Researchers at the University of Kiel, and at the University of Copenhagen have demonstrated that Caribbean box jellyfish (Tripedalia cystophora) can learn at a much more complex level than previously thought—despite only having only one thousand nerve cells and no centralized brain. The team, headed by Anders Garm, PhD, an associate professor at the University of Copenhagen’s department of biology, and Jan Bielecki, PhD, at Kiel University, trained the jellyfish to learn to spot and dodge obstacles, demonstrating that, just like humans, mice and flies, these animals can learn from past experiences.
While the results challenge this previous notion that advanced learning requires a centralized brain, they also shed light on the evolutionary roots of learning and memory. And a better understanding of memory could ultimately help scientists better understand disorders, such as dementia, in which memory is affected.
“It was once presumed that jellyfish can only manage the simplest forms of learning, including habituation—i.e., the ability to get used to a certain stimulation, such as a constant sound or constant touch,” Garm noted. “Now, we see that jellyfish have a much more refined ability to learn, and that they can actually learn from their mistakes. And in doing so, modify their behavior … I don’t claim that we are finding the cure for dementia, but if we can gain a better understanding of what memory is, which is a central problem in dementia, we may be able to lay a building block to better understand the disease and perhaps counteract it.”
The investigators reported on their findings in Current Biology, in a paper titled “Associative learning in the box jellyfish Tripedalia cystophora,” in which they concluded that their findings suggest an “… intriguing possibility that advanced neuronal processes, like operant conditioning, are a fundamental property of all nervous systems.”
Jellyfish have been around on earth for more than 500 million years, demonstrating considerable evolutionary success. Jellyfish and their relatives, collectively known as cnidarians, are considered to be the earliest living animals to develop nervous systems, and to have fairly simple nervous systems and no centralized brain. And with prevailing opinion being that more advanced nervous systems equate to more advanced learning potential in animals, it has generally been assumed that these simple creatures have very little learning capacity. “Learning in general spans a wide range of complexities from simple sensitization and habituation to highly advanced learning such as insight and reasoning,” the authors noted. “Memory formation and learning in animals reside within the nervous system, with the general notion that more advanced nervous systems accomplish more advanced types of learning.”
Anders Garm has been researching box jellyfish for more than a decade. These animals are commonly known for being among the world’s most poisonous creatures. The Caribbean box jellyfish, which is no bigger than a fingernail, has a somewhat milder venom, and a complex visual system, with 24 eyes embedded in a bell-like body. Some of these eyes are image forming, providing box jellyfish with more complex vision than other types of jellyfish. “Like other cnidarians, T. cystophora does not possess a single centralized brain but has instead a concentration of neurons in the four eye-bearing sensory structures (rhopalia), which serve as individual visual processing and integration centers,” the team explained. In the adult jellyfish, these rhopalial nervous systems (RNSs) comprise just about one thousand processing neurons each.
Living in mangrove swamps, the Caribbean box jellyfish uses its vision to steer through murky waters and swerve around underwater tree roots—displaying obstacle avoidance behavior; OAB—to snare prey. To find their way through murky mangroves, four of the T cystophora‘s eyes look up through the surface of the water and navigate using the mangrove canopies. In fact, the authors stated, within the cnidarians, box jellyfish are “extraordinary in behavioral complexity.”
One of the most advanced attributes of a nervous system is the ability to change behavior as a result of experience—to remember and learn. Bielecki, Garm and colleagues set out to test this ability in box jellyfish. The team dressed a round tank with gray and white stripes to simulate the jellyfish’s natural habitat, with the gray stripes mimicking mangrove roots that would appear distant.
They observed the jellyfish in the tank for 7.5 minutes. Initially, the creatures swam close to these seemingly far stripes and bumped into them frequently. But by the end of the experiment, the animals increased the average distance to the wall by about 50% during the 7.5 minute trial, quadrupled the number of successful pivots to avoid collision. “Most importantly, within the 7.5 min trial period the animals had significantly adjusted their contrast:distance response … to less than half the number of contacts with the perimeter wall,” the team stated.
The results demonstrated that the jellies could acquire the ability to avoid obstacles through associative learning, a process through which organisms form mental connections between sensory stimulations and behaviors, in this case learning from experience through visual and mechanical stimuli.
The jellyfish learning effectively takes place through failed evasions. That is, they learn from misinterpreting contrast and bumping into roots. Here they combined the visual impression and mechanical shock they got whenever they bumped into a root—and in doing so, learned when to veer away. “Our behavioral experiments demonstrate that three to five failed evasive maneuvers are enough to change the jellyfish’s behavior so that they no longer hit the roots. It is interesting that this is roughly the same repetition rate that a fruit fly or mouse needs to learn,” said Garm. “We can see that as each new day of hunting begins, box jellyfish learn from the current contrasts by combining visual impressions and sensations during evasive maneuvers that fail. So, despite having a mere one thousand nerve cells—our brains have roughly 100 billion—they can connect temporal convergences of various impressions and learn a connection—or what we call associative learning. And they actually learn about as quickly as advanced animals like fruit flies and mice.”
