The plastic fantastic brain: Why losing one sense rewires others

Study finds worms that can’t feel are better smellers — and the phenomenon is reversible
Dr. Ithai Rabinowitch
Neurobiologist Dr. Ithai Rabinowitch led a new study showing that simple laboratory animals, when deprived of the sense of gentle touch, develop an enhanced sense of smell. Photo by Robert Hood / Fred Hutch News Service

There’s a quirky phenomenon where people who lose one sense can gain near-super abilities in another, especially if that sense is lost early in life. Blind people may hear better; the deaf can have a type of enhanced vision. These “super senses” are not just learned behavior — the brain actually remodels itself, giving more real estate to other senses when one is missing.

Now, a new study has found this sensory juggling also occurs in very simple animals and that the phenomenon is reversible. Unravelling how different senses interact in an animal easily studied in the laboratory can help us better understand sensation in humans — and what happens when someone loses a sense.

The study, published earlier this month in the journal PLOS Biology, showed that when these animals — microscopic roundworms otherwise known as Caenorhabditis elegans — are deprived of the sense of gentle touch, they become super-smellers, able to hunt out sources of food with a much fainter scent than their feeling peers.

Study author and Fred Hutchinson Cancer Research Center neurobiologist Dr. Ithai Rabinowitch, a postdoctoral fellow in Dr. Jihong Bai’s laboratory group, engineered worms with touch neurons that could be switched on and off with a pulse of blue light. This technique (known as optogenetics) allowed them to ask what happens when the animals regain feeling. Rabinowitch and his colleagues found that when the touch neurons were turned back on, the worms’ super-smell disappeared in just a few hours.

These findings are important for a few reasons, said Rabinowitch, who led the study along with Dr. Millet Treinin of the Hebrew University of Jerusalem and Dr. William Schafer of the Medical Research Council Laboratory of Molecular Biology, in Cambridge, England. For one, it means the brain’s ability to reshape itself in compensation for a missing sense is older, in evolutionary terms, than researchers had previously appreciated. Scientists have studied the phenomenon in monkeys, cats and other mammals, but this is the first example in an animal so distantly related to humans.

“C. elegans is a very simple creature compared to mammals, but still it has this very complex form of plasticity and change,” Rabinowitch said.

The human (and worm) nervous system’s exquisite malleability means that things aren’t set in stone, brain-wise, especially for the young. In a characteristic known as neuroplasticity, areas of the brain ordinarily devoted to perceiving sight can switch to understanding sound, and vice versa. If you think of the brain like a complex electrical system, it’s not so much that our bodies switch the red and blue wires when needed, it’s that they can turn red wires blue.

Some blind people, like Daniel Kish, have even learned to use their boosted hearing to seamlessly navigate the world through a series of rapid clicking noises, similar to how bats use sonar to find their way in the dark. Researchers have found that for Kish and other blind people who use this technique, the section of the brain that normally responds to visual cues lights up in brain scans in response to those clicks.

Human brains house about 86 billion neurons, so perhaps it’s not too surprising that they have some backup systems for parts that fail. But an adult C. elegans has only 300 neurons, and they do too.

That means that by understanding how the roundworm swaps signals of touch and smell, scientists may be able to better understand the basic principles of how humans boost certain senses, said Bai, also a study author. Their finding means that even in complex animals like humans, these interactions between different senses in the brain might be built off a simpler version that arose long ago in evolutionary time, he said. And now, they can study that simple version in the simple roundworm.

The microscopic roundworm known as Caenorhabditis elegans. Image courtesy of Dr. Ithai Rabinowitch

‘Why don’t we all hear better?’

Rabinowitch frames his interest in this neural flip-flopping with a simple question: “When blind people, for instance, hear better, you can ask yourself, why don’t [the sighted] hear better in the first place? Why do we have to be blind in order to hear better?” he said. “It’s hard to understand without looking into the details.”

Studies in humans and other mammals can spot the different areas of the brain that switch on or off when senses are lost or boosted, but they often can’t go into more depth than that. Studying simpler animals like C. elegans allow researchers to pinpoint the exact cells — and even the molecules — involved.

To study how well the worms smell, Rabinowitch placed tiny amounts of different chemicals that smell like yummy worm treats near the animals and watched their behavior. (To Rabinowitch, they smell like rotten fruit, marzipan or butter.) Worms with super-smell start moving toward the chemical even when only tiny amounts of it are present; normal worms need more scent to respond.

Of the different scents, Rabinowitch said the marzipan odor is his favorite — and the worms love it too.

“I like to hang out with the worms and smell the marzipan,” he said.

Rabinowitch and his colleagues found that the neurons that respond to touch actively keep smell neurons in check in worms with normal senses. When those touch neurons become inactive, the smell neurons ramp up, uninhibited. So it could be that none of our senses are working to their full potential.

The team also pinpointed the molecular messenger that conveys signals from touch cells to smell cells, telling the latter to tone down. This type of molecule, known as a neuropeptide, could play a role in humans too, Rabinowitch said.

This type of cross-sensory mediation may be advantageous, the researchers speculated.

“It does make sense that there is a kind of preference for diversity of information than volume of information,” Rabinowitch said, but he emphasized that the brain’s predilection for many different, quieter signals over one strong input is as yet hypothetical.

Evolution may have selected for a sensory system with some space to flex, Bai said.

“You don’t want to always work at your extreme. The system will break that way,” he said. “You build stability by allowing room for change. When you lose one sense and the others compensate, that’s the stability built in.”

However, even in the simple worm, sensory plasticity is still a complex picture. The researchers also found that the worms lacking the sense of gentle touch have reduced abilities in some other senses, like feeling touch on their nose, a sense controlled by a different set of neurons than overall gentle touch. The scientists don’t yet understand why some senses are dampened while others are boosted.

The nitty gritty

There are parallels between microscopic worms that can’t feel their surroundings and blind humans, the researchers said. C. elegans worms do not have eyes, relying primarily on body touch to get around. They don’t need sight in their natural environment, living in dark, gritty soil or rotting fruit where they wouldn’t be able to see far anyway, Bai said.

“Humans are vision-dominant, but the worm is touch-dominant. That’s their eye,” he said. “They just have an eye all over their body.”

These findings make new predictions about how human senses could work, Rabinowitch said. Nobody’s yet looked at whether neurons for one sense affect other sensory circuits in people or other mammals. But based on their study, Rabinowitch thinks it could be happening.

In their worm study, the researchers found just a single touch neuron and single smell neuron involved in the sensory interaction. The smell cell that gets downregulated by the touch neuron is one of the first in the scent-sensing pathway. So it’s possible that, for example, vision neurons in sighted humans inhibit some of the very first neurons in the complex highway of nerves that conveys sound information from ear to brain.

“Even if it’s not the very first line of sensation … somewhere that’s very primary in the whole chain of processing could be a good place to look,” Rabinowitch said.

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Rachel Tompa is a former staff writer at Fred Hutchinson Cancer Center. She has a Ph.D. in molecular biology from the University of California, San Francisco and a certificate in science writing from the University of California, Santa Cruz. Follow her on Twitter @Rachel_Tompa.

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