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

by Peter Godfrey-Smith

Perceptual constancies are seen in a fairly wide range of animals, including octopuses and some spiders, as well as vertebrates. This ability has probably evolved independently in several different groups. Another path in the evolution of experience leads to integration. As streams of information come in from different senses, they are brought together into a single picture.

It’s one way of being wired up, and some animals do not integrate their experience nearly as much as we do. For example, in many animals the eyes are on each side of the head, not the front. The eyes then have separate visual fields, either largely or entirely, and each connects just to one side of the brain. In such an animal it is easy for scientists to control what each side is exposed to, by masking one eye. Then we can ask a question that might seem to have an obvious answer: If we show something to only one side of the brain, does the other side get the information too? We are not looking at damaged or altered animals here, so the two sides of the brain have all their natural connections. One would think that the information should get across. Why should evolution set things up so that only half the animal knows what has been seen? But when this question was studied in pigeons, it turned out that the information was not being passed across. The pigeons were trained to do a simple task with one eye masked, then each pigeon was tested on the same task while being forced to use the other eye. In a study using nine birds, eight of them did not show any “inter-ocular transfer” at all. What seemed to be a skill learned by the whole bird was in fact available to only half the bird; the other half had no idea.

An octopus trained on a visual task using just one eye initially remembered the task only when tested with the same eye. With extended training, they could perform the task using the other eye. The octopuses were unlike the pigeons in that some information did get across; they were unlike us in that it did not get across easily.

The special kind of mental fragmentation seen in split-brain humans seems to be a routine part of many animals’ life.

A simple interpretation of these cases holds that you need the ventral stream to have any experience of what’s coming in through your eyes at all. That is probably too simple. It’s likely that dorsal stream vision feels like something, though it doesn’t feel much like seeing.

The senses can do their basic work, and actions can be produced, with all this happening “in silence” as far as the organism’s experience is concerned. Then, at some stage in evolution, extra capacities appear that do give rise to subjective experience: the sensory streams are brought together, an “internal model” of the world arises, and there’s a recognition of time and self.

One might initially say it’s obvious that even simple animals respond to pain in a way that indicates they feel it, squirming and wriggling in distress. But things are not so straightforward. Many responses to bodily damage that seem to involve pain probably do not. For example, rats with a severed spinal cord, and hence no channel from the site of body damage to the brain, can exhibit some of what looks like “pain behavior,” and can even show a form of learning that responds to the damage. Various reflex responses in animals might look to us like pain, because we empathize with them. We need to go past these mere appearances.

Zebrafish were tested first to see which of two environments they preferred. They were then injected with a chemical suspected to cause pain, and in some cases, the less preferred environment had a painkiller dissolved in it. The fish now preferred this environment, but only when it contained dissolved painkiller. They made a choice they’d not normally make, and they made it in a situation where the idea of a more painful or less painful environment would be quite novel to them: evolution could not have set them up with a reflexive reaction to this situation. Similarly, in a study in chickens, birds with damaged legs chose a food that would usually be less preferred, provided that it contained painkillers. Robert Elwood has done experiments of a similar kind in hermit crabs, the small crabs who live in shells made by various mollusks. Hermit crabs are arthropods, relatives of insects. Elwood gave the crabs small electric shocks, and found they could be induced to leave their shell by a shock. But not always: they were more reluctant to leave a higher-quality shell than a low-quality one—they had to be shocked more.

Tests of this kind don’t suggest that all animals feel pain. Insects are in the same large animal group (arthropods) as crabs. Insects appear to behave normally, to the extent that they physically can, even after quite severe injuries. They don’t groom or protect injured parts of their body, but keep doing whatever they were doing. Crabs and some shrimp, in contrast, will groom injured areas. You can still doubt that these animals feel anything, yes. But you can doubt that about your next-door neighbor. Skepticism is always possible, but a case is being built here.

Sentience has some point to it. It’s not just a bathing in living activity.

