Other Minds: The Octopus, the Sea, and the Deep Origins of Consciousness

by Peter Godfrey-Smith

Cuttlefish are relatives of octopuses, but more closely related to squid. Those three—octopuses, cuttlefish, squid—are all members of a group called the cephalopods. The other well-known cephalopods are nautiluses, deep-sea Pacific shellfish which live quite differently from octopuses and their cousins. Octopuses, cuttlefish, and squid have something else in common: their large and complex nervous systems.

To understand these meetings between people and cephalopods, we have to go back to an event of the opposite kind: a departure, a moving apart. The departure happened quite some time before the meetings—about 600 million years before. Like the meetings, it involved animals in the ocean.

One of the most important developments in animal psychology over the last few decades has been the realization of how smart crows and parrots are.

Cephalopods are an island of mental complexity in the sea of invertebrate animals. Because our most recent common ancestor was so simple and lies so far back, cephalopods are an independent experiment in the evolution of large brains and complex behavior. If we can make contact with cephalopods as sentient beings, it is not because of a shared history, not because of kinship, but because evolution built minds twice over. This is probably the closest we will come to meeting an intelligent alien.

As part of all this, at some unknown stage, came the evolution of subjective experience. For some animals, there’s something it feels like to be such an animal. There is a self, of some kind, that experiences what goes on.

An octopus’s eye is similar to ours. It is formed like a camera, with an adjustable lens that focuses an image on a retina. The eyes are similar but the brains behind them are different on almost every scale. If we want to understand other minds, the minds of cephalopods are the most other of all.

Single-celled organisms can sense and react. Much of what they do counts as behavior only in a very broad sense, but they can control how they move and what chemicals they make, in response to what they detect going on around them. In order for any organism to do this, one part of it must be receptive, able to see or smell or hear, and another part must be active, able to make something useful happen. The organism must also establish a connection of some sort, an arc, between these two parts.

Biologists who work on these organisms are more and more inclined to see the senses of bacteria as attuned to the presence and activities of other cells around them, not just to washes of edible and inedible chemicals. The receptors on the surfaces of bacterial cells are sensitive to many things, and these include chemicals that bacteria themselves tend to excrete for various reasons—sometimes just as overflow of metabolic processes. This may not sound like much, but it opens an important door. Once the same chemicals are being sensed and produced, there is the possibility of coordination between cells. We have reached the birth of social behavior.

Bacteria living inside a Hawaiian squid produce light by a chemical reaction, but only if enough other bacteria are around to join in. The bacteria control their illumination by detecting the local concentration of an “inducer” molecule, which is made by the bacteria and gives each individual a sense of how many potential light producers are around. As well as lighting up, the bacteria follow the rule that the more of this chemical you sense, the more you make. When enough light is being produced, the squid who house the bacteria gain the benefit of camouflage. This is because they hunt at night, when moonlight would normally cast their body’s shadow down to predators below. Their internal lights cancel the shadow. Meanwhile, the bacteria seem to benefit from the hospitable living quarters provided by the squid.

The chemistry of life is an aquatic chemistry. We can get by on land only by carrying a huge amount of salt water around with us. And many of the evolutionary moves made at these early stages—those giving birth to sensing, behavior, and coordination—would have depended on the sea’s free movement of chemicals.

The transition to a multicellular form of life occurred many times, leading once to animals, once to plants, on other occasions to fungi, various seaweeds, and less conspicuous organisms. Most likely, the origin of animals did not stem from a meeting between lone cells who drifted together. Rather, animals arose from a cell whose daughters did not separate properly during cell division. Usually, when a single-celled organism divides into two, the daughters go their separate ways, but not always. Imagine a ball of cells that forms when one cell divides and the results stay together—and the process repeats several times. The cells in the clump probably ate bacteria as they hovered together in the sea.

A neuron will release a tiny spray of chemicals into the gap or “cleft” between it and another neuron. These chemicals, when they are detected at the other side, can help trigger (or in some cases suppress) an action potential in that adjoining cell. This chemical influence is the residue of ancient signaling between organisms, pressed inward. The action potential, too, existed in cells before animals evolved, and exists today outside them.

According to the first view, the original and fundamental function of the nervous system is to link perception with action. Brains are for the guidance of action, and the only way to “guide” action in a useful way is to link what is done to what is seen (and touched, and tasted). The senses track what’s going on in the environment, and nervous systems use this information to work out what to do.

