Wayfinding

by M. R. O'Connor

  2. Thirteen kilometres south-west to a site where kante, sharp flints used for stone knives, were found. This was beside a low rise in the ground.

  3. Five kilometres south-east, then round the end of a sandhill to Rungkaratjunku, a sacred site.

  4. Winding in and out between low sandhills, generally west-south-west, sixteen kilometres to Tjulyurnya rock hole by a little hill. The sacred place was two kilometres further on.

  When they arrived at Tjulyurnya, they gathered some of the stones and planned to make camp for the night. But the Aboriginal men started to worry. Had they made a mistake bringing white people to the Dreaming site? Perhaps they shouldn’t have moved any of the stones. Finally, they decided it was best to get back to their previous camp as fast as possible. Everyone got into the two vehicles and shut the windows tightly in order to keep out devil dingo sprits. That’s when disaster seemed to strike.

  “It got so dark we lost the track,” said Myers. (Lewis speculated that the headlights also effaced their night vision and masked the terrain.) “And we drove until we came right around back to where we had started. The men were freaking out because they thought the spirits were dragging us back. The same thing happened again when Jeffrey drove and now they were really freaking out.” Finally their non-Aboriginal mechanic, David Bond, navigated by keeping the Southern Cross in the righthand window to take an easterly course, getting them back to their original camp. What Lewis surmised was that despite the Pintupi’s faultless navigation skills, they were incapable of wayfinding according to the stars. But in Myers’s opinion the problem was not the stars but the speed of the cars they were driving. “When you are walking, you don’t lose your sense of direction. They know where the stars are, they know where the star comes up but I think they don’t need it,” he told me. “How they process [directionality] as they are walking is with bodily orientation. They don’t stop to say, which way is the north? It’s not a matter of calculation, or a simple cognitive thing. It’s very much a constant tracking.”

  By the time Lewis’s research in Australia ended, he had come to believe that his companions’ wayfinding abilities came down to “some kind of dynamic image or mental ‘map’, which was continually updated in terms of time, distance and bearing, and more radically realigned at each change of direction, so that the hunters remained at all times aware of the precise direction of their base and/or objective.” Unbeknownst to him, at the same time he was roaming the desert with the men from Papunya, two neuroscientists over nine thousand miles away in London were developing a very similar theory of human navigation according to a mental map in the brain.

  SPACE AND TIME IN THE BRAIN

  In the early 1970s a young American scientist by the name of John O’Keefe went in search of one thing but got lost and discovered another. Like so many scientific breakthroughs, curiosity, skill, and luck colluded, and in this case, the accident garnered him a Nobel Prize. O’Keefe was interested in recording single neuron activity in the amygdala—the place of emotional learning. One day at his laboratory at University College London he attempted to implant a microelectrode in a rat’s somatosensory thalamus, the place where sensory perceptions are processed. However, he used the wrong coordinates and ended up inserting the electrode into the rat’s hippocampus. As the single cell O’Keefe was recording began to fire, its pattern struck him as peculiar. The cell’s activity seemed to be strongly correlated with the animal’s locomotion. His interest piqued, O’Keefe abandoned his research on the amygdala and began recording single hippocampal cells of rats while they were eating, grooming, and exploring.

  He wasn’t the first to record these cells: a Russian neuroscientist named Olga Vinogradova had recorded them in rabbits in 1970 and thought they might be responses to stimuli. O’Keefe inferred a different significance. As he wrote, “Over a period of months, I began to suspect that their activity didn’t depend so much on what the animal was doing or why it was doing it but had something to do with where it was doing it. Then on one electrifying day I realized with a flash of insight that the cells were responding to the animal’s location or place in the environment.”

  O’Keefe began changing aspects of the rat’s environment and watched the effect on hippocampal cell activity. Even when he turned the lights off in a familiar maze, the cells continued to fire. It didn’t matter which direction the rat was facing, or whether rewards were taken away or changed. The only stimulus that seemed to matter to the cells was the rat’s location. Rather than respond to the changes in stimuli, the cells were signaling an abstract concept of space. O’Keefe called them place cells.