Octopuses, as they evolved their complex behavioral abilities, opted for a partial delegation of autonomy to their arms. As a result, those arms are brimming with neurons and seem able to control some actions locally. Given that, what might octopus experience be like? The octopus may be in a sort of hybrid situation. For an octopus, its arms are partly self—they can be directed and used to manipulate things. But from the central brain’s perspective, they are partly non-self too, partly agents of their own. Let’s consider some analogies with our case, beginning with acts like blinking and breathing. These are activities that normally happen involuntarily, but through attention you can assert control over them. An octopus’s arm movements have something like this combination.

Action by an octopus, then, would mix elements that are usually distinct, or at least seem that way, in animals like us. When we act, the border between self and environment is usually fairly clear. If you move your arm, for example, you control the arm both on its general path and also in many fine details of its motions. Various other objects in the environment are not under your direct control at all, though they can be moved indirectly by manipulating them with your limbs. Uncontrolled movements by an object around you are usually a sign that it is not part of you (with partial exceptions for knee-jerk reflexes and the like). If you were an octopus, these distinctions would be blurred. To some extent you would guide your arms, and to some extent you would just watch them go.

Bence thinks that some relationships that look weird and novel in the octopus case are present in our case too, if we look hard enough. They are usually invisible to us, but they are there. Suppose you are reaching for an object with your hand. If the location or size of the target you are reaching for suddenly changes, your reaching movement changes extremely quickly—in less than a tenth of a second. This is so fast that it is unconscious. Subjects in experiments don’t notice the change—they don’t notice that they’ve changed their own movement, and don’t notice the change in the target object.

In the octopus case, the fine-tuning is greater—it’s more than just fine-tuning—and it does not only happen quickly. The octopus might watch some of the arm’s wandering as if it is a spectator. In us, these adjustments are too fast to see. In the case of humans, these rapid adjustments of the arm come from the brain, and they are visually guided. In the octopus, the motions are guided by the arm’s own chemical and tactile senses, not by vision

Cephalopods in general (not all, but a great many) are skilled color changers. In this prodigious group, giant cuttlefish are perhaps the pinnacle, or at least the most colorful. Some degree of color change is not rare in nature; many animals can modulate their surface color to some extent. Chameleons are the familiar example. But cephalopods are faster and produce a wider range of colors. In the case of large cuttlefish, the entire body is a screen on which patterns are played. The patterns are not just a series of snapshots, but moving shapes, like stripes and clouds. These seem to be immensely expressive animals, animals with a lot to say.

They ambush visitors with well-aimed squirts of water from their jets. But giant cuttlefish seem even more enigmatic and otherworldly than their octopus relatives. They have big brains, both in absolute terms (sheer size) and as a proportion of body mass.

The skin of a cephalopod is a layered screen controlled directly by the brain. Neurons reach from the brain through the body into the skin, where they control muscles. The muscles, in turn, control millions of pixel-like sacs of color. A cuttlefish senses or decides something, and its color changes in an instant. Here is how it works. The skin has an outer layer, a dermis, that acts as a covering. The next layer down contains the chromatophores, the most important of the color-control devices. A single chromatophore unit contains several different kinds of cells. One cell holds a sac of a colored chemical. Around it are muscle cells, one or two dozen of them, which pull the sac into different shapes. Those muscles are controlled by the brain. They stretch the sac to make its color visible, or relax it for the opposite effect. Each chromatophore contains just one color. Different cephalopod species use different colors, and usually the animal has three kinds. In a giant cuttlefish, the chromatophores are red, yellow, and black/brown.

But this mechanism has no means to produce many other colors a cuttlefish might display. There’s no way to produce blue, green, violet, or silver-white. Those colors are produced by mechanisms in the next layers of skin. Here we find several kinds of reflecting cells. These cells do not display fixed pigments, as chromatophores do, but reflect back incoming light. This reflecting need not be a simple mirroring. In iridophores, light is bounced and filtered through tiny stacks of plates. These plates separate and direct the light’s different wavelengths, shining back colors that can be different from those that came in. The results include the greens and blues that chromatophores cannot produce. These cells are not attached directly to the brain, but it seems that some of them are controlled, more slowly, by other chemical signals.