Some biologists have argued that the Ediacarans are members of an animal-like evolutionary experiment, but not properly animals themselves. Rather than sitting on the animal branch of the tree of life, they exhibit a different way that cells can come together to yield an organism.

Before pressing on into the world of bilaterian evolution, let’s pause and ask: which animal produces the most sophisticated behavior, which is the smartest, without a bilaterian body plan? Questions like this are notoriously hard to answer in an unbiased way, but in this case, the answer is clear. The most behaviorally sophisticated animals outside the bilaterians are the—terrifying—box jellyfish, the Cubozoa.

Some cubozoans have truly brutal venom in their stingers, strong enough to have killed large numbers of humans. In northeastern Australia, the presence of box jellyfish clears the beaches completely each summer; for a good part of the year it’s too dangerous to swim off the shore at all, except in netted enclosures. To compound the problem, these jellyfish are invisible in the water. They also have the most complex behaviors of any non-bilaterian. Around the top of their body are two dozen sophisticated eyes—eyes with lenses and retinas, like ours.

During the Cambrian the relations between one animal and another became a more important factor in the lives of each. Behavior became directed on other animals—watching, seizing, and evading. From early in the Cambrian we see fossils that display the machinery of these interactions: eyes, claws, antennae. These animals also have obvious marks of mobility: legs and fins.

In the Ediacaran, other animals might be there around you, without being especially relevant. In the Cambrian, each animal becomes an important part of the environment of others. This entanglement of one life in another, and its evolutionary consequences, is due to behavior and the mechanisms controlling it. From this point on, the mind evolved in response to other minds.

The Cambrian witnessed the appearance of both the compound eyes seen today in insects and camera eyes like our own. Imagine the behavioral and evolutionary consequences of being able to see the objects around you for the first time, especially objects at some distance and in motion. The biologist Andrew Parker has argued that the invention of eyes was the decisive event in the Cambrian.

Octopuses and other cephalopods are mollusks—they belong to a large group of animals which also includes clams, oysters, and snails. Part of the story of the octopus, then, is the evolutionary history of mollusks.

Shells were the mollusks’ response to what looks like an abrupt change in the lives of animals: the invention of predation.

The real survivor is indeed a cephalopod, but nautilus rather than octopus. Still living in the Pacific, present-day nautiluses are little changed from 200 million years ago. Living in coiled shells, they’re now scavengers. They have simple eyes and a cluster of tentacles, and they move up and down, from the deep sea to shallower water, in a rhythm that’s still being studied. They seem to stay higher in the water at night, deeper in the day.

In the cuttlefish, a shell was retained internally, and still helps the animal remain buoyant. In squid, a sword-shaped internal structure called a “pen” remains. Octopuses have lost their shell entirely.

When we try to compare one animal’s brainpower with another’s, we also run into the fact that there is no single scale on which intelligence can be sensibly measured. Different animals are good at different things, as makes sense given the different lives they live.

Octopuses and other cephalopods have exceptionally good eyes, and these are eyes built on the same general design as ours. Two experiments in the evolution of large nervous systems landed on similar ways of seeing.

What I find most intriguing is the octopus’s ability to adapt to new and unusual circumstances—confinement in a lab—and turn the apparatus around them to their own octopodean purposes.

Peter Dews was a Harvard scientist who worked mostly on the interaction between drugs and behavior. He had a general interest in learning, though, and his octopus experiment did not involve drugs at all. Dews was influenced by his Harvard colleague B. F. Skinner, whose work on “operant conditioning”—the learning of behaviors by reward and punishment—had revolutionized psychology. The idea that successful behaviors will be repeated and unsuccessful ones abandoned had been pioneered by Edward Thorndike around 1900, but Skinner developed the idea in great detail. Dews, with many others, was inspired by the way Skinner was able to make animal experiments rigorous and exact.

However, one message of octopus experiments is that there is a great deal of individual variability.

The most famous octopus anecdotes are tales of escape and thievery, in which octopuses in aquariums raid neighboring tanks at night for food. Those stories, despite their charm, are not especially indicative of high intelligence. Neighboring tanks are not so different from tide pools, even though the entrance and exit take more effort. Here is a behavior I find more intriguing. Octopuses in at least two aquariums have learned to turn off the lights by squirting jets of water at the bulbs when no one is watching, and short-circuiting the power supply. At the University of Otago in New Zealand, this became so expensive that the octopus had to be released back to the wild. A lab in Germany had the same problem.