  In the decades since, these cells have fascinated researchers with their plastic, almost magical properties. The pattern of their firing corresponds to a location in the environment, and so, amazingly, an animal’s location can actually be reconstructed just by the firing rate of place cells. This means that scientists can track the neural activity of the rat and, based on this information alone, accurately infer where the rat is in physical space in real time. Studies have shown that once a place cell encodes space, a process that seems to happen within a couple of minutes of a novel experience, it can retain the same firing pattern for months, indicating a role in spatial memory. Place cells have been recorded when a rat is sleeping and seem to fire in similar patterns to the rat’s prior experience, and it has been hypothesized that sleep might be involved in consolidating memories of the spaces the rat has recently explored. These cells are also capable of remapping themselves, meaning different patterns of the same cells will fire when a rat is placed in a different environment.

  Almost immediately after discovering place cells, O’Keefe was struck by the idea that they seemed to prove a little-known theory that had been proposed over thirty years earlier, long before advances in technology allowed scientists to record individual neuron activity. “In thinking about these results over the next day,” wrote O’Keefe about his discovery, “I was assailed by a montage of ideas about the potential significance of this finding: the first was that it might mean that the hippocampus was the neural site of [Edward] Tolman’s cognitive map, a vague hypothetical construct that he had used to explain some aspects of rodent maze behavior but which had never gained much acceptance in the animal learning field and which was little discussed in the 1960s.” O’Keefe experienced a “prolonged euphoria of the classical Archimedean type”: maybe he had found the cognitive map.

  * * *

  The word labyrinth comes from the Greek labyris, meaning “double ax,” a symbol for the Minoan goddess of Crete. It was King Minos who asked Daedalus to design a labyrinth so complex it could imprison the Minotaur, which was later killed by Theseus, who followed Ariadne’s thread to find his way out. The word maze likely had an original meaning of “to be lost in thought,” and in Middle English it meant to confuse, puzzle, or dream. Using rats in mazes to glean insights into behavior and spatial cognition is a tradition over a century old. In the 1890s a young psychology student in Chicago observed how the rats at his father’s farm made runways under the porch of an old cabin to their nests; when the runways were revealed, they looked just like a labyrinth. Maybe psychologists could use labyrinths to find out more about what they called the rats’ home-finding abilities and test their memory and learning?

  One of the student’s colleagues was the experimental psychologist Willard Small, who, inspired by these conversations, became the first person to design a maze for rats. For inspiration he used the famous hedgerow labyrinth, a trapezoidal maze full of twists and dead ends, created at London’s Hampton Court in the late seventeenth century. He put wire mesh on a six- by eight-foot platform and gave it six culs-de-sac. Then he meticulously detailed each and every step the rats took to explore it and marveled when several blind rats found their way as easily as the others. Experiments like Small’s became increasingly popular, so much so that in 1937 Edward Tolman addressed a conference of his colleagues and said, “Everything important in psychology … can b
e investigated in essence through the continued experimental and theoretical analysis of the determinants of rat behavior at a choice-point in a maze.”

  The typical experiment in Tolman’s time was to withhold food from the animal and put the rat at the entrance of a labyrinth that had several blind turns and a food box at the end of the correct path. The researchers would time how long it took the animal to find the food and then test the rat again and again every twenty-four hours. Eventually, every rat would learn where the blind turns were and would follow the most direct route through the maze straight to the food. But sometimes the rats in these experiments would do things the psychologists couldn’t explain. In 1929, one scientist reported that his rat learned a maze and then instead of running through it again to get a reward, pushed off the cover of its starting box and ran across its top, beelining for the food and bypassing the whole experiment. This behavior prompted similar questions to those asked by Felix Santschi, who studied Tunisia’s desert ants. How could rats infer spatial relationships that allowed them to take shortcuts? The popular scientific explanation was that all animal behaviors, including those demonstrated by rats in mazes, were the result of stimulus-response. Rats see, smell, and hear stimuli from the environment and process these through sense organs, which transmit signals to muscles. Learning to turn left or right through a maze was the result of this behavioral conditioning.

