The Eyes Have It

Animals have tremendous visual powers that people are only beginning to understand

10-01-1991 // Joyce Wolkomir and Richard Wolkomir

Retina, a toy poodle, clearly enjoyed her job. For one year, seven days a week, she commuted to her office with her master, Jay Neitz, a researcher then working at the University of California, Santa Barbara. "Mornings, she would race to the car, run from the car to the lab building, run to the elevator and race down to her room," says Neitz.

There, with two co-workers—greyhounds Neitz borrowed from a friend—Retina sat in front of three circular screens. Two of the circles were illuminated with light of one color, the third with light of a different hue. It was the dogs' task to pick the odd-colored screen by poking it with their noses. As a reward for choosing the right screen, they received cheese-and-beef flavored pellets. Their dogs' work skills, after a little on-the-job training, were excellent.

Retina—named for the part of the eye that receives the image—helped Neitz and two fellow researchers, Timothy Geist and Gerald H. Jacobs, prove that dogs do see some colors. Scientists previously had assumed that dogs were totally color blind. In fact, the California team discovered that the creatures see subtle shades of violet and blue as well as humans do. Greens, yellows, oranges and reds, however, are just one color to a dog.

Since helping to dispel the colorblindness myth, Retina has been unemployed. "When the experiment ended, she was very unhappy," says Neitz, who published the study's findings in late 1989. "She raced to the car morning after morning, eager to go to work." Retina may yet find a new job, however, because research on animal vision is in high gear. These days, scientists are studying the eyes and visual perceptions of all sorts of species.

To learn how animals see the world, researchers are fitting owls with goggles and dyeing lambs to fool their mothers, showing slides to pigeons and shining lights in crocodiles' eyes. Vision research is turning up ideas for optical computing and electronics as well as for correcting impaired human sight. But most important, the quest to understand animal vision may teach us more about how brains function and how humans see.

Animals have some impressive visual capabilities. Horseshoe crabs' eyes become more sensitive at night, enabling them to see on dark beaches, according to Syracuse University neuroscientist Robert B. Barlow, Jr., who has studied the crabs' visual system for more than 25 years. Certain mantis shrimp apparently see color vividly in their watery world; their eyes contain at least ten different kinds of color-detecting (cone) cells, compared to the paltry three types in human eyes. A chameleon's eyes, encased in lids that expose only the pupils, swivel independently. The lizard can look ahead with one eye and back over its shoulder with the other.

For exceptionally large eyes, look to birds, says ornithologist Jerry Waldvogel of Clemson University. While human eyes are only an inch across, an ostrich's eyes are almost 2 inches in diameter, nearly the size of tennis balls. Ostriches have the largest eyes of any terrestrial vertebrate. Even tiny songbirds' eyes are larger in proportion to their heads than ours are.

"Our eyes occupy 5 percent of our skull volume, while birds' eyes take up 50 percent of their skulls' volume," says Waldvogel. To him, these numbers suggest "that vision is even more important to birds than to us."

Eyeball placement, as well as size, varies radically among animals. Graham Martin, at Britain's University of Birmingham, recently measured the visual field of the mallard, a bird with eyes set far apart. He found that the duck can see completely around itself and over the top of its head. Without moving its head, it can simultaneously spot hawks diving from above and ducklings paddling astray.

Because the fields of view of its two eyes overlap only slightly, the mallard's zone of binocular vision (where it can judge depth) is narrow. Martin found that the duck's bill is barely within its zone of binocular vision. But rummaging at the pond's muddy bottom for food, the mallard needs little depth perception.

By contrast, hawks and owls, with eyes placed forward on their heads, have a smaller field of view but better depth perception, which they need to strike prey accurately. Binocular vision helps starlings, too, says Martin. They can pinpoint worms and other food as they stir soil with their bills.

Martin has also studied Humboldt penguins and discovered that they have a wide zone of depth perception, including the area around their beaks. He concluded that penguins must rely on vision to catch prey underwater. However, he wondered what swimming penguins see.

Our vision blurs when we submerge, because our cornea (the clear window covering the iris and the lens) focuses light poorly in water. We become extremely farsighted. But water's density prevents our eyes from seeing anything well even at a distance. Martin found that a penguin's cornea is unusually flat, which has the effect of prescription glasses, enabling penguins to see clearly when submerged.

