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Authors: Dean Buonomano

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BOOK: Brain Buys
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In this analogy, each window is a neuron that could be “on” (firing action potentials) or “off” (silent). The key for this system to work is that the pattern must be reproducible. Why would a network of neurons fire in a reproducible pattern again and again? Because that is precisely what networks of neurons do well! The behavior of a neuron is largely determined by what the neurons that connect to it were doing a moment before, and what those neurons were doing is in turn determined by what other neurons did two moments ago.
33
In this fashion, given the same initial pattern of neural activity, the entire sequence of patterns is generated time and time again. A number of studies have recorded from an individual neuron or groups of neurons while animals were performing a specific task and the results show that, in principle, these neurons could be used to tell time over the course of seconds.
34

A related notion is that a network of active neurons changes in time as a result of the interaction between incoming stimuli and the
internal state
of the network. Let’s return to the pond analogy. If we drop the same pebble into a placid pond over and over again, a similar dynamic pattern of ripples will be observed each time. But if a second pebble is dropped in at the same point shortly after the first one, a different pattern of ripples emerges. The pattern produced by the second pebble is a result of the interaction with the state (the amplitude, number, and spacing of the little waves) of the pond when it was thrown in. By looking at pictures of the pattern of ripples when the second pebble was thrown in we could determine the interval between when the pebbles were dropped. A critical aspect of this scenario is that time is encoded in a “nonlinear” fashion, and thus does not play by normal clock rules. There are no ticks that allow for a convenient linear measure of time in which four ticks means that twice as much time as two ticks has elapsed. Rather, like the interacting ripples on the pond the brain encodes time in complex patterns of neural activity. The fact remains, however, that we will have to await future advances before we understand how the brain tells time in the range of milliseconds and seconds.

Neurons initially evolved to allow simple creatures to detect possible food sources and move toward them, and to detect potential hazards and move away from them. While these actions took place in time, they did not require organisms to tell time. So neurons in their primordial form were not designed to tell time. But as the evolutionary arms race progressed, the ability to react at the appropriate time—predict
when
other creatures will be
where
, anticipate upcoming events, and eventually communicate using signals that change in time—provided an invaluable selective advantage. Little by little, different adaptations and strategies emerged that allowed networks of neurons to time events ranging from less than a millisecond to hours. However, as with all of evolution’s designs, the ability to tell time evolved in a haphazard manner; many features were simply absent or added on later as a hack. Consider the circadian clock. Over the 3 billion years that some sort of creature has inhabited the earth, it is unlikely any one of them ever traveled halfway across the planet in a matter of hours—until the twentieth century. There was never any evolutionary pressure to build a circadian clock in a manner that allowed it to be rapidly reset. The consequence of this is jet lag. As any cross-continental traveler knows, sleep patterns and general mental well-being are impaired for a few days after a trip from the United States to Japan; unlike the watches on our wrist, our internal circadian clock cannot be reset on command.

 

As a consequence of evolution’s inherently unsystematic design process, we have an amalgam of different biological time-keeping devices, each specialized for a given time scale. The diverse and distinct strategies that the brain uses to tell time allow humans and animals to get many jobs done, including the ability to understand speech and Morse code, determine if the red light is taking suspiciously long to change to green, or anticipate that a boring lecture must be about to wrap up. The strategies the brain uses to tell time also lead to a number of brain bugs, including the subjective contraction and dilation of time, illusions that can invert the actual order of sensory stimuli, mental blind spots caused by built-in assumptions about the appropriate delay between cause and effect, and difficulties in appropriately weighing the trade-off between the short- and long-term consequences of our actions. This last bug is by far the one that has the most dramatic impact on our lives.

One could also argue that the financial crisis that started in 2008 was closely tied to the same brain bug. To an extent, the financial collapse was triggered by the inability of some homebuyers to make their mortgage payments. Some of these mortgages were interest-only loans designed to exploit our short-term biases—they postpone the need to make substantial mortgage payments. The short-term reward of home ownership, at the expense of unsustainable and progressively increasing mortgage payments, proved too alluring for many.

At the governmental level short-sighted economic decisions have plagued states and nations. Governments have often engaged in reckless borrowing while simultaneously refusing to increase taxes in a myopic effort to avoid short-term budget-tightening cuts and bruises. The long-term consequences of such policies have at best burdened future generations and at worse translated into economic collapse.