The researchers explained further in their paper, “With the current work, we present evidence of operant conditioning in cnidarians, a type of associative learning that has previously only been clearly demonstrated in bilaterian animals, e.g., vertebrates, arthropods, and mollusks .” And operant conditioning, they noted, is defined as learning the effects of one’s own actions to avoid something aversive or obtain something of value. “In the present work, T. cystophora learned to associate low-contrast objects with increased risk of collision.”
The researchers sought to identify the underlying process of jellyfish’s associative learning by isolating the animal’s rhopalia visual centers. Each of these structures houses six eyes and generates pacemaker signals that govern the jellyfish’s pulsing motion, which spikes in frequency when the animal swerves from obstacles.
The team showed the stationary rhopalium moving gray bars to mimic the animal’s approach to objects. The structure did not respond to light gray bars, interpreting them as distant. However, after the researchers trained the rhopalium with weak electric stimulation when the bars approach, it started generating obstacle-dodging signals in response to the light gray bars. These electric stimulations mimicked the mechanical stimuli of a collision. The findings further showed that combining visual and mechanical stimuli is required for associative learning in jellyfish and that the rhopalium serves as a learning center. “Our experiments show that contrast, i.e., how dark the root is in relation to the water, is used by the jellyfish to assess distances to roots, which allows them to swim away at just the right moment,” Garm noted. “Even more interesting is that the relationship between distance and contrast changes on a daily basis due to rainwater, algae and wave action.”
The new research results break with previous scientific perceptions of what animals with simple nervous systems are capable of. “… the behavioral assays and the neurophysiological experiments confirm operant conditioning in the box jellyfish T. cystophora, which, in contrast to habituation and sensitization, is considered associative learning,” the scientists further noted. “Such operant conditioning has previously been considered to require advanced nervous systems including a conventional centralized brain. This notion is now challenged, since the box jellyfish has a dispersed nervous system and lacks a centralized brain.”
Next, the team plans to dive deeper into the cellular interactions of jellyfish nervous systems to tease apart memory formation. They also plan to further understand how the mechanical sensor in the bell works to paint a complete picture of the animal’s associative learning. Garm continued, “If you want to understand complex structures, it’s always good to start as simple as you can. Looking at these relatively simple nervous systems in jellyfish, we have a much higher chance of understanding all the details and how it comes together to perform behaviors. For fundamental neuroscience, this is pretty big news. It provides a new perspective on what can be done with a simple nervous system. This suggests that advanced learning may have been one of the most important evolutionary benefits of the nervous system from the very beginning.”
Garm added, “It’s surprising how fast these animals learn; it’s about the same pace as advanced animals are doing. Even the simplest nervous system seems to be able to do advanced learning, and this might turn out to be an extremely fundamental cellular mechanism invented at the dawn of the evolution nervous system.” Added Bielecki, “Learning is the pinnacle performance for nervous systems. To successfully teach jellyfish a new trick, he said “it’s best to leverage its natural behaviors, something that makes sense to the animal, so it reaches its full potential.” As the authors stated, “Great care was taken to ensure that the experimental sensory input and the evaluation of behavioral output conformed to the capabilities of the experimental animal.”
Having shown where learning is happening in these box jellyfish has given the team unique insights into how to now study the precise changes that occur in a nerve cell when it is involved in advanced learning. “We hope that this can become a supermodel system for looking at cellular processes in the advanced learning of all sorts of animals,” Garm stated. “We are now in the process of trying to pinpoint exactly which cells are involved in learning and memory formation. Upon doing so, we will be able to go in and look at what structural and physiological changes occur in the cells as learning takes place.”
If the scientists are able to pinpoint the exact mechanisms in jellyfish involved in learning, the next step will be to find out whether it applies specifically to jellies or if it can be found in all animals. “Eventually, we will look for the same mechanisms in other animals, to see if this is how memory works in general,” Garm suggested. And their box jellyfish test system could prove more widely informative, the team concluded. “Furthermore, since we demonstrate the full learning capacity of isolated rhopalia, we placed the plasticity of the neuronal processing within the RNS. The simplicity of the RNS, combined with inducible circuit plasticity, makes it an attractive model for studying systems-level learning and memory formation.”
This kind of groundbreaking knowledge could be used for a wealth of purposes, according to “Understanding something as enigmatic and immensely complex as the brain is in itself an absolutely amazing thing,” Garm pointed out. “But there are unimaginably many useful possibilities. One major problem in the future will undoubtedly be various forms of dementia. I don’t claim that we are finding the cure for dementia, but if we can gain a better understanding of what memory is, which is a central problem in dementia, we may be able to lay a building block to better understand the disease and perhaps counteract it.”