Underwater, eyes also see color differently, because suspended particles and other substances in the ocean filter out most red light. When Martin tested penguins' color vision, he discovered that they do not see red. They do see violet, blue and green. Even though they spend much of their life on land, their eyes are adapted to the underwater world, where they hunt. They may even see into the ultraviolet region of the spectrum, where people are blind.

Above water, frogs, salamanders and lizards respond to a kind of light we cannot normally see, says neurobiologist Kraig Adler of Cornell University. He's demonstrated that these animals detect polarized light, light waves filtered by the Earth's atmosphere so they oscillate in only one dimension, like a snake slithering side-to-side. Such polarized light creates bright and dark patterns in the sky that lizards can see. Adler found that desert fringed-toed lizards correlate the polarization patterns overhead with the time of day to get their bearings, because the patterns shift as the sun moves.

Adler tested lizards in tanks by moving hawk-shaped models overhead. Even when a tank kept the lizards from seeing a single landmark on the ground, they scuttled across the sand directly to their burrows, guided by the polarization patterns they could see in the sky.

Lizards do not necessarily use their eyes to see polarized light. Adler has found that lizards—along with frogs and salamanders-detect polarized light using the pineal or parietal bodies, tiny structures in the brains of vertebrates. Although the pineal's function in humans is primarily secretory, in reptiles and amphibians it contains conelike elements that make it function like a third eye. In some species, the pineal body is attached to a patch of light-sensitive cells outside the skull. But the pineal body also can detect light that filters through bone, a good light-blocker but not a perfect one. Experiments have shown that sunlight penetrates even a thick sheep's skull, according to Adler.

How animals interpret what they see is as important as what they see. In birds, most of the brain is devoted to processing visual information, making them intriguing research subjects. By fitting baby barn owls with goggles that distorted their vision, Stanford University neurobiologists Eric and Phyllis Knudsen determined that owls trust their vision more than their hearing. When their ears tell them a mouse is in one spot and their eyes say it is in a different spot, owls ignore their ears. The birds pounce where they think they see the mouse, even if their eyes are wrong.

Britain's Graham Martin took in an injured owl more than 20 years ago, named him Wol after the owl in Winnie the Pooh and studied his vision. "He's made his contribution and now he's pensioned off—we keep him as a pet in the lab, where he supervises all that goes on," says Martin. Wol demonstrated that an owl's night vision is only two-and-a-half times more sensitive than ours. But owls fly well among obstacles like trees even in almost complete darkness because they memorize terrain. "They know their patch inside out," says Martin.

Homing pigeons also orient themselves visually, observing the position of the sun, says Charles Walcott, director of Cornell University's Laboratory of Ornithology, who follows pigeons in an airplane. But when fitted with smoky goggles so they can't see well, pigeons still find their way. They use, Walcott says, "a Chinese laundry list" of fall-back navigational cues, including odors and magnetic fields.

The way sheep interpret the world has also proved a rich topic for research. Sheep have surprising visual abilities. Keith Kendrick, a scientist at Britain's Agricultural and Food Research Council, has found that, like mallard ducks, sheep can see almost completely around themselves. Wild sheep of various breeds can spot a human or a coyote more than half a mile off, even when the interloper is partially hidden. Besides scanning for danger, sheep use their eyes to assess the size of each other's horns, a measure of dominance within the flock.

The way sheep process this information may sound familiar. By staining different parts of lambs with dye, researchers showed that ewes identify their lambs by their faces, just as people recognize each other. Kendrick says that an orphan lamb he raised, at just a few weeks old, knew him from other humans by sight. "They also identify grasses by the shapes of the blades—they like clover," he says.

Kendrick believes sheep are not born able to tell one grass from another—or even necessarily a human from a sheep. "I suspect most of it is learned rather than innate, but proving it is another matter," he says. Last year he had an experience that supported his theory. "I hand-raised a lamb after her mother died giving birth, and I found that given other sheep to look at or me, she'd always prefer me," he adds. "Now she's the dominant female in her flock, and the whole flock seems less bothered than usual by the sight of people."