In the modern world, a long, content, and healthy life is best achieved by long-term planning on the scale of decades. The ability of modern humans to plan for the future is what allows us to best ensure education, shelter, and well-being for ourselves and our loved ones. This skill set relies on the latest evolutionary updates to the nervous system. Specifically, the progressive expansion of the frontal cortex and its ability to not only conceive of abstract concepts, such as past and future, but, in some instances, inhibit the more primitive brain structures that are more focused on short-term rewards. But planning for the future is not innate. It does not simply require the appropriate hardware; it relies on language, culture, education, and practice. Although early humans had the neural hardware, it is unlikely they had the language to help conceptualize long periods of time, the means to measure and quantify the number of elapsed months and years, or the inclination to engage in long-term plans.
35

Some scientists believe that the ability to suppress the sway of immediate gratification serves as an indicator of a number of positive personality traits. In the well-known “marshmallow experiment” originally performed in the late sixties, the psychologist Walter Mischel and colleagues placed a plate with a marshmallow (or another treat) in front of four-year-old children and made an offer: The researcher needed to leave the room but would return shortly. If the child could wait until the researcher returned before eating the marshmallow (or resist ringing a bell to summon the researcher), the child would get to eat two marshmallows. On average the marshmallow remained intact for around 3 minutes, but some children ate it immediately while others waited the full 15 minutes for the researcher to return. In the eighties the researchers decided to track down the participants in the study to see how their lives were unfolding. It turned out that there was a correlation (albeit a weak one) between how long the four-year-olds held out and their SAT scores over a decade later. Further studies have since revealed correlations between the ability to delay gratification and performance on other cognitive tasks.
36
Conversely, some studies have correlated impulsivity with drug addiction or being overweight.
37

In a world in which life was short and governed by the unpredictability of disease, the availability of food, and weather, there may have been little advantage in tackling the strenuous complexities that arise from long-term planning. But in the modern world, the opposite is true: the biggest threats to human beings are often those that arise from the lack of long-term thinking. Yet, as a consequence of our evolutionarily inherited present bias, we tend to make short-sighted decisions that influence not only our health and financial decisions but also encourage us to elect officials who promise short-term “solutions” aimed at exploiting our shortsightedness rather than actually solving problems. A component of the normal development from childhood to adulthood is precisely to learn to consider and adopt farsighted strategies—to wait for the extra marshmallow. But for the most part, even in adults, this is a skill that benefits from practice and education, and is best achieved by conscious awareness of how the disproportionate sway of short-term gratification affects our allegedly rational decisions.

5
Fear Factor

Fear is the foundation of most governments; but it is so sordid and brutal a passion, and renders men in whose breasts it predominates so stupid and miserable, that Americans will not be likely to approve of any political institution which is founded on it.

—John Adams, 1776

And for America, there will be no going back to the era before September the 11th, 2001, to false comfort in a dangerous world.

—George W. Bush, 2003

Fear, in its many guises, exerts enormous sway on our personal lives and on society as a whole. Fear of flying not only influences whether people choose to travel, but prompts some to turn down jobs that require boarding airplanes. Fear of crime may determine where we decide to live and whether to buy a gun, and in some places whether to stop at traffic lights. Fear of sharks prevents some people from going into the ocean. Fear of dentists or medical tests can prevent people from attending to important health problems. And fear of those unlike ourselves is often the seed of discrimination, and sometimes an accomplice to war. But do our fears faithfully reflect the things that are most likely to cause us harm?

In the 10-year period between 1995 and 2005 roughly 400 people in the United States died as a result of being struck by lightning. Within this same period around 3200 died as a result of terrorism, and 7000 died as a result of weather-related fatalities (hurricanes, floods, tornadoes, and lightning).
1
These numbers are all well below the approximately 180,000 murders, which are less than the 300,000 suicides or 450,000 automobile fatalities. All of these numbers are in turn dwarfed by the approximately 1,000,000 smoking-related deaths over those 10 years or the 6,000,000 deaths associated with heart disease.
2

These numbers lead one to suspect that there is only a casual relationship between what we fear and what actually kills us. It is safe to say that many Americans fear homicide and terrorism more than car accidents and heart disease.
3
Yet in terms of fatalities these dangers are barely comparable. Why are deaths attributable to homicide and terrorism more fear-inducing, and more deserving of airtime on the local news, than those caused by heart disease and car accidents? One reason could be that something like terrorism is unpredictable, arbitrary, and blind to the age of its victims. By comparison we all know of the risk factors associated with heart disease, and that heart problems are more likely to take the life of a 70-year-old than a 20-year-old. But automobile accidents are also quite unpredictable and blind to demographics, so this theory doesn’t seem to hold. Another possibility is that our disproportionate fear of homicide and terrorism is related to control. Terrorism, by design, is totally beyond the control of its victims; whereas we have some control over whether we are involved in a car accident. There is likely some truth to this rationale, as it is well established that lack of control is an important factor in modulating stress and anxiety.
4
Nevertheless, a passenger airline being brought down by terrorists is inherently more fear-inducing and anger-provoking than when a plane crashes as a result of mechanical failure—even though mechanical failure is arguably even further outside the passengers’ control. Although there are probably a number of reasons why homicide and acts of terrorism induce more fear than car accidents and heart disease, I suspect the main one is that we are hardwired to fear acts of aggression perpetrated by other humans more than most other modern dangers.

