Other Minds: The Octopus and the Evolution of Intelligent Life

by Peter Godfrey-Smith

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.

A bacterium is so small that its sensors alone can give it no indication of the direction that a good or bad chemical is coming from. To overcome this problem, the bacterium uses time to help it deal with space. The cell is not interested in how much of a chemical is present at any given moment, but rather in whether that concentration is increasing or decreasing. After all, if the cell swam in a straight line simply because the concentration of a desirable chemical was high, it might travel away from chemical nirvana, not toward it, depending on the direction it’s pointing. The bacterium solves this problem in an ingenious manner: as it senses its world, one mechanism registers what conditions are like right now, and another records how things were a few moments ago. The bacterium will swim in a straight line as long as the chemicals it senses seem better now than those it sensed a moment ago. If not, it’s preferable to change course.

We’re arriving at two thresholds, though, not one. In a world of single-celled aquatic life, we’ve seen how individuals can sense their surroundings and signal to others. But we’re about to look at the transition from single-celled life to many-celled life. Once that transition is under way, the signaling and sensing that connected one organism to another become the basis of new interactions which take place within the new forms of life now emerging. Sensing and signaling between organisms gives rise to sensing and signaling within an organism.

Even if Ediacaran life was not as peaceful as has sometimes been supposed, a very different world was around the corner. The “Cambrian explosion” began around 542 million years ago. In a relatively sudden series of events, most of the basic animal forms seen today arose. These “basic animal forms” did not include mammals, but did include vertebrates, in the form of fish. They also included arthropods – animals with an external skeleton and limbs with joints, such as trilobites – along with worms, and various others. Why did it happen then, and why did it happen so fast? The timing may have had to do with changes to the Earth’s chemistry and climate. But the process itself may have been largely driven by a kind of evolutionary feedback, due to interactions between organisms themselves. In the Cambrian, animals became part of each other’s lives in a new way, especially through predation. This means that when one kind of organism evolves a little, it changes the environment faced by other organisms, which evolve in response.

It took a long while for the octopuses to learn to do this, but in the end, nearly all of the octopuses that were tested succeeded. The eyes can guide the arms. At the same time, the paper also noted that when octopuses are doing well with this task, the arm that’s finding the food appears to do its own local exploration as it goes, crawling and feeling around. So it seems that two forms of control are working in tandem: there is central control of the arm’s overall path, via the eyes, combined with a fine-tuning of the search by the arm itself.

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.

Subjective experience is the most basic phenomenon that needs explaining, the fact that life feels like something to us. People sometimes now refer to this as explaining consciousness; they take subjective experience and consciousness to be the same thing. Instead, I see consciousness as one form of subjective experience, not the only form. For an example that motivates this distinction, take the case of pain. I wonder whether squid feel pain, and whether lobsters and bees do. I take this question to mean: Does damage feel like anything to a squid? Does it feel bad to them? This question would often now be expressed by asking whether squid are conscious. That always sounds misleading to me, as if it’s asking too much of the squid. To use an older term, if it feels like something to be a squid or octopus, then these are sentient beings. Sentience comes before consciousness.

Consider the case of tactile vision substitution systems (TVSS), a technology for the blind. A video camera is attached to a pad that sits on the blind person’s skin (for example, on their back). Optical images picked up by the camera are transformed into a form of energy (vibrations, or electrical stimulation) that can be felt on the skin. After some training with this device, the wearers start to report that the camera gives them an experience of objects located in space, not just a pattern of touches on their skin. If you are wearing such a system and a dog walks past, for example, the video system will make a moving pattern of presses or vibrations on your back, but under some circumstances this will not be experienced as vibrations on your back; instead you’ll experience an object moving out in front of you. This happens, though, only when the wearer is able to control the camera, to act and influence the incoming stream of stimulation. The user of the device has to be able to move the camera closer, change its angle, and so on. The simple way to do this is to attach the camera to the person’s body. Then the wearer can make objects loom, and come and go from the visual field. Subjective experience is intimately tied here to the interaction between behavior and sensory input. The moment-to-moment feedback between sensing and acting affects how sensory input itself feels.

In everyday experience there are two causal arcs. There is a sensory-motor arc, linking our senses to our actions, and a motor-to-sensory arc as well. Why turn the page? Because doing so will influence what you’ll see next. The second arc is not as tightly controlled as the first, because it extends into external, public space, rather than remaining inside the skin. Perhaps as you turn the page, someone grabs the book, or grabs you. The sense-to-motor and the motor-to-sense pathways are not on a par. But the neglected junior partner, the effect of action on what we sense next, is surely important. This, after all, is why we do much of what we do: to control what our senses will encounter.

An animal need not send out electrical pulses to encounter this problem. As the Swedish neuroscientist Björn Merker notes, it results just from being able to move. 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.

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. This is vivid in our own case; we experience the world in a way that ties together what we see with what we hear and touch. Our experience is usually of a unified scene. This might seen inevitable, a consequence of having eyes and ears attached to the same brain, but it is not. 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.

They argue that there are two “streams” by which visual information moves through the brain. The ventral stream, which takes a lower path through the brain, is concerned with categorization, recognition, and description of objects. The dorsal stream, which runs above it, closer to the top of the head, is concerned with real-time navigation through space (avoiding obstacles as you walk, getting the letter through the slot). Milner and Goodale argue that our subjective experience of vision, the feel of the visual world, comes only from the ventral stream. The dorsal stream does its work unconsciously, both in DF and in ourselves. After her accident, DF lost her ventral stream, and hence felt almost blind – even as she walked around the obstacles before her. 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. What we experience, in this view, is the internal model of the world that complex activities in us produce and sustain. Feeling starts there – or, at least, it begins to creep into existence when these capacities creep into existence – in the brains of monkeys and apes, dolphins, perhaps other mammals, and some birds. When we think of simpler animals as having subjective experience, according to this view, we’re projecting onto them a fainter version of our own kind of experience. This is a mistake because our experience relies on features they just don’t possess.

