The Wandering Mind

by Michael C Corballis

  Thou hast made him to have dominion over the works of thy hand;

  Thou hast put all things under his feet:

  All sheep and oxen, yea, and the beasts of the field;

  The fowls of the air, and the fish of the sea . . .

  The main problem in deciding whether non-human animals have human-like thoughts is that only humans have articulate language. Language itself is a ‘higher mental faculty’, to use Lloyd Morgan’s expression, and indeed some philosophers and linguists have maintained—wrongly, I think—that the very act of thinking depends on language. But whether or not this is so, we can discover a lot about thought by simply asking people to tell us of their experiences and thoughts. People have no difficulty describing their mental time travels—their memories, plans and fantasies. But even our closest non-human relatives, chimpanzees and bonobos, cannot actually tell us what’s on their minds. Neither can the rather talkative parrot.

  Maybe, though, there is another road into the animal mind that can help, and suggest that animals may indeed be capable of mental time travels. To explain this, I need to introduce you to another animal (or two).

  4.

  THE HIPPO IN THE BRAIN

  …

  You may think that there are other more important differences between you and an ape, such as being able to speak, and make machines, and know right from wrong, and say your prayers, and other little matters of that kind; but that is a child’s fancy, my dear. Nothing is to be depended on but the great hippopotamus test.

  —Charles Kingsley, from The Water-Babies

  Kingsley was not referring to that large animal, but to a small structure in the brain known as the hippocampus minor. This structure was of intense interest following the 1859 publication of Darwin’s Origin of Species, because the distinguished anatomist Richard Owen maintained that only humans possessed it. This showed, he said, that humans could not be descended from apes, as Darwin’s theory implied. Darwin, normally mild-mannered, didn’t much care for Owen, once describing him as ‘spiteful, unfair, ungenerous, extremely malignant, false, rude, unjust, illiberal and disingenuous’. In defence of Darwin’s theory, Thomas Henry Huxley, also known as ‘Darwin’s bulldog’, showed Owen to be wrong by demonstrating that all apes in fact do possess a hippocampus minor. Although a minister of the church, the reverend Charles Kingsley was one of the first to praise Darwin’s book, and his satirical reference to the hippopotamus was a gibe at the esteeemed Dr Owen.

  But Kingsley himself seems to have been a little confused. Following the above passage, he went on:

  If you have a hippopotamus major in your brain, you are no

  ape, though you had four hands, no feet, and were more apish

  than the apes of all aperies. But if a hippopotamus major is ever

  discovered in one single ape’s brain, nothing will save your

  great-great-great-great-great-great-great-great-great-great-great-

  greater-greatest-grandmother from having been an ape too.

  Well, the confusion between hippocampus and hippopotamus was no doubt deliberate and intended satirically, but it was the hippocampus minor, not the hippocampus major, that was supposedly the critical structure. But perhaps he was prophetic, as we shall see.

  The hippocampus minor soon disappeared as a serious contender for human uniqueness, or indeed for anything else, and even lost its name. It is now known by its original name of ‘calcar avis’, meaning cock’s spur. In an entertaining article on the acrimonious debates between Owen and Huxley, Charles Gross remarks that after the controversy had subsided, the calcar avis was to be found ‘only in obscure corners of human anatomy texts, where it still rests’.1

  Of much more interest, as unintentionally foreseen by Charles Kingsley, is the hippocampus major, now better known simply as the hippocampus with the demotion of its one-time junior partner. It’s not so much a hippopotamus that we house in our brains as a seahorse, since hippocampus means ‘seahorse’ in Greek. It was named for its resemblance to that undulating creature, in which the male carries the young (in case you didn’t know). It is a structure on the inner surface of the temporal lobes of the brain—roughly behind your ears.