Fear is evolution’s way of ensuring that animals exhibit proactive responses to life-threatening dangers, including predators, poisonous animals, and enemies. The adaptive value of fear is obvious: a good rule of thumb in perpetuating the species is to stay alive long enough to get around to doing some perpetuating. Our evolutionary baggage encourages us to fear certain things because they comprised a reasonable assessment of what was harmful to our ancestors millions of years ago. But how appropriate are the prehistoric whispers of our genes in the modern world? Not very. As has been pointed out by many, including the neuroscientist Joe LeDoux, “since our environment is very different from the one in which early humans lived, our genetic preparation to learn about ancestral dangers can get us into trouble, as when it causes us to develop fears of things that are not particularly dangerous in our world.”
5

The cognitive psychologist Steven Pinker has pointed out, “The best evidence that fears are adaptations and not just bugs in the nervous system is that animals that evolve on islands without predators lose their fear and are sitting ducks for any invader.”
6
Indeed, species that have managed to colonize uninhabited volcanic islands (generally birds and reptiles) found themselves in paradise because the predators (often terrestrial mammals) lacked transport to the island. Because these founder species evolved over hundreds of thousands or millions of years in the absence of much predation they “lost” the fear and skittishness that is so easily observable in their continental counterparts. Darwin casually commented on the lack of fear in the birds and reptiles he encountered on the Galapagos Islands, and how easy they were to capture and kill: “A gun is here almost superfluous; for with the muzzle of one I pushed a hawk off the branch of a tree.”
7
The loss of fear was likely adaptive because the individuals that did not obsess with every noise around them were able to better focus on their feeding and reproducing endeavors. The downside was that when rodents, cats, dogs, and humans finally made it to these islands, the fearless inhabitants were as close to a fast-food restaurant as nature provides. Lack of fear was a major factor in the extinction of many species, including the dodo birds of Mauritania in the seventeenth century.

Fear in and of itself is certainly not a bug, at least not when expressed in the context in which it was originally programmed into the nervous system. But as with computers, what is correct and useful in one context can become a bug in a different context.
8
The fear module of our neural operating system is so egregiously out of date that it is the cause of misplaced fears, anxieties, and quirky phobias. And the most significant consequence of our fear-related brain bugs is that they underlie our susceptibility to fearmongering.

HARDWIRED AND LEARNED FEAR

There is so much to fear and so little time. How does the brain decide what we should and should not fear? In many cases the answer is that what we fear is encoded in our genes. Innate fears may be an especially fruitful strategy for animals at the bottom of the food chain because learning, by definition, requires experience, and the experience of being eaten is not conducive to trial-and-error learning.

Rats fear cats, gazelles fear lions, and rabbits fear foxes. In these and many other cases the prey’s fear of the predator is at least partly genetically transmitted.
9
The fact that some animals innately fear others was first demonstrated in the 1940s by the ethnologists Konrad Lorenz and Niko Tinbergen. They showed that defensive behaviors in baby geese, such as crouching and running, could be elicited by the profile of a hawk (actually a wooden cutout) flying overhead, even though the baby geese had never seen a hawk. The geese were not merely reacting to any moving object flying overhead, but discriminating the shape of the moving object. A cutout that had a short head and a long tail, much like a hawk, caused the goslings to react more fearfully than a cutout that had a long neck and short tail, much like a fellow goose.
10
These results are rather astonishing, not simply because they imply that fear of an object flying overhead is innate, but because they imply that the shape of the object is somehow encoded in genes and then translated into networks of neurons. In essence, the genetic code has written down “run from moving objects that exhibit two lateral protrusions and in which the ‘head’ to ‘tail’ ratio is small.” Innate, or
phylogenetic,
memories are encoded in DNA, but DNA does not detect objects flying overhead or make animals run. Vision and escape behaviors rely on neurons. In the same manner that the code a computer programmer writes must be compiled into a set of instructions a computer can “understand,” genetically encoded information must somehow be compiled into neural hardware. While neuroscientists have some understanding of how networks of neurons in the visual system can discriminate shapes, how fear-inducing stimuli are genetically encoded and then implemented in neural networks remains a mystery.