The cephalopod’s colored layers are thin and fragile. Cuttlefish look very different when they’ve lost skin through age or damage. Then you see dull white patches. The magic skin is a thin sheet on top of a plain white body.

Once I watched a large cuttlefish from above and saw the left side of its body displaying a passing cloud to another cuttlefish under a rock, while the right side was still and camouflaged, pointing out to sea. Cuttlefish’s color changes often occur in combination with changes to the shape of their body and skin. Sometimes they swim around with dozens of “papillae,” or folds of skin, sticking straight out from their back. These look like tiny versions, an inch or so high, of the plates on the back of a stegosaurus. These papillae have nothing hard inside them, and can be produced in a second. The eyes are the sites of finely detailed modifications in skin shape.

When showing aggression, males will often flatten their fourth arms into shapes like broad blades. Another aggressive gesture is to hold the two “first” arms up like horns. Some cuttlefish make these horns elegantly wavy. Others shape their arms into fiddleheads, hooks, or clubs.

Cephalopods, in almost all cases, are said to be color-blind. This impossible conclusion is based on both physiological and behavioral evidence.

Most humans have three kinds of photoreceptors. Color vision—using this system—requires at least two. Most cephalopods have only one.

This is baffling. These animals are doing so much with color. They are also superb at matching the color of their surroundings, for camouflage. How can you match colors you cannot see? Biologists sometimes offer explanations along these lines: First, cephalopods may be using subtle differences in brightness as indicators of the likely colors (hues) of objects around them, given the typical colors in their environment. Second, the reflecting cells, the mirrors in the skin, can help. You can produce a color you cannot see by reflecting it back from outside. This makes sense of some of what cephalopods can do. Camouflage can be achieved with reflection—if the color you aim to match in your background is also coming toward you from other directions. Simple reflection cannot be the explanation if an animal is matching a color behind its back, while the light coming in from the front is different.

Now we learn that an octopus can see with its skin. The skin is not only affected by light—something true of quite a few animals—but it responds by changing its own delicate, pixel-like color-controlling machinery. What could it be like to see with your skin? There could be no focusing of an image. Only general changes and washes of light could be detected. We don’t yet know whether the skin’s sensing is communicated to the brain, or whether the information remains local. Both possibilities stretch the imagination.

They noted that even if the photoreceptors in the skin are chemically the same as the ones in the eye, their light sensing might be modulated by the chromatophores, or other cells, around them. This might permit one kind of photoreceptor to behave like two. Some butterflies use a similar trick.

One possibility is that a chromatophore might sit on top of a light-sensitive cell, acting like a filter. That photoreceptor would then respond to colored light differently from a photoreceptor paired with a differently colored chromatophore. Another possibility was suggested to me by Lou Jost, an ecologist, orchid expert, and artist. He suggested that the act of changing colors might do the trick. Suppose some light-sensitive cells sit below a layer of many chromatophores. As chromatophores of different colors expanded and contracted, the light passing through them would be affected in different ways. If the animal kept track of which chromatophores were expanded, as well as how much light was reaching its sensors, it could know something about the color of incoming light. The animal would be like a cameraman exchanging one filter for another, as it went through its color changes. A monochrome sensor can detect color if the organism has filters of different colors and knows which ones are operating at each moment.

When it comes to camouflage, octopuses are unsurpassed.

Camouflage is the opposite of signaling; it’s producing colors in order not to be seen or recognized. In some species, signaling then arose—the camouflage machinery was pressed into service as a way of communicating and broadcasting. Colors and patterns were now produced to be seen and noted by observers, such as rivals or potential mates. Intermediate between the clear cases of camouflage and of signaling are deimatic displays. These are dramatic patterns often produced while fleeing a predator. It’s hypothesized that they are an attempt to startle or confuse the foe—to suddenly look different, and weird, in a way that might lead the predator to pause or lose their bearings. Here, the display is supposed to be noticed, but it does not send information to a receiver. It is merely supposed to be confusing or disruptive.

