense of how you are seeing the other figures to its right and left.
ϒ H ∏ M ∇ ⊗ ® ℜ Ψ Ω ℑ K ξ П
If you did this correctly, the figures to the right and left of that symbol became a bit blurry. This is because you have focused the registration symbol with the foveal region of your retina, and this is the only thing you are seeing in true 20/20 vision. There is something very special about how the fovea is structured that is essential to understanding vision.
The second Internet meme is the Chinese Cat Boy, whose real name is Nong Youhui. This little boy was reported in 2012 to be able to see clearly in the dark and to have eyes that shine in the dark much like a cat’s. Alien conspiracy theorists quickly picked up the story (which is the danger of the Internet), and so the information about Nong is a bit muddled. It is clear, however, that Nong can see quite well in the dark. His shining eyes are the result of a lack of pigment cells in the eye caused by a disorder called ocular albinism. Animals with exceptionally good night vision, such as cats, do have a reflective layer of tissue associated with their retina called a tapetum lucidum that allows the retina to capture more light. The tapetum lucidum reflects light, and so it glows in the dark, but Nong’s eyes do not glow because he has a tapetum lucidum. There is no connection genetically or anatomically between ocular albinism and the existence of a tapetum lucidum.
Another eye-related change that animals with night vision have is an increase in the number of cells in the retina. The retina is made up of thousands of small rod- and cone-shaped cells, or rods and cones. Cats have many more rod cells in their retinas, and while Nong’s retina was not examined, it is a pretty good bet that he has a significantly larger number of rod cells in his eyes. After hearing these two Internet-based stories I hope you are now curious about the structure of the retina and what these rod and cone cells are and do.
Although the vertebrate eye is complex, with lots of structures used to focus and filter light, the retina is where most of the action occurs with vision, so it is worth describing its structure in detail. To start, remember that the retina is where the action potentials that send the electrical messages to the brain initiate (see Chapter 10 for where these signals end up in the brain).
The retina is literally a field of two kinds of specialized photoreceptor cells, rods and cones, all connected directly to the brain. In fact, many neurologists consider the retina as part of the brain. How these rods and cones are distributed in the retina and what kind of light they are built to detect determines most of what happens with vision. (There is actually a third kind of photoreceptor cell in the retina, the photosensitive retinal ganglion cells [pRGC]. These cells were discovered about a hundred years ago in blind mice. They will react to light even when the rods and cones are missing or incapacitated. The pRGCs are involved in circadian rhythm maintenance and are only peripherally involved in seeing.)
Visual acuity or resolving power is the job of the cone cells, and the fovea, which is the seat of acuity, is packed with cone cells only. The more cone cells there are in the fovea, the more it is functionally aligned with resolution or acuity. This is also where we pick up the best color resolution in the visual system. Assuming that color vision and acuity are connected in some way would be jumping to the wrong conclusion, though. Even though they are both jobs of the cone cells, they are different phenomena.
When there is low light and hence no need for color detection or strong acuity, the rods take over. Not surprisingly, the best low-light vision is away from the fovea and out toward the periphery of the retina, where all the rods reside.
Rod and cone cells are packed closely together in the retina. The ends of these cells that face toward the outer world are packed with proteins that are embedded in the cell membrane and face outward. These specialized photoreceptor proteins are called opsins, and they are structured much like the chemoreceptors introduced in the beginning of this chapter. There are seven transmembrane domains that wind in and out of the cell membrane to anchor the opsin in the rod or cone. As with chemoreceptors, there is a beginning part of the protein lying on the outside of the cell and a little tail of the protein on the inside of the cell. Connected to the interior of the protein, where the seven domains spanning the membrane reside, sits snuggled into the protein a small chromophore molecule called 11-cis-retinal. This chromophore is photoreactive in that when it is struck by a photon of a specific wavelength it will isomerize (change shape but not chemical makeup) and boot itself out of its cozy home in the opsin. In its isomer state the retinal ceases to fit in the opsin’s home for it. This eviction event in turn results in the opsin changing conformation and triggering the same kind of G protein reactions we saw with chemoreception when I discussed smell and taste.