For example, it has long appeared that captive octopuses can recognize and behave differently toward individual human keepers. Stories of this kind have been coming out of different labs for years. Initially it all seemed anecdotal. In the same lab in New Zealand that had the “lights-out” problem, an octopus took a dislike to one member of the lab staff, for no obvious reason, and whenever that person passed by on the walkway behind the tank she received a jet of half a gallon of water in the back of her neck. Shelley Adamo, of Dalhousie University, had one cuttlefish who reliably squirted streams of water at all new visitors to the lab, and not at people who were often around. In 2010, an experiment confirmed that giant Pacific octopuses can indeed recognize individual humans, and can do this even when the humans are wearing identical uniforms.

Octopuses love to eat crabs, but in the lab they are often fed on thawed-out frozen shrimp or squid. It takes octopuses a while to get used to these second-rate foods, but eventually they do. One day Boal was walking down a row of tanks, feeding each octopus a piece of thawed squid as she passed. On reaching the end of the row, she walked back the way she’d come. The octopus in the first tank, though, seemed to be waiting for her. It had not eaten its squid, but instead was holding it conspicuously. As Boal stood there, the octopus made its way slowly across the tank toward the outflow pipe, watching her all the way. When it reached the outflow pipe, still watching her, it dumped the scrap of squid down the drain.

Other octopus manipulations of foreign objects are done for more practical reasons. In 2009, a group of researchers in Indonesia were surprised to see octopuses in the wild carrying around pairs of half coconut shells to use as portable shelters. The shells, neatly halved, must have been cut by humans and discarded. The octopuses put them to good use.

A wide range of animals use found objects for shelters (hermit crabs are an example), and some use tools for collecting food (including chimps and some crows). But to assemble and disassemble a “compound” object like this, and put it to use, is very rare. It’s not clear what to compare this behavior to, in fact. Many animals combine a variety of materials when making nests—a lot of nests are “compound” objects. But those are not disassembled, carried around, and put back together. The coconut-house behavior illustrates what I see as the distinctive feature of octopus intelligence; it makes clear the way they have become smart animals. They are smart in the sense of being curious and flexible; they are adventurous, opportunistic.

In arthropods, very complex behaviors tend to be achieved through the coordination of many individuals. Some squid are social, but with nothing like the organization of ants and honeybees. Cephalopods, with the partial exception of squid, acquired a non-social form of intelligence. The octopus, most of all, would follow a path of lone idiosyncratic complexity.

On our lineage, the chordate design emerges, with a cord of nerves down the middle of the animal’s back and a brain at one end. This design is seen in fish, reptiles, birds, and mammals. On the other side, the cephalopods’ side, a different body plan evolved, and a different kind of nervous system. These nervous systems are more distributed, less centralized, than ours. Invertebrates’ neurons are often collected into many ganglia, little knots that are spread through the body and connected to each other. The ganglia can be arranged in pairs, linked by connectors that run along the body and across it, like lines of latitude and longitude. This is sometimes called a “ladder-like” nervous system, and it does look like a ladder embedded within the body.

Perhaps most oddly, the esophagus, the tube that carries food from the mouth into the body, passes through the middle of the central brain. This seems all wrong; surely there was never supposed to be a brain there. If an octopus eats something sharp which pierces the side of its “throat,” the sharp object goes straight into its brain. Octopuses have been discovered with exactly this problem.

In an octopus, the majority of neurons are in the arms themselves—nearly twice as many as in the central brain. The arms have their own sensors and controllers. They have not only the sense of touch, but also the capacity to sense chemicals—to smell, or taste. Each sucker on an octopus’s arm may have 10,000 neurons to handle taste and touch.

The central idea is that rather than mediating between sensory input and behavioral output, the first nervous systems came to exist as solutions to a problem of pure coordination within the organism—the problem of how to coordinate the micro-acts of parts of the body into the macro-acts of the whole. The cephalopod body, and especially the octopus body, is a unique object with respect to these demands. When part of the molluscan “foot” differentiated into a mass of tentacles, with no joints or shell, the result was a very unwieldy organ to control. The result was also an enormously useful thing, if it could be controlled. The octopus’s loss of almost all hard parts compounded both the challenge and the opportunities. A vast range of movements became possible, but they had to be organized, had to be made coherent. Octopuses have not dealt with this challenge by imposing centralized governance on the body; rather, they have fashioned a mixture of local and central control. One might say the octopus has turned each arm into an intermediate-scale actor. But it also imposes order, top-down, on the huge and complex system that is the octopus body.

