Octopuses Experience the Emotional Aspects of Pain

New findings support a complex picture of pain in invertebrates. Image credit: suhentu/123RF Stock Photo.

Published August 12, 2021

Editor’s note: This story first appeared on the IASP Pain Research Forum and has been lightly edited for RELIEF.

The simple reflex of withdrawing from a painful stimulus is familiar to all of us – it’s what happens when you quickly remove your hand after touching a really hot stove, for example. Most other animals probably don’t get into trouble with stoves (save a reckless household cat, perhaps), but practically all of them do show similar reflex responses to things that might cause them pain.

That includes invertebrates (animals lacking a backbone). But there has been much debate about whether they experience what are referred to as the affective components of pain – the negative emotions, unpleasantness and suffering that often accompany pain.

Now, new research in octopuses – yes, octopuses – may have settled the question of whether these particular invertebrates can experience affective pain.

Performing experiments that allow for the study of affective pain, Robyn Crook, San Francisco State University, US, demonstrates that octopuses avoid a place that had previously been associated with a noxious stimulus (defined as a stimulus that can actually or potentially cause damage to tissue and may eventually result in pain – think of that hot stove again).

The octopuses also preferred a location that had been associated with relief from pain (analgesia). Crook also shows that these creatures groom, guard, and conceal an experimental injury, behaviors that reflect what is known as discriminative pain.

Finally, Crook also uses a technique known as electrophysiology, which assesses the electrical activity of nerve cells, to show that the behavior the octopuses show is accompanied by changes in the central nervous system.

“The data are so clear – there’s just no way to argue with any of this,” said Jeffrey Mogil, a pain researcher at McGill University, Montreal, Canada, who was not involved with the study.

“The other thing that’s nice about the paper,” Mogil continued, “is that there was a very focused question [Do octopuses experience affective pain?], and she’s given a very focused answer, and she’s done it in three different ways,” Mogil said, referring to the affective pain, discriminative pain, and electrophysiology experiments.

In addition to advancing the understanding of the pain system, the study has ethical implications too – maybe we humans should treat invertebrates differently, for instance.

The study was published online February 22, 2021, in the journal iScience.

Octopuses have affective pain experience…
Previous research from Crook and colleagues showed that the nociceptors of invertebrates, in this case squids, become more electrically excitable after bodily injury (nociceptors are a specialized kind of nerve cell that detects potentially harmful stimuli capable of causing pain). Crook had also shown that this is a way for squid to avoid predation by a natural fish predator, providing an evolutionary explanation for this phenomenon.

That invertebrates experience at least some aspects of pain is not a new idea. But there have been few studies on the pain experience on mollusks like octopuses.

Crook began her study by creating a new three-chambered box that would allow her to do conditioned place preference, and conditioned place avoidance experiments. These experiments allow researchers to test whether animals learn to prefer a particular location, or to avoid a particular location, respectively. This would allow Crook to test the affective component of pain in octopuses.

In the first session of this experiment, each octopus could freely explore all chambers for fifteen minutes, with Crook noting the chamber the octopus preferred the most.

In the second session, the octopus received an injection of acetic acid, a chemical that can cause pain, while other octopuses received saline, a safe and harmless substance. Then, the octopuses were confined to the chamber they initially preferred for twenty minutes. In the third and final session, the octopuses could once again freely explore all chambers.

After the three sessions, Crook found that the octopuses that received acetic acid displayed a clear avoidance of their initially preferred chamber. The octopuses that received saline, however, did not exhibit any changes in their preferred chambers.

“Showing these more subtle cognitive assays, where you ask the animal to make a decision based on how they feel, is a better way of capturing what really matters to us as problematic pain, which is the suffering component,” said Crook.

Crook also looked at the behavior of octopuses that had received both acetic acid and the pain reliever lidocaine right before being confined to their least preferred chamber. Those animals strongly preferred that chamber, whereas octopuses given saline showed no such preference. This demonstrated that the pain relief that lidocaine provided was rewarding only to octopuses experiencing pain and was not inherently rewarding on its own.

…and discriminative pain experience too.
Crook also looked at other behaviors to learn if octopuses could experience what are called the discriminative aspects of pain – the location, quality, and intensity of pain.

Octopuses that had received acetic acid groomed and concealed the area of painful injection for the entire 20-minute trial period, behaviors that stopped after the animals received lidocaine. The grooming by these octopuses resulted in the removal of a small area of skin covering the injection site. This behavior was never seen in the saline-injected octopuses or after lidocaine injection.

“What we saw that was interesting is that the wound attention behavior was really different from what we saw in other types of studies that we’ve done. I suspect that what it’s doing is trying to release the noxious stuff that is in the skin,” explained Crook. “We know that in the wild, as they move about in the reef, octopuses are stung by anemones, for example. So, this is presumably a behavior that has evolved to deal with envenomation,” referring to the injection of venom by venomous animals.

In mammals, noxious sensory information is processed in the brain, which is required for affective and discriminative pain experience. To see whether this held true for the octopuses, Crook recorded the electrical activity of the brachial connectives. These structures connect the nerve cords of the octopus arm to the brain.

These experiments would show that the effects of acetic acid, and of lidocaine, were reflected in the electrical activity that Crook measured. This showed that noxious information is indeed processed in the brain of the animals.

“She’s got the beautiful electrophysiology backing up the behavior,” said Mogil.

Together, the findings support the claim that octopuses have a complex pain experience involving both affective and discriminative components. Crook is now moving toward demonstrating that other invertebrates also experience affective components of pain by studying squid and cuttlefish.

Time for a rethink?
The study’s finding of a complex pain experience in octopuses means it’s time for a more careful consideration of how people treat invertebrates.

“It has implications for regulations on angling, which is a big thing in the world, and for practices such as throwing live lobsters into boiling pots,” said Mogil. “And so, at some point, there are ethical issues that need to be addressed as well.”

Crook agrees. “I think there are a lot of interesting questions that come up when you show an animal like an octopus that diverged from our lineage at least 500 million years ago has managed to evolve much of the same capacity” for pain experience, she said.

“From the perspective of animal welfare and ethics,” she continued, “those are really interesting questions that force us to think about the way we treat animals, but also from the broader perspective of evolutionary biology, there’s this big question that guides my research, which is how many different ways there are to make a complex brain,” Crook said.

“And it’s not just a really basic task, like a reflex, that we share. It is a deeply complex task of the emotional aspects of pain that suggests there’s strong evolutionary pressure driving the selection of affective state,” said Crook.

IASP Pain Research Forum Correspondent Sarah D’Angelo recently graduated with a BS in biology from Rutgers University, Camden, New Jersey, US.