Decapitated worms regenerate heads with old memories

Yup, you read that right.

The worm in question is the Planarian flatworm. Compared to C. elegans, the flatworm doesn’t get as much love in neuroscience. But to regenerative medicine, it is a truly incredible gem.

You see, planaria harbors adult stem cells that imbue them with astonishing regenerative abilities. If you decapitate a worm, the tailpiece can regenerate a COMPLETE head with a fully functioning brain within a few days. What makes this even more incredible is that – unlike C. elegans that have a distributed nervous system* - planaria has a centralized brain in the head region, just like you and me. Planarian neurons also talk to each other in ways similar to ours, with the same majority of neurotransmitters. They can also learn simple associations and keep the memory. Oh, and they look like this:

Science is only starting the tease out the mechanism behind planarian’s regenerative abilities. But to me, an even more tantalizing question is this: what happens to all the memories stored in the chopped-off old brain after a new one takes its place? Does planaria revert to a state of tabula rasa, or does it carry with it memories of its merry old life?

Shomrat T and Levin M. 2013. An Automated Training Paradigm Reveals Long-term Memory in Planaria and Its Persistence Through Head Regeneration. J Exp Biol. Doi: 10.1242/jeb.087809

This is the question this paper set out to answer. Planarians have this feeding quirk: when fed in a new environment, they tend to be more “cautious”, taking longer to go after the yummy liver morsels that they love. Once they’ve been fed many times in the same environment, they “feel safe” and go right after the food.

Scientists trained a group of planarians to associate feeding with a rough-floored Petri dish (pictured on top)– significantly different from the smooth-floored one they’re kept in. 4 days after the final training session, scientists put both trained and untrained worms into the rough-floored dish, with one extra twist: the food was now illuminated by light shining through the dish. Planarians hate light; in order to get the food they’d have to be VERY comfortable with the environment.

As you can see from the red line below, 4 days after the last familiarization session, trained (right side) planarians took much less time to grab the food compared to their untrained (left side) peers. This was also observed 14 days after training (black line), meaning that the memory of the familiar rough-floored dish lasted at least that long.

Results! Fig 3 from the paper.

Results! Fig 3 from the paper.

Scientists then decapitated the worms (both trained and untrained), and waited patiently while the worms regrew their heads. Roughly a week later, scientists pre-fed the worms to satiety in their home dish, and 4 days later tested them for memory of the rough-floored Petri dish. As you can see from the green line above, the trained-and-beheaded worms seemed to have lost the memory of the feeding environment, taking just as much time to go after the food as the untrained-and-beheaded worms.

Is the memory completely lost? Worms trained to associate food with an environment can re-learn the same association much faster than naïve-untrained worms. (You can brush up on a rusty skill much faster than learn it from scratch.) To see if a hint of the old memory remained, scientists pre-fed both trained and untrained decapitated worms in the rough-floored Petri dish. To the familiarized worm, this is a previously encountered environment; for the unfamiliarized, this is a first introduction to the dish. Previously it took these worms 10 days of training to form a food-environment memory, so this one-time training session shouldn’t result in significant learning.

Scientists tested the worms for memory of the rough-floored dish 4 days later. As you can see from the blue line in the figure above, the trained worms (right) quickly re-familiarized with the feeding environment, taking much less time than the untrained ones (left) to feed. This suggests that maybe the memory is not all gone – it’s just not easily accessible without reactivation.

Here's a summary. After decapitation and head regrowth: Pre-feeding in home dish = no difference between trained and untrained. Pre-feeding in rough-floored (training) dish = previously trained worms remember better.

What to make of all this? Can old memories be re-grown along with the head? My first reaction was maybe the decapitated worms had some sort of modification going on in the peripheral nervous system, which resulted in their sensitization to food-environment learning. By comparing the blue and green lines, you can see that both untrained (left) and trained (right) worms learned and remembered the feeding dish after one-time training. However, peripheral modifications doesn’t explain why previously trained worms learned and remembered the feeding environment BETTER.

The authors also designed their experiment very cleverly. In the test dish, the worms had to recognize food and the feeding environment, and make a decision to move towards it against their natural preference (stay away from light). This cautious approach strongly argues that the brain is involved, ie it’s not a simple reflex.

Memory is stored in neuronal communications in the brain. Could it be that a rough correlate is also stored in stem cells of the planaria? This way, when stem cells divide to form a new brain, the memory would return. Although this scenario sounds like sci-fi, it actually could occur through epigenetic mechanisms (changing the pattern of gene expression). There’s just not a lot of evidence for it yet.

While still skeptical, I have to admit the idea that memory can survive decapitation and brain regrowth is tantalizing. Although us humans don’t have planarian’s outstanding regenerative abilities, we do share similar neural transmission mechanisms. What does this study tell us about our own memories?

*Edited for accuracy: many thanks to all the people who pointed out that C elegans do not have "many little 'brains'" as I first put it. Very bad wording on my part. C elegans have a ring of ganglia (clusters of neurons) but not a centralized brain. For more please refer to the link in the comments.

Shomrat T, & Levin M (2013). An automated training paradigm reveals long-term memory in planaria and its persistence through head regeneration. The Journal of experimental biology PMID: 23821717