A large nervous system evolves to deal with coordination of the body, but the result is so much neural complexity that eventually other capacities arise as byproducts, or relatively easy additions to what the demands of action-shaping have built. I said “or” just above—byproducts or additions—but this is definitely an “and/or.” Some capacities—such as recognition of individual people—might be by-products, while others—such as problem solving—are the results of the evolutionary modification of the brain in response to the octopus’s opportunistic lifestyle.

There is, it seems, a kind of mental surplus in the octopus.

There are also more subtle psychological similarities. Octopuses, like us, seem to have a distinction between short-term and long-term memory. They engage in play with novel objects that aren’t food and have no apparent use. They seem to have something like sleep. Cuttlefish appear to have a form of rapid eye movement (REM) sleep, like the sleep in which we dream. (It’s still unclear whether there’s REM-like sleep in octopuses.)

Some features show a mixture of similarity and difference, convergence and divergence. We have hearts, and so do octopuses. But an octopus has three hearts, not one. Their hearts pump blood that is blue-green, using copper as the oxygen-carrying molecule instead of the iron which makes our blood red. Then, of course, there is the nervous system—large like ours, but built on a different design, with a different set of relationships between body and brain. The octopus is sometimes said to be a good illustration of the importance of a theoretical movement in psychology known as embodied cognition. These ideas were not developed to apply to octopuses, but to animals in general, including ourselves, and this view has also been influenced by robotics. One central idea is that our body itself, rather than our brain, is responsible for some of the “smartness” with which we handle the world. Our body’s own structure encodes some information about the environment and how we must deal with it, so not all this information needs to be stored in the brain.

Octopuses have a different embodiment, which has consequences for their different kind of psychology.

When advocates of embodied cognition such as Chiel and Beer give examples of how bodies provide resources for intelligent action, they mention the distances between parts of a body (which aid perception) and the locations and angles of joints. The octopus body has none of those things—no fixed distances between parts, no joints, no natural angles. Further, the relevant contrast in the octopus case is not “body rather than brain”—the contrast usually emphasized in discussions of embodied cognition. In an octopus, the nervous system as a whole is a more relevant object than the brain: it’s not clear where the brain itself begins and ends, and the nervous system runs all through the body. The octopus is suffused with nervousness; the body is not a separate thing that is controlled by the brain or nervous system.

The elaborate forms of experience found in us derived from simpler forms in other organisms. Consciousness surely did not, James said, suddenly irrupt into the universe fully formed. The history of life is a history of intermediates, shadings-off, and gray areas. Much about the mind lends itself to a treatment in those terms. Perception, action, memory—all those things creep into existence from precursors and partial cases. Suppose someone asks: Do bacteria really perceive their environment? Do bees really remember what has happened? These are not questions that have good yes-or-no answers. There’s a smooth transition from minimal kinds of sensitivity to the world to more elaborate kinds, and no reason to think in terms of sharp divides.

Sentience comes before consciousness.

Loops that link actions back to the senses are not only seen in us. They are present also in very simple forms of life. But they become more marked in animals, especially because animals can do more.

Often these loops lead to a problem, as an animal attempts to work out what’s going on around it. Some fish, for example, send out electric pulses for communication with other fish, and also electrically sense other things going on around them. The self-produced pulses will affect their own senses, though, and it may be difficult for a fish to distinguish the pulses it has made from electrical disturbances that are due to external things. To deal with this problem, whenever a fish emits a pulse it also sends a copy of the command around to the sensing system, enabling that system to counteract the effect of the pulse it has produced. The fish is tracking and registering the distinction between “self” and “other,” between the effects on its senses of its own actions and the effects of events going on around it.

An earthworm withdraws when something touches it—the touch might be a threat. But every time the worm crawls forward, it causes part of its body to be touched in just the same way. If it withdrew at every touch, it could never move at all. The worm succeeds in moving forward by canceling the effects of those self-produced touches.

This interaction between perception and action is also seen in what psychologists call perceptual constancies.