Human opsins are a large and diverse set of proteins coded for by genes in the human genome. There are nine major types, but not all are involved in the visual system. The relevant opsins for vision are rhodopsin, red opsin, green opsin, and blue opsin. Important to the story of super color vision in humans is that the green and red opsins reside right next to each other on the X chromosome in the human genome. Blue opsins are located on human chromosome 7, and rhodopsin, the final opsin involved in color vision, is found on chromosome 3.
Light, which is both wavelike and particlelike, consists of photons that can have specific wavelengths. For any photon of a specific wavelength there is an opsin that will react to it. Other opsins will simply sit there and wait until a photon of wavelength that they like hits them. So, for instance, any photons hitting the retina with a wavelength of 557 nanometers (visible light has extremely small wavelength) will hit all kinds of cells in the retina, but only the opsin in cone cells responsible for red color vision will be shaken up. On the other hand, if the photon has a wavelength of 420 nanometers, it will again hit all kinds of rod and cone cells in the retina as well a lot of opsins, but only the blue color opsin in cones will react to it. Oddly, if there is very little light hitting the retina (in other words, it is dark), all of the cone opsins shut down and the rod opsin, a rhodopsin, goes to work. It reacts with photons with wavelengths of about 505 nanometers and interprets the photoreaction and subsequent phototransduction (the signal to the brain) as blue-green color. This is why any night vision that we might have is relatively colorless. Of course, light coming to our eyes exists in a range of wavelengths and not just at 557, 420, or 505 nanometers. So, while photons of wavelength 557 nanometers are what a red-cone opsin reacts to optimally, the opsin will still react, but in a less enthusiastic manner, with light of, say, 550 nanometers. In fact, the red-cone opsin will react with light all the way down to 500 nanometers, but again not as enthusiastically as it would with light at 557 nanometers. The enthusiasm with which the opsin reacts determines the degree with which the G coupled cascade will send messages to the brain and affects how different shades of red or green or blue are detected by the cone cells in the retina.
By looking at the genomes of a lot of people and knowing what kind of color vision they have, researchers have discovered that there are multiple kinds of opsins for both the red-green kind and the blue kind in the cone cells. The different kinds of red-green opsins are called long-wave variants, and there are two major ones: LW (long wave) and MW (medium wave). There is one short wave (SW) for the blue opsin.
The evolution of the LW, MW, and SW genes is a fascinating story. Human variation in seeing colors is best understood by considering the distribution of opsins in organisms in the tree of life. Some bacteria have opsin genes and use these genes as a source of energy from light. The one commonality of opsins across all organisms that have them is that they use a small molecule called retinal as a partner in function. Because light isomerizes retinal, the change in shape of this small molecule has been exploited for many tasks in the tree of life. Plants don’t have opsins, nor do some very primitive animals, such as sponges and the pancake-shaped placozoans. But neither of those two early diverging animals nor plants even have nerves, let alone a brain. Cnidarians such as jellyfish, corals, and hydras have light organs and opsins. Ctenophores, the comb jellies, have opsins, too. In some cases, these organisms have a neural net and large numbers of opsins, suggesting that they are detecting broad ranges of light. The box jellyfish, a box-shaped cnidarian cubazoan, has eighteen opsin genes and a complex light-sensing organ that even has a lens!
But it is in vertebrates where the opsin genes really took hold. Although those squishy organisms that immediately precede vertebrates in the tree of life such as sea urchins, sea squirts, and acorn worms have a small repertoire of opsin genes (less than five), vertebrates such as fish, frogs, lizards, and birds all have a much larger number (sometimes more than twenty).
How did the number of opsins jump to twenty? If the animals leading to vertebrates had five or so opsins, then the common ancestor of vertebrates had to have at most five opsins, too. This larger number of opsin genes coincides with a special event in vertebrate evolution, which gives a clue to one way that new genes are generated in the genomes of organisms.
The common ancestor of tunicates (a sea squirt and a hemichordate) and vertebrates again had five opsins. As the tunicates diverged, they maintained the five or fewer gene state. But in the common ancestor of all vertebrates (a different ancestor than the tunicate-vertebrae common ancestor), the entire genome duplicated itself, not once but twice. Whole genome duplications in plants are pretty common (polyploidy abounds in plants), but in animals they are rare. So, this rare double duplication of the genome resulted in the multiplying of the genes in the genomes of vertebrates.