A large male will try to act as a “consort” to a female, monopolizing her and keeping other males away. When a rival male approaches, the consort and the intruder begin competitive displays. The two males will lie side by side quite close in the water. Each will stretch out as far as it can, often with a gentle curve in its body. They will blaze with color changes and patterns. Having stretched one way, a cuttlefish will often turn 180 degrees around and stretch out in the other direction. This turning, unfussed and deliberate, looks like a dance from the court of some civilized French king. The stretching, in contrast, looks like competitive yoga. The mix of yoga and courtly dance suffices to determine which cuttlefish is larger, and the larger almost always prevails.

Cuttlefish sex, if it results, is a peaceful affair by the standards of the animal kingdom. They mate head to head. The male attempts to grasp the female front-on. If she accepts him, he will envelop the female’s head with his arms. Having reached this position, there are a couple of minutes of stillness. Apparently he is blowing water at her with his funnel during this period. The male then uses his left fourth arm to take a sperm packet and place it in a special receptacle below the female’s beak, and, with more rapid motions, he breaks the packet open. They separate.

I think that some cephalopods, especially cuttlefish, have an expressiveness that goes beyond anything with a biological function.

Some cuttlefish, and a few octopuses, go through an almost continual, kaleidoscopic process of color change that appears disconnected from anything going on outside them, and appears instead to be an inadvertent expression of the electrochemical tumult inside them. Once the color-making machinery on the skin is wired to the electrical network of the brain, all sorts of colors and patterns might be produced that are simply side effects of what is going on within.

If you look closely at the “face” of a giant cuttlefish—the area between its eyes and down the first part of its arms—you will often see an ongoing murmur of very small color changes. Perhaps the machinery of color change is in an “idling” state there.

Brancusi favored shape rather than color, but if I looked closely, I would see a constant restlessness in all the colors on his face.

Suppose that by changing its colors a cephalopod affects the light that reaches sensors within its skin. Then some of these ongoing low-level color changes might be a way of surveying the chromatic environment.

In the playback experiments, a baboon would behave differently, being much more attentive, when a series of calls indicated an important event of this kind. As Cheney and Seyfarth say, it seems that the baboons construct a “narrative” from the series of sounds they hear. This is a tool they use for the purposes of social navigation.

Nicola Clayton and others at the University of Cambridge, through a long series of studies, have shown that birds can store food of different kinds in hundreds of distinct places to retrieve later, and can remember not only where they have put food but what was put in each place, so the more perishable items can be retrieved before the longer-lasting ones.

The chimps sometimes seemed to show “insight,” Köhler said; they could work through novel problems spontaneously. Most famously, they stacked boxes on top of each other and climbed up on them to reach food hanging out of reach. Köhler weakened the idea that there is a necessary link between language and complex thought. Some evidence pushes this way even in the human case. The Canadian psychologist Merlin Donald’s book Origins of the Modern Mind, published in 1991, made use of two “natural experiments.” First, he looked at evidence about the lives of deaf people in preliterate cultures that also lacked sign language. He argued that these people lived more normal lives than we’d expect if language was essential to complex thought.

When you move your head or shift your gaze, the image on your retina continually changes, but this is not perceived as a change in the objects around you. You continually compensate for your own eye movements, so when something does move in the environment, you register it. This requires that you keep track of your own decisions to act. With an efference copy mechanism, as you decide to act, sending a “command” of some sort to your muscles, you also send a faint image of the same command (a “copy” of it, in a rough sense of that term) to the part of the brain that deals with visual input. This enables that part to take into account what your own motions are doing.

