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Octopuses鈥� astonishing mental skills might help us unearth the roots of intelligence 鈥� but first we need to understand what makes them so smart

BETTY the octopus is curled up in her den, eyes half-closed and clutching a piece of red Lego like a child with a teddy bear. She is, says Kerry Perkins, cephalopod researcher at the Sea Life aquarium in Brighton, UK, much better behaved than some of the octopuses she has worked with. One used to short-circuit a light in its tank by squirting water at it, and would do so whenever the bulb was left on at night. Another made a bid for freedom via the aquarium drainage system, which it seemed to know headed straight out to sea. 鈥淎ny octopus tank worth its salt has a way of stopping the octopus from escaping,鈥� Perkins says as she adds two weights to the lid of Betty鈥檚 tank. 鈥淭hey love to explore.鈥�

Aristotle once took this kind of curiosity as a sign that octopuses are stupid 鈥� after all, he pointed out, just waving your hands in their direction brings them close enough to catch. We now know that it is just one example of how smart they are. Between them, cephalopods, which also include squids, cuttlefish and nautiluses, can navigate a maze, use tools, mimic other species, learn from each other and solve complex problems. If the latest analyses are to be believed, these skills might show a rudimentary form of consciousness.

Cephalopods are the only invertebrates that can boast anything like this kind of mental prowess, and some of their more impressive tricks are shared with only the cleverest vertebrates, such as chimps, dolphins and crows. Yet they evolved along a completely separate path, from snail-like ancestors, and their brains look completely alien to our own (see 鈥淎 brain apart鈥�).

Understanding how these two very different pathways converged on the same amazing abilities therefore promises to get to the very root of intelligence. After 50 years of research, the latest anatomical studies are finally throwing up some insights, revealing what kind of architecture is necessary for complex behaviour. Some researchers, meanwhile, are examining the intriguing questions of when and why this kind of intelligence evolved, and which animals got there first.

Until recently, looking at the inner workings of cephalopod brains was impossible 鈥� the tools available couldn鈥檛 delve much deeper than basic anatomy. In the 1950s and 60s, renowned neurophysiologist J.Z.Young mapped the major lobes of the cephalopod brain and what they do. But without the means to study the brain at the level of individual nerve cells and connections, or to examine living ones, Young鈥檚 work ground to a halt in the 1980s. Still, it was not before he and others had noted several similarities between the cephalopod brain and those of intelligent vertebrates.

For one thing, the cephalopod brain is concentrated in the head, as opposed to the rope-ladders of nerve knots, or ganglia, that run the length of the bodies of their closest mollusc relatives. Like ours it is lateralised, meaning that it is split into two halves connected by a bundle of nerve fibres, and then divided into further specialised lobes. Also like the mammalian brain, some of these lobes are folded, greatly increasing surface area, and some regions have miniaturised neurons, enabling more of them to be packed in. The distance between neurons is also shorter than in other molluscs, allowing faster transmission of impulses through the brain. All this adds up to a brain that can process information rapidly, with plenty of room for memory storage.

Over the past few years researchers have delved deeper, adapting the latest techniques to study living brain tissue. And the closer they look at these strange minds, the more parallels they find with our own brains.

鈥淭he closer researchers look at these strange minds, the more parallels they find with our own brains鈥�

, a neurophysiologist at the Hebrew University of Jerusalem in Israel, is at the forefront of this work. He recently adapted methods used to study live slices of vertebrate brains to keep samples of octopus brain alive in a bath of oxygenated salt water. He then passed electrical impulses through the tissue and recorded the routes they took.

Using this technique Hochner has found that neurons in the vertical lobe, long known to be the site of learning and memory in most cephalopods, are organised much like the vertebrate hippocampus, which does more or less the same job. Both have large numbers of input fibres from the senses, and these run at right angles across great swathes of smaller processing neurons, making lots of connections before converging on a narrower tract of output fibres (). Hochner also found that the octopus peduncle lobe and the vertebrate cerebellum, which both control movement, share a similar structure 鈥� they have lots of thin fibres lined up next to each other.

These similarities are fascinating when you consider that cephalopod neurons are much simpler than vertebrate brain cells: their synaptic connections involve fewer proteins, for example, and they lack a fatty myelin covering that in vertebrates helps to speed up signal transmission. All this suggests that when it comes to intelligent behaviour, it is the overall architecture of the brain that counts, not the building blocks. 鈥淚t鈥檚 just a matter of how you construct the networks,鈥� says Hochner.

Octopuses behaving badly

A criss-crossed system of nerve fibres and neurons might be the best way to facilitate complex learning and memory, for instance, since it maximises the number of synaptic connections involved in memory storage. The arrays of parallel fibres, meanwhile, might be the most efficient way to deal with lots of sensory information quickly, giving the creature better control of its movements.

It鈥檚 early days, but Hochner hopes to build on this work by watching learning and memory as it happens in the brain of a living octopus. 鈥淲e don鈥檛 know in what forms this information is coded and treated and processed. This is something we would like to do more by doing recordings in the behaving animal,鈥� he says.

