Tadpoles ‘see’ with eyes on their tails in Tufts experiment

It sounds, at first, like a plot twist from a zany movie about a mad scientist: What if an eye were transplanted onto a tadpole’s tail? Would the frog-in-the-making be merely a laboratory freak -- a kind of Mr. Potato Head of science? Or would the tadpole actually be able to see out of its backside?

Now, a pair of serious Tufts University biologists have carefully done the experiment, demonstrating for the first time that a blind tadpole can see with an eye bulging from its tail. Researchers showed the eye can detect changes in colored light and guide the tadpole’s behavior, even though the nerves from its eye connect only to the spinal cord. Remarkably, that means signals sent from the displaced eye through the central nervous system were correctly interpreted by the brain.

The research, led by a Tufts biologist who is known for approaching big questions in biology from unexpected angles, probes an important and very real question confronting scientists in fields that range from regenerative medicine to robotics: if you create a new sensor -- whether it’s a replacement eye or a new camera -- how do you integrate that with an organism’s (or robot’s) abilities?

“What we’re fundamentally interested in is how the brain-body interface works when the body architecture is changed,” said Michael Levin, the Tufts biologist who led the work, published Wednesday in the Journal of Experimental Biology.

In other words, learning how organisms can integrate signals from a displaced eye into at least a rudimentary form of sight could provide an informative example for scientists -- whether they are programming software that will guide how a robot uses its body or designing prosthetic sensory organs.

To do the study, researchers transplanted a developing eye from one tadpole embryo on to the backside of another tadpole embryo. They did this 230 times, and in almost all cases, the eyes grew to about the same size and shape along the tadpoles’ tails. All of them faced outward, like normal eyes. Nerve cells sprouted from the eyes in about half of the tadpoles. In some, these nerves tapped in to the spinal cord. The scientists removed the tadpoles’ regular eyes, leaving them blind.

They then exposed these tadpoles, as well as normal ones, to red or blue light, giving them a shock when they were in areas of red light. Normal tadpoles learned to avoid the red light. Blind tadpoles did not learn to avoid the shocks, presumably because they could not detect the different light colors. But a fifth of the tadpoles who were blinded, but had been given an eye on their tail that connected to the spinal cord, were able to avoid the shocks.

“I really like this approach, and not just because it’s different or exotic,” said Günther K.H. Zupanc, a biology professor at Northeastern University who was not involved in the research.

Understanding how the auxiliary eye becomes a source of vision in a frog could help guide scientists who want to build prosthetics that are more than just a glass eye.

“It’s very easy to build sensors which are sensitive to light, sensitive to different colors, which have high resolution,” Zupanc said. “What would be very important is this device can communicate with the right brain structures [to create vision]; otherwise, it’s just a cosmetic thing.”

Josh Bongard, associate professor of computer science at the University of Vermont, said that although he works in a different field, building robots, the paper is exciting. Engineers would love to have robots that can carry on or adapt if they lose an arm or sensory capability. On the flipside, if a new sensor were added, it would be ideal if the robot could learn about how to use it, without needing new software.

“This kind of work, coming from biology, changes the way we think about machines in general,” Bongard said.

The new work is part of a larger project in Levin’s laboratory, which examines how electrical signaling could be involved in processes such as limb regeneration, or tumor growth. But the question everyone in his lab bet on as the study progressed was a bit more lighthearted. What would happen to the eye when the tadpole turned into a frog? Would it die and drop off with the rest of the tail, or would it somehow be preserved in the metamorphosis?

The answer can be seen in Levin’s lab: “Do we have frogs with eyes on their butts in the lab?” Levin said. “We most certainly do.”