If your fingers could taste, smell and touch: chemotactile sensation in the octopus

Like most folks living alone during quarantine, I’ve picked up quite a few new hobbies. My favorite of these hobbies, by far, has been learning to play the ukulele. I’ve never played an instrument before, but the thing I’ve found most challenging is getting one of my hands to move through chords while making the other hand strum to a specific beat. There have been many times after missing that E chord for the 10th time, I’ve wished my hands could act independently of my brain and perfectly perform their separate duties. Honestly, how wonderful would this ability be for our lives in general? Imagine if one of our hands could cook dinner while the other did our math homework. Think of how much time we could save! While my musical musings might seem a little outlandish, in reality this is not a totally alien possibility. There is life on our planet that can do this. One animal specifically: the octopus.

Left: An image of an octopus used in this study

Right: A zoomed in view of a single octopus sucker

More than half of the 500 million neurons that make up the octopus central nervous system are located in their arms, far away from the central brain. Each arm has its own cluster of neurons called a “ganglia”. These separate “mini-brains” allow each arm to act completely autonomously from each other and from their central brain. In fact, some studies have shown that if you separate an octopus arm from its body it can still perform a number of complex behaviors. Octopus arms are even more unique thanks to their ability to smell and taste as well as touch. Imagine being able to taste the mouse or phone screen you’re using right now! Each octopus arm has a number of highly mobile suckers and they use these suckers to taste, smell and touch the environment around them. Each of these suckers has its own separate ganglia which means that even the individual suckers can act totally on their own. The ability of these suckers to interact with their environment using multiple senses piqued the curiosity of a group of researchers at Harvard led by Dr. Lena van Giesen.

We humans sense our environment through a group of very specialized receptor cells. Receptor cells take in sensory stimuli like sound or smell and then send signals about them to our brains. We then use these signals to inform how we behave. These receptor cells exist in places like our skin, ears, and tongues. It turns out that octopuses have very similar cells in their suckers.

Going into the experiment, the researchers expected to find receptors for smelling or tasting similar to ones that have been observed in critters across the animal kingdom. However, they were surprisingly unable to find anything resembling the receptor types that have been well studied in other animals. However, they did find a large number of a type of receptor that had similar genetic markers to receptors found in human brains that process chemicals called neurotransmitters. But these receptors looked nothing like anything anyone had seen before. The authors postulated that these receptors might be different because they were more suited to the unique needs of octopuses and other members of its animal family, known as cephalopods. They called these cells chemotactile receptors or CRs.

Dr. van Giesen and colleagues theorized that CRs were used in contact-dependent chemosensation. In other words, they hoped that these were the receptors necessary for that special ability of the suckers to taste/smell the things they touch. In order to test this theory the researchers analyzed the responses of a few types of CRs to different chemicals they might find in the environment of an octopus. They found the CRs to become more active in the presence of a fish extract and less active when tested with octopus ink. This result made sense based on known octopus preferences: octopuses love to eat fish and only project ink as a warning or fear response. The researchers then tried a number of different compounds, some found in an octopus’ natural environment and some not. Overall, they found that different subtypes of receptors reacted in a unique way to each chemical.

Often these CRs were found in the suckers as pairs or groups of one or many subtypes. The researchers found that when activated together, some CRs changed how they would react to chemicals in comparison to when they were on their own. This is amazing because it suggests that the number of chemicals these suckers can detect is quite large and not limited to the number of CRs. This is like if you were eating a sour candy but could only taste the sourness or the sweetness and not both. Think how boring that would be. But when you can taste both, the candy’s taste is so much more complex and exciting. Our plethora of taste senses (sweet, sour, salty, umami, etc.) makes eating food constantly new and exciting. This seems to be the same for octopuses; their diverse set of CRs makes them able to process many different and fascinating signals from their environment.

Finally, once the authors of this paper had a list of different chemicals and how the CRs responded to each, they wanted to see what role these CRs played in overall octopus behavior. The researchers measured octopus behavior by counting the number of times they touched things and how long they kept their arm on the object being touched. In response to polygodial, a defensive chemical that is emitted by marine invertebrates (the octopus' favorite snacks), the octopus increased the number of times it touched but decreased the duration of touch in comparison to normal sea water. The researchers then tried other chemicals they knew activated the CRs but were not defensive signals to test if different types of stimuli changed behavior. Again, the octopus increased the number of touches and decreased duration of touch but also showed less avoidance-like behavior. This suggested that the chemicals that activate CRs increase the octopus' desire to explore things through touch while sending different signals to the brain about how to behave depending on the type of smell/taste.

Overall, this exciting research beautifully indicates the way octopus biology is primed for incredibly precise autonomous use of their individual arms. Thanks to specialized tools, like their individual suckers and the special chemotactile receptors in them, octopuses are able to interact with their aquatic environment in a way we humans can only dream of. Perhaps one day we will have brains in our arms. It would certainly make learning a new instrument much easier!

Edited by Manasi Iyer

References

van Giesen L, Kilian PB, Allard CAH, Bellono NW. Molecular Basis of Chemotactile Sensation in Octopus. Cell. 2020 Oct 29;183(3):594-604.e14. doi: 10.1016/j.cell.2020.09.008. PMID: 33125889; PMCID: PMC7605239.