This is no mean feat, however. Octopuses make it notoriously difficult to get recordings from electrodes inserted into the brain, because they can selectively shut off blood supply to an area of their body or brain. That鈥檚 if they allow the researchers to insert electrodes at all. , a cephalopod researcher at the City University of New York tells the story of one colleague who took on that challenge: 鈥淗e thought the octopus was anaesthetised, so they put the electrode in and the octopus reached up with an arm and pulled it out.鈥� That marked the end of his work with octopuses. 鈥淗e has worked with lots of animals but he said 鈥榯hat animal knows what I鈥檓 thinking. He doesn鈥檛 want me to do this so I鈥檓 not going to鈥�,鈥� Basil says.

Basil鈥檚 colleague was joking, but some researchers strongly suspect that octopuses, and perhaps cuttlefish and squid, have a basic form of consciousness. The leading proponent of the idea is , a comparative psychologist at the University of Lethbridge in Alberta, Canada. Consciousness is difficult to define, but Mather says that if you consider it to be a notion of self in space and an ability to make decisions based on information from previous experience and the current situation, cephalopods pass with flying colours.

Experiments in the 1980s, for example, offered octopuses a tasty hermit crab with a stinging anemone on its back. Unlike other predators, the octopuses didn鈥檛 back off after the first sting. Instead they tried various strategies to get rid of the anemone: jetting water at it from their siphon, attacking from below, and attempting to delicately extract the crab with one tentacle. Octopuses show similar cunning when they are presented with a clam 鈥� they will often try to get at the meat inside by drilling a hole with their beak, before injecting a poison to stop the clam鈥檚 heart or disable the muscles that clamp the shell shut. 鈥淭here is some evidence that the location of the hole that is drilled is learned 鈥� it is no use putting it in most places,鈥� says Mather. 鈥淚 think that this has to be 鈥榙ecision-making鈥�.鈥�

Inspired by these findings, Mather drew the latest results together in 2008, building a strong case for cephalopod consciousness (). She was able to include numerous other examples of the kinds of advanced abilities that might constitute conscious thought. Octopuses and cuttlefish can learn by observing each other, for example, something that suggests a notion of 鈥渟elf鈥� and 鈥渙ther鈥� and perhaps the ability to put themselves mentally in that position. Cuttlefish also seem able to send contradictory signals simultaneously: a male might show a courtship display to a female facing one side of his body and a 鈥渂ack off鈥� display on the other to a challenging male, for example. At other times, a male might try to deceive his love-rivals by wearing a female-like pattern that leads the other males to believe he is no threat, as he edges closer to his mate. These look a lot like conscious decisions based on the information at hand.

More recent findings would seem to back up Mather鈥檚 conclusions. A 2009 study, for example, reported that veined octopuses (Amphioctopus marginatus) will hulk a heavy shell around all day in case it comes in handy for shelter later on (). This rare example of tool use suggests an ability to plan ahead, showing the kind of complex decision-making that defines consciousness. And a report last year showed an octopus mimicking the movements of a flounder to avoid the attention of predators, though it may just be an innate response The Biological Bulletin, vol 218, p 15).

鈥淰eined octopuses will hulk a heavy shell around all day because they know it might come in handy for shelter鈥�

Basil, who works mainly with nautiluses, says the behavioural evidence is 鈥渢antalising鈥�. 鈥淭ool use and observational learning suggests to me that if you are able to look at another entity and know that it is 鈥榦ther鈥�, then there鈥檚 likely to be a sense of self.鈥� However, she warns that when a creature is so different to us, it is difficult to have any idea of what they are thinking, or even if they are thinking at all.

To get round this, Basil plans to look for direct physical evidence of consciousness in the brain itself. 鈥淲e have mirror neurons, which we use to infer emotional states of others 鈥� to infer what is going on in another鈥檚 brain. If we can find something equivalent in cephalopods that would be a good piece of evidence to start with,鈥� she says. Mirror neurons seem to fire both when an animal observes another individual performing an action and when it performs the action itself. Basil plans to start looking for this kind of activity in the olfactory lobe of her nautiluses, the equivalent of the vertical lobe in octopuses, where learning and memory takes place.

Early origins

If something akin to a mirror neuron were to turn up in the nautilus it would be a huge surprise. Nautiluses have been around for almost 500 million years, meaning that they are probably very similar to the common ancestor of all cephalopods (see timeline). According to the received wisdom, cephalopods didn鈥檛 evolve their big brains until much later 鈥� 65 million years ago 鈥� when they started to face increased competition from bony fish. They had to adapt fast, and this brought about a 鈥渃ognitive radiation鈥� 鈥� a fast track to a big brain and complex behaviour. A neuron in the nautilus that seems to underlie conscious behaviour might suggest that the earliest cephalopods were already on the road to a complex brain.

There鈥檚 not any evidence for this yet, but Basil, along with Frank Grasso, a comparative psychologist at the City University of New York, already has some reason to think that cephalopods evolved complex behaviours early in their evolutionary history, perhaps as a result of infighting within the group. They recently put some nautiluses through the kinds of tests previously reserved for the other cephalopods. While their brains are nowhere near as complex as their younger relatives, they have many of the same abilities in learning, memory and spatial awareness. 鈥淭hey remember a very complex maze with visual elements in it for three months, just like an octopus. Never in a million years would I have thought that,鈥� says Basil.

If these suspicions pan out with future work, it could mean cephalopods developed their skills hundreds of millions of years ago.

That would be a serious blow to our mammalian pride. We often consider warm-blooded vertebrates to be the poster children for intelligence on Earth, but in the race to evolve a brain that can make sense of the world it lives in, there鈥檚 every chance the mollusc got there first.