Figure 5.1 Fear “memory” in an amygdala neuron: A tone does not elicit a fear response in a naïve rat or many action potentials in an amygdala neuron that was being recorded from. During fear conditioning a tone is followed by a brief shock. After this learning phase the tone elicits a fear response in the rat as well as many spikes in the neuron. This new neuronal response can be thought of as a “neural memory,” or as being the neural correlate of fear learning. (Maren and Quirk, 2004; modified with permission from Macmillan Publishers LTD.)
Fear conditioning provides one more example of how the brain can write down information by changing the strengths of synapses. And once again this process is mediated by Hebbian plasticity.18 You might recall from Chapter 1 that Hebb’s rule states that if the pre- and postsynaptic neurons are simultaneously active, the synapse between them should become stronger. This is what occurs during auditory fear-conditioning. The amygdala neurons receive inputs conveying information about the painful shock used as the unconditioned stimulus, and the synapses conveying information about the shock are strong to begin with—presumably because the painful stimuli are innately capable of triggering defensive behaviors. So when an auditory tone is paired with a shock, some amygdala neurons fire because they are strongly activated by this shock. When these same neurons also receive inputs from presynaptic neurons activated by the auditory tone, these synapses are strengthened because their pre- and postsynaptic components are active at the same time. As we have seen, this Hebbian or associative synaptic plasticity is implemented by the NMDA receptors—those clever proteins that detect an association between pre- and postsynaptic activity. Indeed, blocking the NMDA receptors during fear conditioning prevents learning, but blocking these same receptors after fear conditioning does not prevent rats from freezing, indicating that the NMDA receptors are necessary for the initial learning (storage) but not the recall (readout) of the memory.19
If the synapses onto the neurons in the lateral amygdala are the neural memory, it follows that damaging these cells would erase the fear memory. Experiments by the neuroscientist Sheena Josselyn and her colleagues at the University of Toronto have shown that after selectively killing the subset of neurons that were the recipients of the potentiated synapses, mice no longer froze to the tone.20 Importantly, killing these neurons did not impair the mice’s ability to learn to fear new stimuli, indicating the memory loss was not simply produced by general amygdala dysfunction. These studies suggest that it is possible to actually delete the memory that encodes a given fear.
The identification of the brain area, the neurons, and even the synapses that appear to underlie fear conditioning has opened the door to understanding and potentially reversing some of the psychiatric problems caused by fear. A number of disorders, including anxiety, phobias, and posttraumatic stress disorder (PTSD) are produced by what amount to bugs in the fear circuits of the brain. Phobias are characterized by an exaggerated and inappropriate sense of fear to specific stimuli such as snakes, spiders, or social situations. PTSD is a disorder in which fear and anxiety can become pervasive states, triggered by thoughts or external events; for example, a soldier with PTSD may reexperience the stress of battle after hearing a firecracker. In these cases it seems that certain stimuli are overly effective in activating the fear circuits in the brain. Thus, we might wonder if it’s possible to counteract the ability of these stimuli to activate the fear circuits.
Classical conditioning can be reversed as a result of extinction. When Pavlov’s dogs were repeatedly exposed to the sound of the bell in the absence of the unconditioned stimulus, they eventually stopped salivating when they heard the bell. Extinction is an essential component of classical conditioning since the associations in our environment change with time. It is just as important to stop salivating to a bell when it is no longer predictive of anything as it is to learn the association in the first place. Fear conditioning can be extinguished when multiple presentations of the conditioned stimulus are presented in the absence of shocks, and studies of this process have led to fascinating insights into what it means to “unlearn” something. Contrary to what one might imagine, extinction does not seem to correspond to erasing the memory of the initial experience. If I create a memo on a whiteboard that says, “stop by the dry cleaner’s,” after accomplishing the task, I could either erase the memo (irretrievably deleting information about my goal of stopping by the dry cleaner’s) or I could write underneath it, “ignore the above message, mission accomplished.” In the case of fear conditioning the brain seems to take the latter approach. Extinction does not rely on decreasing the strength of the synapses that were potentiated in the lateral amygdala; rather, it relies on the formation of a new memory that essentially overrules or inhibits the expression of the older memory.21 The obvious advantage of this method is that it is likely easier to “relearn” the initial memory if necessary, allowing for an “undelete” operation.
Phobias and PTSD appear to be fairly resistant to the normal processes of extinction. But in some cases, particularly those in which not much time has elapsed since the original experience, it may be possible to truly erase the memories responsible for phobias or PTSD. We discussed the process of reconsolidation in Chapter 2: under some circumstances, each time a memory is used it becomes sensitive to erasure again—by drugs that inhibit protein synthesis or by the storage of new information—presumably because in the process of synaptic strengthening, the synapse itself becomes labile, or mutable, again.22 This reconsolidation process is thought to be valuable because it allows our memories to be updated in an ever-changing world; as the people around us age, our memories of their faces are retouched, not stored anew.