Kendrick sees his ongoing work as more than a sheep fan's curiosity. "In disorders like schizophrenia and autism, people's ability to respond correctly to what they see breaks down," he says. He hopes that studies of sheep vision will lead to insights into human disorders. "It turns out that the principles of neural processing embodied in a sheep's brain are remarkably similar to those found in monkeys and probably in humans as well." It shows, he adds, "that the way the brain carries out the complex task of visual recognition is remarkably similar in different species."

Some species, however, have dissimilar talents in visual processing. Julie Neiworth, a researcher at Carleton College in Minnesota, once saw a laboratory pigeon land on her computer keyboard's space bar. The pigeon's weight sent the cursor marker skittering across the computer screen. Fascinated by the moving light, the pigeon tracked it across the screen, pecking at it, which prompted Neiworth to test a pigeon's ability to calculate the trajectory of a moving object.

"We can follow a moving object—like a baseball-with our eyes, and calculate where it will go as long as its speed remains constant," says Neiworth. "But if it accelerates or slows as it moves, we don't do so well."

Neiworth created a program that sends a light snaking across a computer screen in various configurations, its speed constantly changing. Then she taught pigeons that every time they pecked at the moving light and hit it, as scored by electronic sensors in the screen, they would receive their favorite food as a reward. "To hit the fast-moving light, they have to calculate its trajectory and then peck where it's going to be," says Neiworth. It is a game, she notes, at which the pigeons excel. And it indicates pigeons have perceptual skills that people do not.

Pigeons even do well in a vision scientist's version of art history. Donald Kendrick, a psychologist at Middle Tennessee State University, has been showing pigeons pen-and-ink drawings of birds and mammals from nineteenth-century scientific journals. If the pigeons can tell bird drawings from mammal drawings by pecking the appropriate slide, they earn a treat.

"We show them perhaps 35 pictures of birds and 35 pictures of mammals, and after 5 to 30 days of training, they 4o well," says Kendrick. He checks the pigeons by showing them previously unseen drawings, to make sure they are not simply memorizing the pictures. "They're definitely conceptualizing the qualities 'birdness' and `mammalness,'" he says.

Recently, Kendrick showed pigeons photographs of landscapes. "The pigeons have large windows looking out over the lab's backyard, and they get excited if they see a squirrel running around out there," he says. So the researcher made photographic slides of the yard from various angles, including some angles the pigeons had never seen. The birds distinguished slides of the lab's yard from slides of similar-looking fields. "It's not easy—students have trouble with it, and sometimes even I can't remember which is the right slide," says Kendrick.

But can pigeons match a photograph with the real object it represents? To find out, Kendrick photographed toy soldiers, little space ships, yo-yos, tiny trucks—"They all came from my son's toy box," he says. Then he taught the pigeons to peck a slide of a particular toy, such as a yo-yo, to earn a treat. Finally, he put the trained pigeon in a T-shaped maze. On one side of the T was an actual yo-yo. On the other side was a different toy.

"They were funny to watch," says Kendrick. "They'd come to the maze's crossbar, look right, look left, than run to the yo-yo." They clearly recognized the three-dimensional toy from the two-dimensional picture, an achievement we take for granted among humans but might not expect from pigeons.

Psychologist Robert Cook, now at Tufts University, also worked on the photograph tests. He created fantasy creatures by cutting apart drawings and pasting mammal heads on bird bodies, and vice-versa. He found that pigeons see a picture with a mule's head on a duck's body as a bird. To a pigeon, however, a duck-headed mule is a mammal. "It turned out they made their judgment on the overall shape of the body—if it was mostly mule, then it was a mule," says Cook.

A pigeon brain is small. "It's about the size of your thumb," Cook says. "Yet, its representation of the world is not much different than ours." He hopes that studies of pigeon vision, a natural marvel of miniaturization, could lead to artificial eyes for humans, powered by thumb-sized computers. His pigeons, like Retina the poodle, are apparently happy to help.

"They seem to enjoy the experiments," says Cook. "Pigeons have a good work ethic."

Writers Joyce and Richard Wolkomir, who see the world clearly, thanks to glasses, live in the Vermont countryside.

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