  It is the hippocampus that is utterly critical to mental time travel—our ability to travel mentally backward and forward in time. The common feature of the amnesic cases Henry Molaison and K.C. and Clive Wearing, introduced if you remember in Chapter 2, is that all had suffered major loss of tissue in the hippocampus. In her book on Clive, Deborah Wearing records that she was shown a scan of his brain, and writes that ‘by the time they had figured out what was wrong with Clive and started pumping the anti-viral drugs into him all he had left were seahorse-shaped-scars where his memory used to be’.

  Figure 4.1. The hippocampus (left) and the real seahorse (right).

  And it is the hippocampus that is at the hub of the system that lights up when people wander mentally back and forth in time. In preceding chapters, I also mentioned the Cluedo-like experiments in which we ask our subjects to recall 100 events in their lives, and then rearrange the people, objects and places featuring in these events and ask our long-suffering participants to imagine future scenarios based on these novel arrangements. The subjects lie in the MRI scanner while they perform these feats, and the areas of the brain that are activated correspond largely to the default-mode network. This is the ‘mind-wandering’ network, and includes prefrontal lobes, temporal lobes and parietal lobes. It matters little whether the participants are recalling the past or imagining future events—the activated areas overlap quite extensively.

  The hippocampus is the Grand Central Station of this network, reciprocally connected to other areas in the network, including both the cortical areas above and the more emotional areas below. It is responsible for what has been called ‘temporal consciousness’, or knowing where you are in the ribbon of time. Oddly enough, although people with damage to the hippocampus seem lost in time and stuck in the present, they may still be able to answer questions about events in time that do not involve themselves—such as the death of Princess Diana, or what the next medical breakthroughs are likely to be. The job description of the hippocampus, it seems, is to deal with personal matters—the recording and retrieval of personal events, and the making of personal plans.

  The hippocampus seems to be a forward-looking structure, with the front (anterior) end concerned more with the future and the rear (posterior) end with the past. In our Cluedo study, when people imagined future scenarios, and were later asked to try to remember them, both ends of the hippocampus were often activated. That is, imagined scenes were also remembered as though they had actually occurred. This could perhaps help explain why some memories are false—for instance, why Hillary Clinton remembered running to escape gunfire when she arrived in Bosnia, when in fact her arrival was peaceful and welcoming. Maybe she had imagined the threatening scenario before arriving there, and this memory had lodged in her brain as though it had actually happened. But who knows? Possibly Hillary herself doesn’t know.

  Besides its role in mental time travel, the hippocampus has another talent. It records locations in space. In 1978, John O’Keefe and Lynn Nadel (one-time PhD classmates of mine) wrote a book that has become a classic of neuroscience, called The Hippocampus as a Cognitive Map. Their work was based on the recording of activity from microelectrodes inserted into different regions of the hippocampus of the rat. If the rat was placed in a maze, the location of activity corresponded to where the animal was located. The single cells (or neurons) became known as ‘place cells’—a bit like a GPS system lodged in the brain itself.

  It turns out that our own human hippocampus also contains place cells. In a report published in 2003, neurosurgeons inserted electrodes in the hippocampi and other brain areas in patients being monitored for potential surgery for intractable epilepsy. Their purpose was to locate the seizure foci, but the electrodes also allowed them to record from single cells while the patients explored a
nd navigated a virtual town on a computer screen. Some of the hippocampal cells responded to specific locations in the virtual town. Cells in the adjacent parahippocampal region also responded to views of landmarks in the town.

  The hippocampus is not a static map, though. Activity in place cells adjusts when the animal, rat or human, moves into a new environment. Maps can also exist at different scales, much like the zoom function on internet maps. For instance, it appears that small-scale maps are located in toward the rear of the hippocampus, and large-scale maps toward the front. The coding of time is also graded, like an adjustable calendar. You can replay your past or imagine your future over years, days, or minutes. The representation of space-time in the hippocampus and neighbouring regions is complex, and not yet fully worked out.