  Tolman, a graduate of the Massachusetts Institute of Technology, was one of the first psychologists to doubt that theory. He called its adherents the “telephone switchboard school” for their mechanistic reductionism. Tolman thought that rats had brains capable of learning routes and building representations of the environment. Rather than thinking of them as mechanized automatons with inputs and outputs, Tolman described the rat’s mind as containing a “cognitive-like map of the environment.” He specified that this cognitive map wasn’t just a strip map of the particular paths that led to the food but a comprehensive map that included the location of food and the surrounding space, enabling rats to find novel routes. The idea of a cognitive representation of space was a radically different explanation for rat navigation. And Tolman went so far as to argue that the same mechanism was at work in humans; his classic paper on the subject, published in 1948 in Psychological Review, was called “Cognitive Maps in Rats and Men.”

  At the end of the paper Tolman elucidated an argument that he called “brief, cavalier, and dogmatic.” Was it possible, he wrote, that many people’s social maladjustments could be interpreted as the result of having too narrow and limited cognitive maps? In one example, Tolman wrote about the tendency for individuals to focus their aggression on outside groups. Poor southern whites, he wrote, displace their frustration with landlords, the economy, and northerners onto black Americans. Americans as a whole displace their aggression onto Russians and vice versa. He wrote,

  My only answer is to preach again the virtues of reason—of, that is, broad cognitive maps.… Only then can these children learn to look before and after, learn to see that there are often round-about and safer paths to their quite proper goals—learn that is, to realize that the well-beings of White and of Negro, of Catholic and of Protestant, of Christian and of Jew, of American and of Russian (and even of males and females) are mutually interdependent. We dare not let ourselves or others become so over-emotional, so hungry, so ill-clad, so over-motivated that only narrow strip-maps will be developed.

  For decades after Tolman first wrote about it, the cognitive map remained an obscure concept, and few psychologists, let alone animal behaviorists, were interested in it. Tolman himself probably never guessed that such maps might have a neural basis, the product of a cognitive mapping system located in a specific place in the brain. Sadly, he passed away in 1959, long before O’Keefe began recording place cells in the rat hippocampus.

  * * *

  Before moving to London, O’Keefe had studied at McGill University’s psychology department in Montreal, a mecca at the time for physiological psychology, and became friends with another graduate student, Lynn Nadel. Both were New Yorkers—O’Keefe was born in Harlem, and Nadel was born in Queens—and both had studied with the psychologist Don Hebb, who encouraged his students to theorize about the neural basis of cognition and test their ideas. O’Keefe and Nadel stayed friends even after leaving Montreal. Nadel went to Prague to do a postdoctoral fellowship, and when the Soviet Union invaded Czechoslovakia in 1968, he drove his wife and kids across Europe to O’Keefe’s home in London. Nadel shared O’Keefe’s interest in the hippocampus, and he joined University College London to collaborate with O’Keefe on his research into the cognitive map.

  Initially they set out to write a single paper proposing the hippocampus as the source of Tolman’s cognitive map. The paper grew to hundreds of pages long. Along the way they realized that in order to refute the standard theory of animal learning as stimulus-response, they would have to master the theory first. Eventually they sent their research to fifty different colleagues to solicit feedback, and six years later, instead of a paper, they had a book, one that would end up influencing the trajectory of the next forty years of neuroscience. Called The Hippocampus as a Cognitive Map, it was published in 1978 and dedicated to both Tolman, “who first dreamed of cognitive maps in rats and men,” and Hebb, “who taught us to look for those maps in the brain.”

  * * *

  O’Keefe and Nadel’s tome begins with a most basic assertion—that space is one of the most important forces shaping the human mind.

