We’re all familiar with Pavlov’s conditioning experiments with dogs. Dogs were treated to an unconditioned stimulus — something to which they would normally respond with a specific behavior, in this case, meat juice which would cause them to drool. Then they were simultaneously exposed to the unconditioned stimulus and a new stimulus, the conditioned stimulus, that they would learn to associate with the tasty, drool-worthy stimulus — a bell. Afterwards, ringing a bell alone would cause the dogs to make the drooling response. The ability to make such an association is a measure of the learning ability of the animal.
Now…how do we carry out such an experiment on a cephalopod? And can it be done on a cephalopod with a reputation (perhaps undeserved, as we shall see) as a more primitive, less intelligent member of the clade?
The nautilus, Nautilus pompilius despite being a beautiful animal in its own right, is generally regarded as the simplest of the cephalopods, with a small brain lacking the more specialized areas associated with learning and memory. It’s a relatively slow moving beast, drifting up and down through the water column to forage for food. It has primitive eyes, which to visual animals like ourselves seems to be a mark of less sophisticated sensory processing, but it has an elaborate array of tentacles and rhinophores which it uses to probe for food by touch and smell/taste. Compared to big-eyed, swift squid, a nautilus just seems a little sluggish and slow.
So let’s look and see how good a nautilus’s memory might be. First, we need a response to stimuli that we can recognize and measure, equivalent to the drooling of Pavlov’s dogs. While they don’t measurably salivate, the nautilus does have a reaction to the hint of something tasty in the water — it will extend its tentacles and rhinophores, as seen below, in a quantifiable metric called the tentacle extension response, or TER.
The nautilus will extend those tentacles when treated to an unconditioned stimulus: a spritz of fish juice. Now we just need an unconditioned stimulus. A bell won’t do, but those simple eyes can respond to light, so investigators use a blue light, one similar in wavelength to the glow of luminescent bacteria.
Now we have a nice clean experiment: strap a nautilus to a bit of pipe in a tank. Shine a blue light at it, then give it a squirt of fish juice, which prompts it to splay out those tentacles. Do that ten times at an interval of a few minutes, and then let them rest for a period of time. Then the test: shine the blue light on the animal, without the fish juice, and see if it extends its tentacles.
The answer is yes, it does. The nautilus learns fairly quickly to associate a light pulse with the prospect of an imminent food stimulus, as measured in two different ways, the tentacle extension response and the ventilation rate (the animal breathes faster if it thinks it’s going to get a whiff of fish.)
Those graphs illustrate another interesting phenomenon; what’s being varied is the period between the training with the combination of the conditioned and unconditioned stimulus, and the presentation of a series of blue lights, the conditioned stimulus, without the reward. The response is biphasic. They remember the association well in a window of time of less than an hour after training, and then they seem to forget … and then they respond strongly again 6-12 hours after the training. This looks like a two-step memory, with short term and long term components; there is rapid assimilation of an association, and a different process that leads to long term consolidation of the lesson.
These results are comparable to similar results obtained in the cuttlefish, except that long term memory in the nautilus is relatively shorter. That’s impressive, since the nautilus lacks the brain structures (the vertical lobe complex) that are considered important for learning and memory in other cephalopods. That suggests that this is a mechanism that may have evolved independently in the nautilus, or that the brain structures in more visual cephalopods are refinements and elaborations of a primitive ability.
I’m also impressed with their ability relative to certain vertebrates. I’ve supervised several student projects that have tried to assess learning and memory in zebrafish, and they are much more difficult. We have the complication that these fish lack a simply assessed unconditioned response; they have to be trained, for instance, to swim to a particular area in a tank to show their interest in a stimulus, and their behavior is complicated by schooling and other confounding social behaviors — it usually takes a few weeks of training to get a measurable response to something like a light stimulus. I’m a bit envious of an animal and a protocol that can show a response to a conditioned stimulus within minutes after a relatively short training period; fish are such flaky flibbertigibbets when it comes to this sort of thing.
Crook R, Basil J (2008) A biphasic memory curve in the chambered nautilus, Nautilus pompilius L. (Cephalopoda: Nautiloidea). J Exp Biol 211:1992-1998.