But a funny thing happened on the way to mammals. The number of opsin genes was reset at eight. The platypus, a monotreme and the closest relative to marsupials and mammals, has eleven opsins. So, gradual loss of opsin genes is more than likely how mammals ended up with eight. Alternatively, the platypus might have gained some opsin genes by a process called gene duplication (as opposed to whole genome duplication). This resetting of the number of opsin genes in mammals is not so surprising, given that the ancestral mammal was more than likely nocturnal and had no use for a large repertoire of light-sensing molecules. Eight opsin genes seems to be the sweet spot for mammals, although humans usually have nine in our genomes. So, an even funnier thing happened on the way to primates (box 9.2). The eight opsin genes of the ancestral primate included a rhodopsin, an L/M opsin, and an S opsin, which are involved in color vision. The L/M opsin is a single opsin that has two forms—the L form and the M form.
Of the nine opsins in the human genome, rhodopsin, the S opsin on chromosome 7, and the two opsins on the X chromosome (L and M) are involved in color vision. Humans need all three opsins to be expressed in their cone cells for normal color vision and hence are normally trichromatic. But each opsin can be mutated so that it is nonfunctional, has diminished function, or reacts to a variant wavelength of light. Another possibility is that hybrid opsins can arise as a result of an L opsin (red) gene mixing it up with a green M opsin gene. Because the two genes are similar in their sequences, they can often align themselves across from each other on the X chromosome and a recombination event can occur, producing two products, one with a red gene front end and a green gene back end and one with a green gene front end and a red gene back end.
BOX 9.1 | OUR GENOME
Every human cell in the human body has twenty-three pairs of chromosomes. There are twenty-two pairs of what are called autosomes, numbered from 1 to 22 (the largest chromosome in terms of amount of DNA on it is numbered 1 and the smallest is numbered 22). Autosomes are the collection of chromosomes generally not involved in sex determination. The final or twenty-third pair are the sex chromosomes; in females, there are two of the same kind of chromosome, called X chromosomes. (The X chromosome is one of the larger chromosomes in our genomes with two thousand or so genes.) In males, there is a single X chromosome with its two thousand genes and another smaller chromosome with fewer than one hundred genes called the Y chromosome. Most of the genes on the X chromosome are not found on the Y, so males have only one copy of any gene that resides on the X chromosome.
All of these possibilities result in a parade of ways that color vision can be deficient in males, because of the X-linked nature of L and M. With two loci on different chromosomes involved and the only combination that gives trichromatic vision (having at least one L, M, and S), several other gene combinations can occur where color vision will be deficient. Males with normal color vision, or trichromatic vision, would be
LM/Y S/S
or
LM/Y S/z,
where the LM/Y represents the opsin genes from your mother’s X chromosome and your father’s Y chromosome, which lacks an opsin. The z indicates that the opsin is nonfunctional or missing. The S/S and S/z notations indicate the possible opsin combinations from chromosome 7, one from each parent. If you are unlucky enough to be a male with no functioning L, M, and S genes (again represented by a z), genetically you would be zz/Y z/z, and you would be what is called monochromatic and unable to discern color at all. In other words, your cone cells have no opsins at all. You would still have some vision because you would have rhodopsin in your rod cells, but you would lead a very dark and shadowy visual life. This is a condition that actually exists in a large number of individuals on the Micronesian island of Pingelap. Other ways to be a male monochromatic would be
Lz/Y z/z,
zM/Y z/z,
zz/Y S/S, or
zz/Y S/z.
In two cases, the opsin genes from your mother’s X chromosome have only an L (Lz/Y z/z) or an M opsin (zM/Y z/z), or in other words, only one opsin instead of the normally linked two, and you would see the world basically in black and white. In the cases of zz/Y S/S and zz/Y S/z, the cone cells would have only a single kind of opsin (S) in them, and this would produce an extreme black and white world. Females have more chances to make up for missing X chromosomal opsins, and so the frequency of monochromatic effects in females is much lower than in males. Dichromatic males are much more common in many populations. For instance, about one in ten males of northern European descent has one of the following genotypes:
Lz/Y S/S,
Lz/Y S/s,
zM/Y S/S, or
zM/Y S/s,
and therefore has two opsins in their cone cells. Such individuals are called dichromatic and cannot discern different combinations of colors depending on which opsins are mixed up, most commonly having red-green color blindness.
