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Wednesday, December 6, 2023

How Octopuses Use Their Suction Cups to Taste Through Touch

Nicholas Bellono, a professor of molecular and cell biology at Harvard University, was worried about his first octopus. “It’s not trivial to have an octopus in the lab,” he says. They're wily creatures who require specific water conditions and diets, and have a penchant for carrying out elaborate escapes. But those worries were no match for Bellono’s curiosity. “We just thought, ‘This animal is pretty crazy, so we should just study that,’” he says.

The result of that curiosity is a paper published Thursday in Cell in which Bellono’s lab reveals yet another very cool thing about these invertebrates: a unique type of receptor in the tissue of their suction cups that can taste surfaces by touching them. “Octopuses’ arms are like big tongues that are probing around and making contact,” Bellono says. As they brush their arms across surfaces, molecules on those surfaces bind to receptors in the suckers, which send signals to a long axial nerve running the length of the octopus’s limb.

The new paper also shows that the signal doesn’t have to travel all the way to the animal’s brain to be decoded. Instead, it’s processed and acted on by nerves distributed in the arms, independent from the octopus’s central nervous system. The findings help explain more about how the cephalopods sense and explore their environments and about how their limbs act on stimuli independently.

“This is a really exciting finding,” says Charles Derby, a professor of neurobiology and biology at Georgia State University, who was not involved in the research. He says any time scientists find a new type of sensing cell, it's a big deal. “Animals are cool in that they are really plastic, in an evolutionary sense,” he says. This study helps add to the big picture of how animals have evolved and adapted to their surroundings over time.

Bellono specializes in researching how animals adapt their sensory systems to survive in particular environments. In just two short years, he’s brought around 30 species into his lab, including sharks, squid, jellyfish, photosynthetic sea slugs, and anemones. He likes to step into the animal room and marvel at each creature’s unique adaptations. And when it came to the octopus, Bellono was especially interested in its limbs. The creature would explore surfaces by running its arms over objects, and sometimes, when specific chemicals were present, an octopus would alter the type of touch it was using, quickly tapping the surface. Previous studies had characterized this “taste by touch” behavior, but there was no research about the stimuli, cells, receptors, or neural processing involved in the process. So Bellono set out to find what sensory mechanisms might explain this unique behavior, and what molecules might be interesting to the octopus.

Just defining what the sense of taste is and how it works for aquatic organisms can be counterintuitive for land dwellers. For those of us above the water line, taste happens when soluble molecules—chemicals dissolved in liquids or fats—come into contact with receptors on the tongue. Insoluble molecules, which aren’t dissolved and can be floating through the air, are sensed through the olfactory neurons in the nose. But in water the opposite is true. Soluble molecules float easily through aquatic environments, while insoluble molecules—the stuff that won’t dissolve—stick to surfaces and have to be physically touched in order to be sensed. So for the octopus, Bellono asks, “Is it just based on the molecule that’s detected? Is it based on the organ? Is it based on the distance?”

“In the case of the octopus, it really seems to be contact-dependent,” he concludes. To find these taste receptors, the researchers started by looking at cells in the places where the octopus makes most contact with objects: its suction cups. The Harvard team was able to identify mechanoreceptors, which respond to touch, but the team couldn’t find any chemoreceptors, which react to chemical signals.

So next, the team turned to the octopus genome. There were no sequences for chemoreceptors in the suckers, but previous researchers had identified what they described as “atypical acetylcholine receptors”—cells that would normally respond to signals from the nervous system but which, in this case, didn’t have the right binding sites for those signals. Bellono wondered if these might be the elusive taste receptors. The team cloned those sequences and expressed them in cells in the lab so they could study their structure, which molecules they respond to, and how they might send signals to the octopus’s nervous system.

They found that these chemoreceptors are built out of combinations of proteins, which create a binding site and an ion channel that sends an electrical charge back to the nervous system. Different combinations of proteins building the chemoreceptors mean that they are sensitive to different molecules. When the right molecule binds to this receptor, the complex sends an electrical signal to the nerve along the octopus’s arm.

The receptors Bellono tested are sensitive to several terpenoids, molecules produced by many marine invertebrates as a defense mechanism. Octopuses often hunt by stretching their arms into caves and crevices, searching for prey they can’t see. These chemicals could signal to the octopus that they’re encountering a dangerous animal and discourage the octopus from eating it by leaving a bad—or at least a warning—taste in it’s sucker.

The ability of these receptors to sense the terpenoids was also inhibited by octopus ink, something cephalopods release when they’re alarmed or as an escape mechanism. This could indicate that octopuses’ peripheral nervous systems are able to prioritize signals about danger over signals for food, telling them to stop looking for a snack and start being more alert to a potential problem in their environment.

In an email to WIRED, Tessa Montague, a postdoctoral fellow at Columbia University who studies cephalopod neurology and who was not involved in this study, writes that this paper provides some of the deepest insights available into the taste and touch mechanisms that an octopus uses to interact with its environments. “This study provides evidence that octopuses have evolved sensitive and sophisticated mechanisms to detect chemical cues with their suckers, and these local signals may permit the animal to react appropriately to the environment without the need to transmit signals to the central brain,” she writes.

After identifying and studying these cells on their own, the Harvard researchers went back to studying the octopuses in their lab—they now have eight—to see how these chemo-tactile receptors affect their behavior. The team divided a tank in half, leaving one side clean and treating surfaces on the other side with different terpenoid molecules. On the clean side, an octopus would fan its arms out, sweeping through the water and exploring it. But when the octopus’s suckers sensed the terpenoids on the treated side, it would stop searching and tap the surfaces quickly, retracting its arms and avoiding the area with the molecule.

Bellono speculates that this behavior indicates an evolutionary advantage that allows the octopus to safely explore the nooks and crannies of its environment for food while avoiding prey that might be dangerous. “Chemo-tactile behavior facilitates ‘blind feeding’ involving searching for food in seafloor crevices,” he writes in the study. That sensation, he thinks, “might serve to abort search behavior in response to repulsive signals.”

But Bellono still has plenty of questions he hasn’t been able to answer. His team has only found and sequenced a fraction of the octopus’s chemoreceptors, so he doesn’t know how many there are, how many different combinations of proteins could combine to create different levels of sensitivity, or how many molecules the receptors might be sensitive to. Because the proteins can reassemble to make new receptors, it’s possible that octopus taste sensitivities vary by species, by habitat niche, or even over the course of the mollusk’s lifetime. “If an animal is hungry, does it change the expression of certain proteins to detect prey, versus other things?” Bellono wonders.

He also doesn’t know what the sensation of taste by touch is like to the octopus. Are there some molecules that attract it and others that are displeasing? What is delicious to an octopus?

So Bellono will have octopuses in the lab a little longer. The team has tried to help the cephalopods feel more at home, building little dens out of coffee cups where they can hide. And, after a few escape attempts, the researchers took a few precautionary steps too, placing bricks on top of the tanks and wrapping the outside of the aquariums with velcro, a texture octopuses dislike. Bellono says the animals seem pretty content these days, though he admits he’s probably anthropomorphized them a bit. But the lab members have to stay vigilant. You never know when an octopus might want to get a little taste of freedom.

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