Some neuroscientists have suggested that it might be possible to take advantage of this reconsolidation process to erase traumatic memories using a two-step process. First, evoking the traumatic memories might serve to make the underlying synaptic changes labile again; second, the administration of certain drugs or continued presentation of the fear-evoking stimulus might then actually reverse synaptic plasticity and thus erase the original memory. In other words, a memory that once represented something dangerous would be “updated” to represent something neutral. Although some studies of fear conditioning suggest that this strategy might erase the original memory,23 the validity of this approach with the entrenched memories that contribute to phobias or PTSD will have to await future research.
PREPARED TO FEAR
So far, we have explored two answers to the question, How does the brain decide what it should and should not fear? In some cases fear is innate, such as a goose’s fear of a hawk. Yet, in other instances, animals learn to fear things that have been associated with threatening events, such as when a rat learns to fear a tone paired with a shock. I for one would have thought that these two explanations covered all the possible bases. Not so. Consider ophidiophobia: many species of monkeys, not unlike humans, are very fearful of snakes—a reasonable behavior since an inadvertent encounter with the wrong snake can result in serious injury or death. But how does a monkey know it is supposed to fear snakes? Is fear of snakes programmed into their genes or learned? Ever the empiricist, Charles Darwin recounts his own anecdotal experiments that illustrate the thorny nature of this question in The Descent of Man:
I took a stuffed and coiled-up snake into the monkey-house at the Zoological Gardens, and the excitement thus caused was one of the most curious spectacles which I ever beheld. Three species of Cercophithecus [a genus of African monkeys] were the most alarmed; they dashed about their cages, and uttered sharp signal cries of danger, which were understood by the other monkeys. A few young monkeys and one old Anubis baboon alone took no notice of the snake.24
It was once widely assumed that much like the geese that are innately fearful of hawks, monkeys are genetically programmed to fear snakes. The story is, however, considerably more interesting. In many monkeys the fear of snakes is not strictly innate or learned; rather, it is the propensity to learn to fe
ar snakes that is innate. Wildborn monkeys often freak out when shown a fake snake; whereas monkeys born in captivity are often much more aloof in their response, suggesting that fearfulness is learned. But monkeys seem ready and willing to jump to the conclusion that snakes are dangerous. In fact, it is quite easy to teach monkeys to fear snakes, but difficult to teach them to fear something neutral, like flowers. In studies performed by the psychologist Susan Mineka and her colleagues, rhesus monkeys raised in captivity were not any more fearful of real or toy snakes than they were of “neutral” stimuli, such as colored wooden blocks. Fear was measured by specific behaviors such as retreat from the objects, as well as by how long (if at all) it would take monkeys to reach over the object to get a treat. These same monkeys were later shown a videotape of another monkey exhibiting a fearful response to a snake, and after this short instructional video, the lab monkeys demonstrated a clear hesitancy and apparent fear both of the real and toy snakes.
One might be tempted to conclude from these experiments that fear of snakes is 100 percent learned in monkeys, but next Mineka and her colleagues studied whether the monkeys would be equally amenable to learning to fear other things. They showed monkeys videos of a demonstrator monkey reacting fearfully to snakes on some trials, and to a novel object, such as a flower, on other trials. As before these monkeys developed a fear of snakes, but they did not become afraid of flowers. These experiments have been replicated and support the assertion that while monkeys are not innately afraid of snakes, they are innately prepared to learn to fear snakes.25
Presumably this is true of humans too. Children also learn to fear by observing others; as children observe their parents’ reactions to situations, they can absorb their anxieties and fears.26 Although the issue has never been studied (there are obvious ethical concerns in studying fear in children), one would expect that children are more apt to learn to fear snakes, as compared to, say, turtles, when observing their parents’ reacting fearfully to these creatures.