  Space plays a role in all our behavior. We live in it, move through it, explore it, defend it. We find it easy enough to point to bits of it: the room, the mantle of the heavens, the gap between two fingers, the place left behind when the piano finally gets moved. Yet, beyond this ostensive identification we find it extraordinarily difficult to come to grips with space.… Is space simply a container, or receptacle, for the objects of the sensible world? Could these objects exist without space? Conversely, could space exist without objects? Is there really a void between two objects, or would closer inspection reveal tiny particles of air or other matter?… Is space a feature of the physical universe, or is it a convenient figment of our mind? If the latter, how did it get there? Do we construct it from spaceless sensations or are we born with it? Of what use is it?

  They believed that the purpose of the hippocampus was to process and construct models of the physical universe in which we exist. This was a controversial claim. The field of cognitive neuroscience treated many learning processes as diffused throughout several interconnected systems. Now Nadel and O’Keefe were claiming that when it came to the spatial mapping system, the physiology of a single circuit deep in the medial temporal lobe had evolved specifically to create and store spatial representations. But why did the “Constructor of Brains,” as they jokingly referred to the mind’s creator, require that spatial mapping occur in one specialized part of the brain?

  The reason, they argued, was that space itself is special. Whereas color, motion, and other properties of objects in the physical universe can be taken away, so to speak, space has a unique status: it is an “ineliminable property of our experience of the world.” The first fifty pages of The Hippocampus as a Cognitive Map is a survey of theories of space throughout Western philosophy. The authors jump from Isaac Newton to Gottfried Leibniz to George Berkeley to Immanuel Kant, pointing out that these philosophers and many other physicists and mathematicians fall into one of two camps: either they conceived of physical space in absolute terms or in relative terms. An absolute view of space, espoused by Newton in the seventeenth century, is that it is a fixed framework—a container, so to speak—in which objects exist. In contrast, the relative view of space is that it is made up of the relationships among objects and can’t exist independently of those relationships. Berkeley, Leibniz, and David Hume went so far as to argue that our minds can’t even access the physical world—because they questioned the physical world’s very existence. To them,
space was manufactured by the human mind. Over his lifetime, Kant swung between these arguments before eventually publishing the Critique of Pure Reason in 1787 in which he argued that space was absolute, but only because the mind was innately equipped to organize it that way. Or as O’Keefe and Nadel put it, “Space was a way of perceiving, not a thing to be perceived.” For the two neuroscientists working centuries later, Kant’s ideas were not only inspiring; they felt that they had discovered the neural basis for his philosophical model of an a priori spatial faculty.

  In their book, O’Keefe and Nadel argued that both an absolute and relative understanding of space were important for humans. The Constructor of Brains had “hedged his bets and incorporated both systems into his invention.” An organism experiences space in relationship to itself (egocentric), but the brain is also capable of what they called “nonegocentric cognition,” or allocentric perspective, an ability to objectively represent the environment in three-dimensional space. This is the cognitive map in the hippocampus.

  Nadel and O’Keefe based their theory on several hundred studies from “lesion literature,” in which animals and in some cases humans with damage to their hippocampi were tested on tasks to try and understand what aspect of cognition was affected. When researchers took away the part of the brain responsible for organizing space, the consequences were devastating. For example, in 1975 O’Keefe and Nadel and several of their students took thirty-two male rats and gave sixteen of them lesions by cutting open their skulls and crushing their fornix—the nerve fibers that act as an output from the hippocampus—with jeweler’s forceps. All of the rats were then kept from water until they were thirsty, and tested repeatedly on how quickly they could find water in a room. The location of the water never changed, but those rats that had the lesions were incapable of remembering where it was or the route to get there, and thus of doing what is called place-learning. The animals searched for water each time as though it was the first time they were taking the test; they had lost their cognitive mapping capability. These studies were the scaffolding for Nadel and O’Keefe’s hypothesis regarding the key function of the hippocampus. The hippocampus’s cells, they argued, encode space in an allocentric (nonegocentric) framework, the map. Then the animal uses that map for navigation, computing the distance and direction between landmarks, orienting itself and inferring spatial relationships.