A team of scientists has shown how the environment shapes learning and memory by training locusts like Pavlov's dog to associate different smells with reward or punishment.
Desert locusts are notorious for their devastating swarms. However, they do not always live in swarms -- they switch between a lone living 'solitary phase' and a swarming 'gregarious' phase. The two phases differ profoundly in looks, behaviour and in their life style.
The new research from the Universities of Leicester, Sussex and Cambridge examines how locusts associate odours with nutritious or toxic food. The research, published in the journal Current Biology, was supported by the Portuguese Foundation for Science and Technology (FCT), Champalimaud Foundation, The Royal Society, the Biotechnology and Biological Sciences Research Council (BBSRC) and the Leverhulme Trust.
Solitary locusts rely on camouflage to evade predators, and they avoid eating toxic plants; but gregarious locusts eat these plants to 'impregnate' themselves with toxins to deter predators. The transformation to gregarious behaviour, which happens when solitary locusts are forced together into a crowd, is complete within a few hours.
Dr Swidbert Ott from the University of Leicester said: "Locusts should consider toxic food 'bad' while they live alone but 'good' when they are in a swarm, which made us wonder, how do swarming locusts learn that 'bad is the new good'?"
Such research is important because it provides new insights into how animals can quickly switch between very different life styles that are adapted to different environments.
"Our research shows how animals that undergo a profound transformation in their life style also adapt their learning and memory capabilities to cope with the new environment in which they find themselves," says Dr Jeremy Niven from the University of Sussex.
Dr Patrício Simões, who carried out the experiments as part of his doctoral study at the University of Cambridge and the Champalimaud Neuroscience Programme, explains: "When we presented solitary locusts with an unfamiliar odour together with toxic food, they assigned it an aversive ('bad') value. But if the locust is in a crowd and starting to change towards gregarious, it assigns an appetitive ('good') value to the same odour. Ecologically, this makes sense because, being a gregarious locust, it should find and eat toxic plants to defend itself against predators.
"Then we asked, if a solitary locust has already learned about an odour and then it finds itself in a crowd, what would happen to its memories? Can it switch the value that it has assigned to the odour, or more precisely, does crowding change the value of a previous memory from aversive to appetitive? We found that locusts cannot do this: they are stuck with the value of their already acquired memories. However, strikingly we found that locusts in this transitional period also cannot form any new aversive memories, while they can still form new appetitive memories.
"We then simulated the context in which the switch to swarming behaviour takes place in the field. We show that this simple, selective block of aversion learning enables the locusts to effectively re-train themselves to learn that the same odour that indicated 'bad' now indicates 'good'."
As Dr. Ott explains: "Desert locusts aggregate into swarms when they run out of food -- the crowding is driven by hunger and competition for the last few plants in the desert. They are pretty desperate when they transform into the gregarious phase, so they will give the toxic plants another try. And because they can no longer form aversive memories, any food is now rewarding and they form the new 'correct' appetitive memory with the odour. This is how they re-train themselves to eat the toxic plants. It would be great to be able to do this experiment in the field but it would be quite tricky."
Dr Niven adds: "Because newly crowded locusts don't form memories about toxins they ingest, all they remember is the pleasant side of what they ate, and they ignore the toxin. In this way, a smell previously associated with a toxin can become associated with a pleasant experience.
"The changes in learning and memory we're proposing don't require the locusts to understand what's happening to them -- they just have to feed and form associations."
The study recalls the work of Russian physiologist Ivan Pavlov who famously studied dogs salivating in anticipation of food. Pavlov rang a bell every time he presented the dog with food. After a few 'training sessions' ringing the bell alone was sufficient to make the dog salivate, as it had come to associate the sound of the bell with getting food.
The scientists trained the locusts just like Pavlov trained his dog, except that the unfamiliar smell replaces the bell in Pavlov's experiments: they gently blew vanilla or lemon odour at the restrained locust, while they spoon-fed it with artificial food.
After training, the researchers 'asked' the locust: do you prefer vanilla odour or lemon odour. "We walk the locust on a rod that bifurcates into two arms: one arm has lemon odour, the other vanilla. So the locust has to make up its mind: do I go to vanilla or to lemon. Without training, locusts like vanilla more than lemon. But if you pair nutritious food with lemon during the training, they will go to lemon. And if you train solitary locusts with toxic food and vanilla, they will also go to lemon."
The new results show how brains do not solve problems 'in a vacuum' but in interaction with the environment.
"Simply crowding a locust won't change its mind about the odour being 'bad'," the authors say: "We first thought, this is pretty daft, the locust should now like the odour. But even we humans struggle to forget food poisoning although we know the next meal is fine. The locusts do not operate in a vacuum, they live in the desert. And in the circumstances that they need to re-evaluate the 'meaning' of an odour, it takes only a simple modification of the rules by which they learn: turn off learning 'bad' but keep learning 'good', and the locust can retrain itself.
"So a little brain with simple rules goes a long way if you let it interact with the environment."
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