Dopamine. Serotonin. If you are a neuroscientist like me, these words conjure up images of chemicals, ideas like ‘pleasure’, ‘mood’, ‘reward prediction’, and ‘diarrhea’ (really, no one discusses THAT part of serotonin). Most people think of dopamine and serotonin as chemicals that influence mood, things subject to drugs like antidepressants and cocaine. But did you ever think of swimming? No?
Obviously, you are not a nematode.
Vidal-Gadea et al. “Caenorhabditis elegans selects distinct crawling and swimming gaits via dopamine and serotonin” PNAS, 2011.
(Make sure to click on the links, there are VIDEOS!)
In order to understand how dopamine and serotonin affect swimming and crawling in these worms, we need to first understand the idea of gait. Gait (when I think of gait I usually think of horses) is just the movement of an animal across a surface. They are usually characterized by how the feet (or belly, or what have you) falls as the animal moves, but they can be very physiologically different from each other. For example, humans can walk, or they can run. They cannot do something in between the two (a jog, though slow, is a slow RUN, not a walk). Similarly, a nematode has ‘gaits’. It can swim, OR it can crawl. The two movements are highly distinct, and it can’t do something that’s evenly in between.
With crawling, the nematode wriggles back and forth, in the same way you are used to seeing snakes like sidewinders crawl, in S shapes. When the worm hits water, though, it switches immediately, and starts arcing its body back and forth in C’s, which is swimming. The supplemental information has a great movie of this here (don’t worry, it’s free!).
Now the question that the authors of this study wanted to answer was whether the swimming and crawling of these nematodes was controlled via the same neural circuits, or a different ones. And are these two movements distinct GAITS?
To test this they watched the nematodes move on “land” (agar) and in water, observing both crawling and swimming. They then put them into a thick, gloppy liquid. If swimming and drawling were not different gaits, the thick liquid would cause kind of a swim/crawl (a swawl? a crim?). But the worms instead ALTERNATED between very slow crawling, and very slow swimming. (Check out the movie) It’s clearly two series of gaits, you can swim OR you can crawl, but you can’t do something in between.
So what stimulates this swimming to crawling and back again? It turns out it’s mechanical stimulation. There are two ways to make a ‘tode switch gaits (well, except for putting it into or taking out of water, obviously). You can press it between two glass plates until it’s in a tight spot. It will then start crawling. Or you can FEED THE WORM IRON and MAGNETIZE it to a surface. That kind of pressure will make it crawl instead of swim. And this is just SO cool to me. I mean, how many animal models can you MAGNETIZE?! I think I want one of these things as a pet.
In C. elegans, areas that are mechanosensitive (sensitive to mechanical stimulation like being pressed flat or magnetizing) are associated with the neurotransmitter dopamine. So the authors wanted to see how the dopamine impacted crawling. C. elegans only has 8 dopamine neurons, so it’s not too hard to selectively take them out. When they did, the nematodes could still swim, and still crawl, but they couldn’t TRANSITION from swimming to crawling. They had lost the ability to initiate the crawling gait. (And again, you really should watch the movies. A picture wouldn’t do it justice). But the ‘todes could still crawl if you poked at them. This means that dopamine was important for the gait transition, not for the movement itself.
They then took the nematodes, and instead of getting rid of dopamine neurons or magnetizing them, they used optogenetics to put light-activating genes into the nematode’s dopamine neurons. So now the dopamine neruons only come on when they SAY they do, when a certain kind of light is turned on. Without the light, the C. elegans acted like worms with no dopamine, unable to switch from swimming to crawling. But with the light turned on, the nematodes managed the swimming to crawling gait transition just dandy.
What you can see along the bottom here is the curvature of the nematode. Small deflections are crawling (that small curling S shape) while large deflections are the C shaped swimming. You can see that the ‘todes keep swimming until the light is turned on and the dopamine neurons are activated, which makes the nematode start crawling almost immediately.
So that’s swimming to crawling, what about crawling to SWIMMING? It’s the same two gaits, but a different gait change. And if dopamine makes a swimming nematode crawl, it turns out serotonin makes a crawling nematode swim.
The effects of serotonin are basically parallel to the effects of dopamine here. When C. elegans can’t synthesize serotonin (which you can do by knocking out the enzyme that makes the chemical) normal swimming was a little screwy, but more importantly, the animals couldn’t make the TRANSITION from crawling to swimming in the first place. And it turns out that serotonin perpetuates swimming, even when the water is gone.
So it looks like dopamine and serotonin control the changes in gaits, with serotonin controlling the crawl-to-swim, and the dopamine controlling the swim-to-crawl.
So what is this sort of thing important for? Well, first, it’s really COOL. I mean, look at those little swimming dudes (and you can control them with MAGNETS!!!). Not only that, this paper provides more evidence that dopamine and serotonin may be most important in switching behaviors on and off (at least in the nematodes). This is important for our understanding of motion and gait, and how gait can be disrupted. A good example of this is Parkinson’s disease, where disruptions in dopamine signalling result in shaking, and in freezing when someone attempts to initiate movement. That’s a GAIT disruption, and showing that ways in which it is conserved in nematodes could allow us to use nematodes as a model for aspects of the disorder. Not bad for a little nematode.
Vidal-Gadea, A., Topper, S., Young, L., Crisp, A., Kressin, L., Elbel, E., Maples, T., Brauner, M., Erbguth, K., Axelrod, A., Gottschalk, A., Siegel, D., & Pierce-Shimomura, J. (2011). Caenorhabditis elegans selects distinct crawling and swimming gaits via dopamine and serotonin Proceedings of the National Academy of Sciences, 108 (42), 17504-17509 DOI: 10.1073/pnas.1108673108
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