The fact that evolution has programmed animals to fear certain stimuli (e.g., the smell or appearance of their predators) is not surprising. What is surprising is that some creatures appear to have evolved the ability to manipulate the fear circuits of other animals. Specifically, some parasites have the rather spooky ability to change the behavior of their hosts to better suit their own agendas. Rabies is one example. Dogs with rabies secrete an abundance of saliva that contains a virus eager to infect its next host. If infected dogs simply lay in a corner all day the chances of this happening would be very low. But if they become aggressive enough to go around biting other animals, the chances of the virus making it into the bloodstream of potential hosts are increased. Like a body snatcher, the lowly rabies virus appears to manipulate the behavior of dogs to suit its own needs. Another example of
neuroparasitism
is provided by the single-cell organism
Toxoplasma gondii
. This protozoan can only reproduce in cats (their
definitive hosts
), but their life cycle requires a stage in one of their
intermediary hosts
, which include rats. Once in a rat
Toxoplasma
form cysts, which need to make their way from inside the rat to a cat. While this has been known to occur naturally, of course, the parasite seems to play the role of an evil matchmaker by mucking with the fear circuits of rats, thus increasing the likelihood the cysts will make if from the rat to the stomach of a cat.
11

Genetically encoding what an animal should fear is a priceless evolutionary adaptation. But it is also a very inflexible strategy because it can only be reprogrammed on a slow evolutionary timescale; when a new predator emerges (as may happen when new animals arrive on an island), it might take thousands of generations to update the fear circuits. Endowing animals with the ability to learn during their lifetimes what they should fear provides a more powerful approach, opening entirely new strategies for avoiding predators: they can learn which sounds and smells precede the appearance of predators, or the locations where predators are more likely to be hanging out.

As most people who have been bitten by a dog know, humans can easily learn what to fear. Virtually all mammals seem to share this ability, which in its simplest form is termed
fear conditioning
. In a laboratory setting, fear conditioning can be studied in humans by delivering a brief shock to the forearm of volunteers shortly after the presentation of a preselected image (the positively conditioned stimulus or CS+). The notion is that people will learn to “fear” the stimulus that predicted the shock. These threatening stimuli elicit an assortment of so-called autonomic responses—physiological changes that take place automatically and unconsciously, and include increased heart rate, pupil dilation, piloerection (goose bumps), and sweating. The latter can be quantified by
skin conductance
, which measures the electrical resistance between two points on the skin (this is the same measure a polygraph uses). Indeed, an increased skin conductance response to a conditioned stimulus, such as the image of a yellow triangle, is observed after it has been paired with a shock.
12

Mice and rats can also be conditioned to fear a neutral stimulus. Rodents often respond to a threatening stimulus, such as a cat, by remaining immobile, a behavior referred to as
freezing
(a reaction humans have also been known to express in frightening situations). Immobility makes sense if the visual systems of your most common predators are highly tuned to movement. A mouse normally does not freeze in response to a harmless auditory tone; however, if this tone is consistently paired with an aversive stimulus, such as an electrical shock, it learns to fear the tone. Next time the mouse hears the tone it “freezes” even though no shock is presented.

Fear conditioning is among the most robust forms of learning in many animals. Humans and rodents alike can be conditioned to fear particular sounds, images, smells, or places. These learning experiences can last a lifetime for some people, and contribute to phobias such as fear of dogs or of driving a car.
13

THE NEURAL BASIS OF FEAR

For neuroscientists, emotions are rather frustrating. They are hard to define and measure, and they are inextricably intertwined with the biggest mystery of all: consciousness. Nevertheless, compared to other emotions, we are considerably less ignorant about the neuroscience of fear. This may be because fear is such a primitive emotion—perhaps the primordial emotion. Fear seems to rely heavily on evolutionarily older brain structures and, as opposed to more veiled emotions such as love and hate, animals express a well-defined repertoire of fear-related behaviors and autonomic responses. Together, these two factors have greatly facilitated the challenge of unveiling the neural basis of fear.

The amygdala, one of the evolutionarily older structures of the brain that contributes to processing emotion, is of fundamental importance for the expression and learning of fear.
14
Experiments in the 1930s revealed that damage to the temporal lobes, which contain the amygdala, made monkeys very tame, fearless, and emotionally flat. In humans, electrical activation of the amygdala can elicit feelings of fear, and imaging studies demonstrate that there is increased activity in the amygdala in response to fear-provoking stimuli, such as threatening faces or snakes. Additionally, patients with damage to both the left and right amygdala have difficulty recognizing fear in the faces of other people.
15
(Although the amygdala is critically involved in fear, it is important to note that it also contributes to other emotions and is activated by emotionally charged stimuli in general, including images of sex or violence.)

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