  The hippocampus also seems to swell to meet spatial demand. London taxi drivers have to undergo extensive training to learn the precise geography of that large and confusing city. They must be able to decide the quickest route to a passenger’s destination immediately, without looking at a map, consulting a GPS system, or asking a controller by radio or cellphone. This requirement was set up in 1865, and is known as ‘The Knowledge’. Brain-imaging has shown that the hippocampi of these taxi drivers are unusually enlarged. They are also larger than those of London bus drivers, who simply have to follow designated routes. London bus drivers, though, are better than the taxi drivers at learning new spatial tasks, suggesting that the taxi drivers may already have crammed about as much spatial information into their hippocampi as those little seahorses can take. In any event, it seems that the hippocampus is as important to knowing where you are in humans as it is in rats.

  In rats, as in humans, the hippocampus also plays a critical role in laying down memories. It has been known for some time that if you stimulate a cell in the hippocampus with a high-frequency volley of electrical pulses, the connection (synapse) between that cell and the upstream one it connects to is strengthened. The effect is known as ‘long-term potentiation’, and is long-lasting, sometimes persisting for months. It was originally demonstrated in the rabbit in 1966 by Terje Lømo in Oslo, Norway, but has since been widely studied in rats, as in other species. It is generally considered to be the basis of memory. Your memories, then, are established through the strengthening of connections in your brain, with the hippocampus playing the commanding role. This is not to say that memories are lodged in the hippocampus alone. Long-term potentiation may hold them there for a while, but they eventually diffuse into other regions of the brain. And it’s the hippocampus that finds them again.

  We should not be surprised that the hippocampus is involved in recording where we are in space as well as in time, since mental time travel takes place in a space-time manifold. It is, as I suggested earlier, the Grand Central Station for our mental excursions, recording our mental comings and goings. But its seemingly similar roles in rat and human open the possibility of answering the question I raised in the previous chapter: is mental time travel unique to humans?

  The secret life of Walter Ratty

  In their classic 1978 book, O’Keefe and Nadel wrote that the addition of a temporal component ‘changes the basic spatial map into a human episodic memory system’. The question has since arisen, though, as to whether the temporal component was already present in our mammalian forebears. Recent evidence suggests that even rats may imagine past and future events.

  Place cells in the rat hippocampus are occasionally active after the rat has been in some specific environment, such as a maze, as though the animal is actively remembering where it was, or perhaps imagining where it will be—or might be. This activation occurs in what are known as ‘sharp-wave ripples’ which sweep out sequences of place cells, as though the animal is mentally tracing out a trajectory in the maze. This occurs sometimes when the animal is asleep, or when it is awake but immobile. It is as though the animal is replaying its experience in the maze, perhaps while dreaming or daydreaming—for a laboratory rat, being in a maze is probably the most exciting event of its day. The ripples, then, suggest that the rat is mentally wandering from one part of the maze to another.

  These mental perambulations need not correspond to the paths that the rat actually traversed. Sometimes the ripples sweep out a path that is precisely the reverse of one the rat actually took. It may be a path corresponding to a section of the maze the rat didn’t even visit, or a short cut between locations that wasn’t actually traversed. One interpretation is that the ripples function to consolidate the memory for the maze, laying down a memory for it that goes beyond experience, establishing a more extensive cognitive map for future use. But mind-wandering and consolidation may be much the same thing. One reason that we daydream—or even dream at night—may be to strengthen our memories of the past, and allow us, and the rat, to envisage future events. I return to the dream world in Chapter 7.

  The imagined trajectories, if that is what they are, are more rapid than the actual ones. I think this is true of our own mental wandering. It takes me about an hour to walk to my place of work from my home, but when I imagine the walk, and the landmarks I encounter, it takes less than a minute or so. Mentally, we travel in the fast lane. It is not altogether clear, though, whether time itself moves faster in the mental world, or whether we flit from location to location, leaving out chunks of the journey.