There are three major dichromatic states: protanopia, deuteranopia, and tritanopia. Protanopes are those individuals who have no functioning M opsins (Lz/Y S/S or Lz/Y S/s) and hence no red cone cells. Deuteranopes lack functional L opsin proteins (zM/Y S/S or zM/Y S/s) and thus have no green cone cells. Tritanopes are extremely rare; they lack blue cone cells as a result of nonfunctional S opsins (LM/Y z/z). All of these opsin gene arrangements in humans produce diminished color vision. But there are also some opsin gene arrangements that produce what is called anomalous trichromacy. These are individuals with three opsin types and hence three kinds of cone cells, but one of the opsins is that hybrid L/M gene I introduced earlier. Such individuals are usually males and see in three colors, but the three colors are slightly altered from what a normal trichromat would see.
Note that the color vision system so far describes losses of genes through mutation or even complete deletion, but the opposite can occur. The addition of a functional opsin gene or two to the genomic repertoire is also a possibility. Many animals have added opsin genes to their color perception repertoire to enhance their color detection capacities. And these are not simple additions of opsins outside the color detection range (400 to 700 nm) of humans. That’s not to say that many insects and other animals have not added mechanisms for detecting outside of the range of 400 to 700 nanometers.
As noted previously, simple mutations in the opsin genes can change the wavelength of light to which the opsin will maximally respond. If an organism has an opsin that responds best to 560 nanometers, the opsins will maximally respond to light of that wavelength and less so to other wavelengths. Organisms can see color at wavelengths other than the optimal wavelength for their opsin. But if an opsin is added that is specific for a wavelength not covered by the normal opsins, then color vision is accentuated for the wavelength optimal for that added opsin, enriching the color detection of the organism.
For instance, butterflies and crustaceans called stomatopods have taken the game to its limits. Some butterflies are tri- and tetrachromatic but have added extra opsins to fine-tune the color detected. Colias or sulphur butterflies have seven color vision opsins, several of which are simply add-ons that act slightly differently. The crustacean stomatopods have an amazing twenty color vision opsins. But they also have six opsins that detect polarized light and two that detect luminescence. The twenty color opsins mean that at least twelve wavelengths are specific for an opsin in these organisms, giving stomatopods color acuity that both dissects and amplifies the usual trichromatic color vision.
Such additions to the human genome in opsin genes would produce what scientists call tetrachromatic individuals. These people would have four kinds of cone cells and would occur mostly in females (since males have only one chance to get the L and M opsins right because they have a single X chromosome). Males are much more likely to have fewer opsin genes than the normal trichromatic state. And females have two chances because they have two Xs, increasing the possibility of being a tetrachromat. Such individuals would have an extra kind of cone cell and would theoretically be able to see more colors than trichromats, who can already discern among millions of colors.
Very few cases of human tetrachromats are documented, and even when a tetrachromat is verified at the genome level, it is difficult to identify the range of color vision these women might have. Having four kinds of cone cells doesn’t mean that a brain will interpret what these cone cells detect as different colors, or so the argument goes. Oddly enough, the search for tetrachromatic women usually begins by searching for men with altered color vision. These men are the anomalous trichromats from above. The reasoning is that the mothers of such men gave an X chromosome to their sons that has the anomalous recombinant opsin on it that leads to the fourth kind of cone cell. If the mother also has normal L and M opsin genes on her other X chromosome and two normal S opsins on the two chromosome 7s in her genome, then she will make four cone cells: L, M, and S opsins and the L/M opsin (the recombinant gene which she transmitted to her anomalous trichromatic son). She would potentially be able to have four distinct general wavelengths of light that she could discern with her eyes.