Subjective experience does not arise from the mere running of the system, but from the modulation of its state, from registering things that matter. These need not be external events; they might arise internally. But they are tracked because they matter and require a response. Sentience has some point to it. It’s not just a bathing in living activity.

To put it too anthropomorphically: you would send an arm out deliberately and hope the local fine-tuning goes right. 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. To tell the story this way is to tell it from the vantage point of the “central octopus.” That might be an error.

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. Each is much less than a millimeter in diameter.

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. If the skin’s sensing is carried to the brain, then the animal’s visual sensitivity would extend in all directions, beyond where the eyes can reach. If the skin’s sensing does not reach the brain, then each arm might see for itself, and keep what it sees to itself.

Cuttlefish and other cephalopods are brimming with output. Publish or perish. To some extent, this output is designed by evolution to be seen; sometimes it is camouflage, but sometimes it is meant be noticed, by rivals and the opposite sex. The screen also seems to run through much chatter and murmuring, happenstance expression. And even if cephalopods have hidden powers of color perception, a lot of their wild chromatic output is surely lost on watchers. The baboons, on the other hand, can say hardly anything. Their channel of communication is very limited. But they hear much more. These are both partial cases, unfinished, in a sense, though one should not think of evolution as goal-directed. Evolution is not heading anywhere, not toward us or anyone else. But I can’t resist seeing, in both animals, an unfinished quality. They are both animals with a one-sidedness in their version of the fundamental signaling duality, the interlocking roles of sender and receiver, producer and interpreter. On the baboon side, there’s a soap opera life, frantic and stressful social complexity, and little means to express it. On the cephalopod side, there’s a simpler social life, hence less to say, but such extraordinary things expressed nonetheless.

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. Once a sentence of inner speech is composed, it is exposed to the same sort of processing that would apply to a sentence we hear.

Inner speech provides one way we are able to route things through our minds in such a way that information can be assessed and used. Inner speech does not live in a little box in your brain; inner speech is a way your brain creates a loop, intertwining the construction of thoughts and the reception of them. And when that’s done, the format provided by language allows you to bring ideas together in an organized structure.

In 1950, the German physiologists Erich von Holst and Horst Mittelstaedt introduced a framework for talking about these relationships. I used one of their terms earlier in this chapter: efference copy. I’ll now outline some more of their framework. They used the term afference to refer to everything you take in through the senses. Some of what comes in is due to changes in the objects around you – that is exafference (with “ex” for outside, and pronounced in the same sort of way as “ex-boyfriend”) – and some of what comes in is due to your own actions: that is reafference (pronounced “re-afference”). Animals face the challenge of distinguishing between the two. Reafference makes perception more ambiguous. If your own actions did not alter what your senses pick up, life would be easier in some ways. One way to deal with the problem is with the “efference copy” mechanisms I described earlier. As you move, you send a signal to the parts of yourself that deal with perception, telling them to ignore some of what comes in: “Don’t worry, that’s just me.” Problems stem from reafference, but so do opportunities. You can affect your own senses in useful ways. Here the aim is not to filter out an unwanted contribution to what is perceived, but instead to use your actions to feed perception. A simple example is writing something down, a note to yourself, which you will read later. You act now, changing the environment, and later you will perceive the results of your act. This will ena...

Mutations often tend to affect particular stages in life. Some act earlier, others act later. Suppose a harmful mutation arises in our imaginary population which affects its carriers only when they have been around for many years. The individuals carrying this mutation do fine, for a while. They reproduce and pass it on. Most of the individuals carrying the mutation are never affected by it, because some other cause of death gets them before the mutation has any effect. Only someone who lives for an unusually long time will encounter its bad effects. Because we are assuming that individuals can reproduce through all their long lives, there is some tendency for natural selection to act against this late-acting mutation. Among individuals who live for a very long time, those without the mutation are likely to have more offspring than those who have it. But hardly anyone lives long enough for this fact to make a difference. So the “selection pressure” against a late-acting harmful mutation is very slight. When molecular accidents put mutations into the population, as described above, the late-acting mutations will be cleaned out less efficiently than early-acting ones.

It’s not that the loss of a shell alone created the evolutionary pressure leading to those nervous systems. Rather, a feedback system was established. The possibilities inherent in this body create an opportunity for the evolution of finer behavioral control. And once you have a larger nervous system, this makes it worthwhile to further expand the body’s possibilities – collecting all those sensors on the arms, creating the machinery of color change and a skin that can see. The loss of the shell also had another effect: it made the animals much more vulnerable to predators, especially fast-moving fish, with bones and teeth and good vision. That put a premium on the evolution of wiles and camouflage. But there is only so much those tricks will achieve, only so many times they will save the animal. An octopus can’t expect to live a long time, especially as they must be active as predators themselves. They can’t just hide in a hole and wait for food to come to them. They have to be out and about, and once in the open they are vulnerable. This vulnerability makes them ideal candidates for the Medawar and Williams effects to compress their natural lifespan; a cephalopod’s lifespan has been tuned by the continual risk of not making it to the next day. As a result, they have ended up with their unusual combination: a very large nervous system and a very short life. They have the large nervous system because of what those unbounded bodies make possible and the need to hunt while b...

Memory in animals has several varieties. An important kind of memory in human experience is episodic memory – memory of particular events, as opposed to memory of facts or skills. (Your memory of your last birthday is an episodic memory; your memory of how to swim is a procedural memory, and your memory of the location of France is a semantic memory.)