  In another clever experiment, rats were placed in an environment with 36 food wells, arranged in a six-by-six array. They were given experience eating from these wells, so they learned the environment pretty well. One particular food well was then established as a Home location where food could be found, and the rats were then lured to different locations from which they had to find their way Home. The researchers recorded from multiple sites in the hippocampus, and discovered ripples corresponding to these Home routes, but they were played before the rat actually embarked on the journey. What is interesting is that they were generally routes the animals had not actually traversed before. This seems to be mental time travel into a future event. The authors of the study suggest that the hippocampus ‘functions in multiple conceptual contexts: as a cognitive map in which routes to goals might be explored flexibly before behaviour, as an episodic memory system engaging in what has been termed “mental time travel” . . .’. The hippocampus, in other words, can lay out an action plan.

  Perhaps to labour the point, recordings from the hippocampus seem also to tell which way a rat will turn at a choice point in a maze. The rats in question were trained to alternate left and right turns at a particular spot in the maze. Between trials, they were taken out of the maze and placed in a running wheel. While they were running, recordings from their rippling hippocampi again revealed activity corresponding to paths taken in the maze, including which way they would turn when next placed in the maze. The rats, it seems, were planning their next turn. My mind wanders, too, when I’m on a treadmill, but I also use time on the treadmill to figure out what I might do later. How do we know the rat was not just reminiscing about the way it turned on some previous trial, and not on what way they will turn next? Well, perhaps because of the time they spent in the running wheel, they sometimes made errors when placed back in the maze—say, turning left instead of right. But this error was signalled by the hippocampal activity, showing that the rat was actually planning a wrong turn. The study’s authors write that activity in the hippocampus, ‘having evolved for the computation of distances, can also support the episodic recall of events and the planning of action sequences and goals’.

  Maybe hippocampal recordings might one day help goalies know in advance which way the kicker will shoot when given a free kick at the goal.

  I have dwelt on these rat experiments because they seem to show that even the humble rat indulges in mental time travel. Like rats, we are creatures that move on the face of the earth, so space is fundamental to our wanderings, both physical and mental. It would not be surprising, then, if our mental time travels did evolve from the simple replaying, a
nd pre-playing, of spatial movements. You have to go back some 66 million years to find the common ancestor of rat and human. Over that long interval our mental faculties have surely diverged, but in a spatial world the mechanisms involved in living, remembering and planning in space are critical, and are probably conserved through evolutionary time. Mental time travel may well be one of the earliest of mental faculties to evolve. It is fundamental to all moving animals to know where they are, where they’ve been, and where they’re going next. In Chapter 2, I described the mnemonic device known as the method of loci, whereby we remember lists of things by locating them mentally in some familiar terrain, and then mentally wander through the terrain to recover them. This no doubt derives from our spatial heritage.

  What about birds, who are surely the experts in spatial travel? They indulged in air travel long before we humans did, and still do it much more gracefully than we do in our clumsy air machines. For a while it was thought that birds did not have hippocampi, leading to the frivolous theory that the function of the hippocampus was to prevent flight. But the bird brain is organised rather differently from the mammalian one, and it turns out that there is a region in the bird brain that is homologous to the mammalian hippocampus. It develops from a region of the embryo that corresponds to the part of the mammalian embryo from which the mammalian hippocampus derives. Anatomists now identify this region as the avian hippocampus. Far from preventing flight, the avian hippocampus is critical to their travel plans, as well as their food-gathering strategies. Not surprisingly, birds that cache food in multiple locations have larger hippocampi than those that don’t. In this, they are the avian equivalents of London taxi drivers.

  Of course, our own mental travels are more complex than simply moving from place to place. For a start, our cognitive maps are extraordinarily flexible. As I suggested earlier, they can zoom. Let me take you on a brief tour. First, imagine you are sitting at your desk (as I am right now). You can imagine the other objects on the desk—a half-finished crossword, a small stack of books, an empty cup. Zoom back a little and imagine the room, the sofa, the bookcase lining the far wall, the door leading to the hallway. Zoom back further and take a mental wander around the house (or apartment). Zoom out now to the suburb, the small row of shops, the bus stop, the intersection of streets. Take a deep breath and keep zooming—to the city, the country, the world. You can also flit about—to Paris, New York, or the place with the forgotten name in the Italian Alps.