Experiment Module: Identifying the Brain Structures Involved in Conditioned Fear

Conditioned fear is a phenomenon that can be easily induced in the laboratory and that has been used to determine what neural circuits are involved in fear behaviours.

Conditioned fear is the process by which a stimulus with no particular significance becomes, by association, a sign of imminent danger. For example, if your neighbour’s dog has already bitten you once, you are probably going to be afraid whenever you have to go into your neighbour’s yard. For you, your neighbour’s trees and buildings have simply become associated with the painful bite of his dog.

In the laboratory, the most common conditioned-fear experiments involve placing a rat in a cage where small electrical shocks can be administered to the rat’s feet through the floor. The researchers place the rat in the cage, subject it to a particular sound, then immediately administer a slight shock to its feet. After only a few repetitions of this procedure, the rat associates the sound with the shock and becomes afraid when it simply hears the sound. For the rat, the neutral stimulus of the sound has become a conditioned fear.

Not only can conditioned fear be induced very quickly, but it has the added advantage of lasting a very long time. It thus represents a very strong association that is unlikely to be forgotten and that scientists can test without worrying about how long ago it was learned.

Another characteristic of conditioned fear is that scientists have been able to induce it in just about any species, ranging from flies and molluscs to fish and monkeys. Conditioned fear thus seems to have been preserved by evolution and to play a fundamental role in the survival of species.

But the two most interesting things about conditioned fear are: (1) that the sensory system through which the conditioning is applied often is well understood and can be used as a starting point to trace the pathways involved in the brain; and (2) that the behavioural response of fear involves several well known, measurable, physiological changes, such as accelerated heart rate and elevated levels of stress hormones in the blood.

The question that researchers want to answer is, how does a new acoustic stimulus that has no particular intrinsic meaning manage to trigger a defensive behavioural response as the result of a conditioned fear? To answer this question, researchers start with two solid pieces of information. They know where this phenomenon begins (in the auditory system and its connections to the brain), and they know where it ends (with the defensive behavioural response and its physiological manifestations). All the researchers have to do is find the connections between the inputs and the outputs.

One researcher who helped to revive the scientific study of emotions through his experiments on conditioned fear was Joseph LeDoux of New York University. In a first set of experiments with laboratory rats, LeDoux investigated what parts of the auditory system were essential for establishing conditioned fear. First he made lesions in the auditory cortex of a number of rats (the part of the brain where sounds are identified). But he found that he could still induce conditioned fear in these rats.

Next, he removed the auditory thalamus (the structure just before the cortex) from the auditory systems of another set of rats. Unlike those rats whose auditory cortex had been removed, these rats could no longer acquire a conditioned fear. Lesions made in the underlying structure, the midbrain, had the same effect.

It was thus apparent that in conditioned fear, the auditory stimulus had to reach the thalamus. But where did the stimulus go after that to trigger the emotional reaction of fear? The neuroanatomy manuals of the day showed the auditory cortex as the only output pathway for the auditory thalamus.

To answer this question, LeDoux and his colleagues began injecting their animals with tracer substances that were absorbed by the neurons, thereby allowing the pathways followed by their axons to be observed and traced. Using this method, the researchers identified four subcortical regions that receive axons from the auditory thalamus.

In a series of experiments, each of these pathways was then destroyed in turn. The researchers thereby discovered that for a conditioned fear to be established, only one of these pathways was needed: the one leading to the amygdala.

The discovery of this new sub-cortical pathway explained why the lesions in the auditory cortex, though they did prevent the animals from identifying a sound precisely, did not prevent them from acquiring a conditioned fear. The neural pathway from the thalamus to the amygdala simply bypassed the cortex.

At about the same time, another researcher, Bruce Kapp, had discovered the central nucleus, a subregion of the amygdala with connections to regions of the brainstem that are involved in controlling heart rate and various responses of the vegetative nervous system.

Kapp therefore proposed that it was these brainstem regions that received the outputs from the amygdala and enabled the numerous bodily responses involved in conditioned fear. Soon afterward, a study of lesions in the central nucleus showed that Kapp’s intuition had been correct: destroying the central nucleus interfered dramatically with the behavioural response of conditioned fear.

Thus, through the experimental methods of lesion and tracing, scientists were able to identify the basic “wiring” and the main structures in the brain that were involved in conditioned fear reactions. Subsequent studies showed that the amygdala plays a central role in the emotion of fear, whatever the nature of the sensory stimulus that triggers it.

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