Earlier, I mentioned John Dewey, who commented on Hume’s omission of inner speech when he described what he found within. For Dewey, inner speech was important but its role was largely recreational, a vehicle for storytelling. It’s odd that he did not discuss other uses. This might be because Dewey was so intensely social a philosopher; he thought that most of the important things we do take place out in the open. For Vygotsky, inner speech has a role in what is now called executive control. Inner speech gives us a way of performing actions in the right order (turn off the power first, then unplug the machine), and exerting top-down control over habits and whims (don’t eat another slice). Inner speech can also be a medium of experiment, for putting ideas together to see what comes of the combination (how would things look if I could travel as fast as light?). Within a terminology used by Daniel Kahneman and other psychologists, it’s a means for System 2 thinking. This is a slow, deliberate style of thinking we engage in when we encounter novel situations, as opposed to the rapid System 1 thinking that makes use of habits and intuitions. System 2 thinking tries to follow proper rules of reasoning, and tries to look at things from more than one side. It is ponderous but powerful.

But how could something as mundane as an efference copy system give rise to something so powerful? The mere existence of bits of language floating about inside us ought not to have so many consequences. Part of the explanation may lie in the way that sentences of inner speech can be attended to. They are made available to much of the brain in something like the same way that ordinary speech is. Indeed, the similarities are so strong that it’s easy for people to mistake sounds that exist only in their auditory imagination for sounds they are actually hearing. In an experiment done in 2001, people were told to listen to featureless random noise through a set of headphones, and were told that the song “White Christmas” might occasionally be played very quietly through the noise. They had to press a button if they were sure they’d heard the song. About a third of the subjects pressed the button at least once, but in fact the song was never played. The usual interpretation of the experiment is that the subjects in the experiment imagined the tune they were supposed to listen for, and sometimes mistook their own auditory image for a genuine playing of the song. The sounds we cook up in our heads, including the sounds of words, are broadcast in our minds in something like the way that many ordinary perceptual experiences are broadcast.

These phenomena, including the “White Christmas” experiment, have informed some attempts to explain a common symptom of schizophrenia in which people “hear voices” in a way that disrupts action and a sense of self.

Any ordinary human has at his or her disposal a field for the performance of countless invisible actions. The echoes and commentary, the chatter and cajoling, are as vivid as anything in our inner lives. You can be sitting motionless, watching an unchanging scene, and your mind can be alive with this stuff, teeming with it in a great jumble.

We often reflect on our inner states by forming inner questions, commentaries, and exhortations about them, and this is not idle or merely recreational; it can help us do things we’d not otherwise be able to do.

However language arose, its appearance changed the course of human evolution. By some path that we can presently only speculate about, language was also internalized; it became part of the machinery of thought.

Giant cuttlefish, these large and complicated animals, have very short lives: just one or two years. The same is true of octopuses; one or two years is a common lifespan. The largest, the giant Pacific octopus, can make it to about four years at the outside.

They spontaneously began to fall apart. Soon some were missing arms and clumps of flesh. They began to lose their magical skin. At first I thought some of them were producing white patches as part of a display, but a closer look showed that the outer layer of skin, the living video screen, was instead falling off, leaving plain white flesh behind. Their eyes went cloudy. As this process reaches its end, the cuttlefish is unable to control its height in the water. Once the decline starts, it occurs very quickly. Their health seems to drop off a cliff. Once I knew this stage was coming, interacting with these animals, especially the friendly ones, became poignant. Their time was so short. This discovery also made the puzzle of their large brains even more acute. What is the point of building a large nervous system if your life is over in a year or two? The machinery of intelligence is expensive, both to build and to run. The usefulness of learning, which large brains make possible, seems dependent on lifespan. What is the point of investing in a process of learning about the world if there is almost no time to put that information to use?

Cephalopods are evolution’s only experiment in big brains outside of the vertebrates.

A strange-looking rock-dwelling fish that inhabits the same patch of sea as my cephalopods is from a group that includes fish who live to two hundred years of age. Two hundred! This seemed extraordinarily unfair. A dull-looking fish lives for centuries while the cuttlefish, in their splendor, and the octopuses, in their curious intelligence, are dead before they are two?