Finding potential tetrachromats is not too difficult. These are usually women who self-identify as having extraordinary color vision. There is a simple test to determine if they have the genomic capacity for tetrachromatic color vision, and that is to sequence the opsin gene loci on their X chromosomes and make the call from there. Finding genomic tetrachromats is much more difficult, even though some researchers suggest that up to 2 percent of females on the planet are tetrachromats. There are some compelling web-based stories about women with tetrachromatic vision in the context of art, but these cases are rare. Even when genomic tetrachromats are found, sometimes they simply do not have any better color vision than trichromats. In 2010, Gabi Jordan and colleagues examined a relatively large population using the anomalous trichromat approach and found twenty-four females who were genomic tetrachromats, but after several color vision tests were administered, only one of them could be found to have anything close to tetrachromatic vision.
BOX 9.2 | COLOR VISION IN MONKEYS
There is an especially interesting arrangement for the males of a species of catarrhine (Old World) monkeys. These male monkeys have sex chromosomes—one X and one Y. The L/M opsin is on the X, and so the males of this kind of monkey have only a single copy of the L/M opsin, and they get either an L opsin or an M opsin by the luck of the draw. This state of having one L or M opsin and an S opsin is called dichromacy. Either way, the males in this species can see only two kinds of color, because they have only two kinds of cone cells in the retina. Females, on the other hand, will have two opsins, and in some cases they will get a mixed L and an M opsin, and this allows them to have three-color vision, or trichromacy. In addition, some females will be either M/M or L/L and will see only two kinds of color. Males are obligate dichromats, whereas females are trichromats and dichromats. In any given population of catarrhine monkeys, then, there are three color views of the world: a dichromatic M world, a dichromatic L world, and a trichromatic world.
Kimberley Jameson and colleagues evaluated four human subjects to compare artists’ ability and the possible role of tetrachromatic vision that might be associated with that ability. They constructed an experiment in which a comparison is made between two states for each of two variables: an artist-tetrachromat, an artist-trichromat, a nonartist-tetrachromat, and a nonartist trichromat. They then addressed three basic questions with this design by comparing how the four different individuals responded to color vision tests:
• Does the genomic makeup of an individual influence color vision? This test simply compared the artist-tetrachromat and the nonartist-tetrochromat to the artist-trichromat and the nonartist-trichromat. If enhanced color vision was found when there are four opsin genes versus three, then it has a genomic component.
• Does artistic training influence color vision? In this test, the artist-trichromat and artist-tetrochromat were compared with the nonartist-trichromat and the nonartist-tetrochromat.
• Last, do training and genomic makeup influence enhanced color vision? This test involved comparing the artist-tetrochromat and the nonartist-trichromat with the artist-trichromat and the nonartist tetrochromat.
Only the second test was not significant, indicating that art training is not sufficient to enhance color vision. The other two tests indicate that there is a genomic component and that training and genomic component are synergistic. The obvious caveat to this study is the number of individuals examined, but as a first try at understanding tetrachromatic color vision enhancement it set the bar pretty high.
Modern humans are thus quite variable for color vision. But can we make predictions about our close extinct relatives, such as Neanderthals? Thanks to amazing technology development in genome sequencing, researchers can now look at the genomes of extinct and long-dead specimens. So far, the oldest specimen to yield analyzable DNA is a 450,000-year-old Homo sapiens individual found in Spain. More and more long-dead Neanderthal and H. sapiens specimens have had their whole genomes sequenced, and so it is possible to look at many of the nuclear-encoded genes in the genome as they existed tens of thousands of years ago. And apparently, the question of whether our archaic relatives saw color like us is an interesting one to boot. The idea is that our modern living styles require enhanced color vision that might have evolved recently after our divergence from archaic humans. In addition, anatomical evidence and the ecological distribution of Neanderthals suggest that they liked dimmer light than modern humans do. John Taylor and Thomas Reimchen examined this question by looking at several Neanderthal genomes and some modern H. sapiens fossil genomes. In addition, a third genus Homo specimen found in the Denisova Cave in central Asia, called Denisovan, was examined. The authors found no resolvable differences between our current-day opsin genes and the long-dead opsin genes of Neanderthals, Denisovan, and long-dead H. sapiens. This result is amazing, given that the genomes tested are all more than thirty thousand years old.