XENOPHOBIA
Like our primate cousins, our innate fear predispositions are not limited to poisonous animals, potential predators, heights, or thunderstorms, but can include a built-in fear of members of our own species. This fact is demonstrated by another type of fear conditioning experiment in humans. Studies have shown that it is possible to condition humans to fear subliminal images—images that are presented so quickly that they are not consciously processed. Not surprisingly, it is easier to condition humans to fear some images over others, such as images of angry faces over happy ones. In one study, a happy or angry face was presented for a few hundredths of a second and paired with a shock. When an image is flashed for this length of time and immediately followed by a “neutral” face, people do not report seeing the happy or angry face. Nevertheless, subjects exhibited a larger skin conductance response when the shock was paired with an angry face than when it was paired with a happy face. Together with a number of other studies, these results indicate that humans are innately prepared to fear angry people.27
An innate fear of angry individuals and strangers, or a propensity to easily learn to fear them, was likely to increase one’s lifespan over most of primate evolution. Chimpanzees can be extremely unkind to strangers, as males have been known to pummel to death outsiders found in their territory. These attacks can be incredibly gruesome, and may include biting off the testicles of the victim.28 The primatologist Frans de Waal states that “there is no question chimpanzees are xenophobic.”29 Even in the artificial settings of zoos it is extremely difficult to introduce a new adult male into an established social group. There are many reasons primates and other social animals are aggressive toward outsiders, including competition for food and females. In chimps, fear of strangers is probably influenced by learning, but like other social animals, there is probably an innate preparedness for fearing outsiders. Humans are unlikely to be any different.30 An innate uneasiness and distrust of outsiders makes evolutionary sense—and is part of basic survival. It is believed that competition and aggression between neighboring groups was constant throughout human evolution, and it is obvious today in the interactions among both indigenous groups and nation-states.31 On this point Frans de Waal recounts a story:
An anthropologist once told me about two Eipo-Papuan village heads in New Guinea who were taking their first trip on a little airplane. They were not afraid to board the plane, but made a puzzling request: they wanted the side door to remain open. They were warned that it was cold up in the sky and that, since they wore nothing but their traditional penis sheaths, they would freeze. The men didn’t care. They wanted to bring along some heavy rocks, which, if the pilot would be so kind as to circle over the next village, they could shove through the open door and drop onto their enemies.32
Paradoxically, many anthropologists believe that the constant warfare between competing groups was also responsible for the evolution of cooperation and altruism.33 Altruistic behaviors, such as going to war for your village or nation, represent an evolutionary conundrum. If one gene resulted in the expression of altruism, and that gene was present in all the members of a social group, the group as a whole would prosper from this selflessness; for instance, a tribe of altruistic warriors will be more fearless and effective in battle, which in turn increases the dominance and growth of their clan. However, any individual lacking the gene will benefit from the altruism of the group without partaking in any of the cost of these behaviors (such as dying in battle). These “defectors” without the altruism gene would reproduce more, and eventually bring the whole edifice of altruism tumbling down. The argument goes that warfare kept this problem in check: groups with a high proportion of freeloaders might from time to time be wiped out by groups that benefited from having the full complement of altruists in their midst.
Regardless of whether intergroup violence played a critical role in the amplification of altruism, it is undoubtedly the case that intergroup warfare has been omnipresent throughout primate and human evolution. Thus it seems likely that a propensity to fear outsiders would remain well entrenched in our genetic code. But how do social animals know who is or is not an outsider? In chimpanzee communities of dozens of members it is likely that each individual knows every other. This is of course impossible in the large human settlements that emerged after the advent of agriculture, and even more so in modern societies. We can determine if someone is from our tribe by using a variety of genetic and cultural phenotypes: the color of people’s skin, what type of clothing they wear, whether they speak the same language or have the same accent, and so on. Unfortunately, the need to know whom to fear, combined with the use of simple traits to distinguish in-group from out-group, helped lay the foundation for the racial, religious, and geographic forms of discrimination that remain so well rooted in human behavior today.
TELE-FEAR
What we fear is the result of a three-pronged strategy devised by evolution: innate fear (nature), learned fear (nurture), and a hybrid approach in which we are genetically predisposed to learn to fear certain things. From these strategies at least two fear-related brain bugs emerge. The first is that what we are programmed to fear is hopelessly outdated, to the point of being maladaptive. The second is that by observation we involuntarily learn to fear a variety of things that are unlikely to harm us.
No matter how many times I witness someone juggle, I will never actually learn to juggle without hands-on experience. Some things simply can’t be learned by observation. Fear is not one of them. Not only can we learn to fear by observation, but vicarious learning can be as effective as firsthand experience. In a study performed by Elizabeth Phelps and Andreas Ollson at New York University, volunteers sitting in front of a computer screen were shown pictures of two different angry faces, one of which was always paired with a shock. A second group of volunteers underwent observational learning: they viewed the subjects in the first experiment receiving shocks when one of the angry faces was displayed (in reality they were viewing actors th
at pretended to jerk their arms in response to what viewers assumed was a shock). A third group was simply shown one of the angry faces and told that they would receive a shock when they saw that face. Amazingly, the magnitude of the skin conduction response to the angry face was approximately the same in all three groups.34 The vicarious experiences of shocks were as effective as actually being shocked, and this seems to hold true primarily for stimuli like angry faces that we are genetically hardwired to fear.
We have now seen examples in which both monkeys and humans learned to fear something by observation. Both the monkeys and humans were, however, totally duped. They were not actually firsthand eyewitnesses to any threatening events; they were just watching movies. Observational learning is so effective that we learn by watching videos, which may have been filmed at times and places far removed from our own reality, or that are entirely fictitious productions. Most people will never actually see a live shark, much less witness a shark attacking another human being. Yet, some people cannot avoid thoughts of sharks lurking just beyond the shoreline. Why? Because Steven Spielberg, as a result of his exceptional directorial skills, has singlehandedly created a generation of selacophobics. Like the observer monkey who developed a fear of snakes by watching a movie of another monkey acting stressed out over a toy snake, the movie Jaws triggered and amplified our innate propensity to fear large predators with big, sharp teeth. This genetically transmitted propensity to learn to fear certain things has been termed preparedness or selective association and is thought to be the explanation for why we are much more likely to develop phobias of snakes or spiders than of guns or electrical outlets.35
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