Pavlovian training: can pea plants learn?

Pavlov's dogs learn to salivate at the sound of a bell, if the bell was presented alongside their dinner enough times first. We now call this Pavlovian conditioning in his honour, and we know that lots of animals, us humans included, can learn like this. In recent years, plant scientist Monica Gagliano has been talking about what she dubs plant cognitive ecology. She's presented some surprising results that suggest that pea plants can be trained a bit like Pavlov's dogs. Chris Smith spoke with UC Davis scientist Kasey Markel, who decided he'd better investigate, and set up an experiment to replicate the results...

Kasey - Me and a fellow researcher were having one of those late night discussions about the nature of consciousness. And we decided that learning was maybe a necessary, but not sufficient condition for consciousness. And so we were wondering which organisms in the kingdom of life had the capacity for learning. And we saw a recently published study that showed learning was reported in plants. And it was very recent and as yet unreplicated, and therefore seemed ripe for replication and expansion efforts.

Chris - And in that particular study, what had they done? And what had they found?

Kasey - What they had done was to adapt the classic Pavlov's dogs experiment for pea plants. So in Pavlov's dogs, you can ring a bell always before the arrival of food. And eventually the dogs will start salivating as soon as they hear a bell. And in this experiment, what they had done was present blue light right before a fan, such that the plants would associate the blue light with the fan.

Chris - So in this instance by pairing the fan, which is one kind of stimulus, with light, something the plants are sensitive to and are always going to grow towards, the argument is that you can train the plants to recognise that there's a fan and it will either be where the light is or opposite to where the light is, depending upon how you've done the experiment and the plants will steer their growth accordingly.

Kasey - Precisely. When these experiments have been done in animals, we tend to forget things after we've been taught them. And so what I was interested in doing was discovering how long the plants could remember this training that had been done in the experiment. We know from the original experiment, they can remember for at least one day, but I suspected it might be longer than that.

Chris - So what did you do?

Kasey - The plan was to run the experiment and design it such that I could test them on successively further out days. So one day after the training, two days, three days, and see if we could get what's called a forgetting curve where there's learning, and then over time, the learning becomes progressively diminished.

Chris - Can you just describe your experiment? What it looked like, what you actually did?

Kasey - Yeah. So my experiment pretty directly followed the protocol of the original study. And these plants are in a capital Y shaped maze. And on the top of each arm, there's a blue light and a fan. And for a period of three days, blue light and the fan will be activated either on the same arm of the maze or on opposite arms of the maze to train the plants. And then on the fourth day for the testing phase, the blue lights are all disactivated and the fans are alone turned on and we try to use the fan to manipulate the direction of growth of the plant based on what it's been trained.

Chris - Therefore one would anticipate if the plants can learn, the fan tells the plant where the light is

Kasey - So that was our expectation. And the plan was to start with that and then test from further and further days out to see how long it took the plants to forget the information. But unfortunately we were unable to actually replicate that feat of training the plants based on the association with fan and light.

Chris- It just didn't work?

Kasey - Yeah. It just didn't work.

Chris - Do you think that's because you did something wrong, or do you think that actually the original observation was just by chance?

Kasey - There are a couple of possibilities there, obviously it's always possible that we did something wrong. I spent a lot of time reaching out to the original authors, but unfortunately they didn't get back to me to kind of help troubleshoot. There were a few things that weren't precisely clear in terms of exactly which equipment they had used or which source they had used for the supply of seeds, things like that. It's also possible, however, that the original study for one reason or another can't be replicated.

Chris - What did you do next then?

Kasey - Well, unfortunately at this point there wasn't all that much I could do. I reached out to a couple of fellow plant scientists and plant physiologists for kind of help with troubleshooting. I reached out more times to the original scientists, but kept replicating the experiments. At some point I'd replicated them kind of as much as I could and run out of time. And so I wrote up my results and started trying to publish them.

Chris - And that's the interesting thing here isn't it? Because you say started trying to publish them, what you were trying to publish was a negative result, not just a negative result - a negative result, refuting someone else's positive result. I don't suppose that was an easy path to take, was it?

Kasey - It's been a little bit difficult to publish. I originally reached out to the journal that had published the initial report and spent a long time, over a year actually, in the peer review process there, but ultimately it was rejected. And so I started sending it elsewhere and I'm happy to say it's been accepted at eLife

Chris - Out of interest, when you say it was rejected, did you get some reasoning for why they found your results less compelling than the original observation?

Kasey - Strangely that actually wasn't the claim. All four reviewers ended up agreeing that my experimental design was more rigorous than the original claim. However, because of the lack of the novelty in the results, two reviewers decided it was not worthy of publishing. And two reviewers were strongly in favour of publishing, ultimately that ended up with a rejection.

Chris - And what does that say to you about the practice and process and therefore the reliability more broadly of the results that we see in the scientific corpus?

Kasey - It certainly has been an education to me that it's much safer to trust results that have been replicated in at least a couple of different labs, rather than just looking at one off studies from a single laboratory.

Chris - Well, you know what they say, give peas a chance, although after all those efforts, perhaps Kasey Markel might disagree.