Nothing to fear but fear itself

Late one night, a woman strolls through an urban park, and a belligerent man yells at her to come to the bench where he is sitting. The woman casually walks over to the man, who puts a knife to her throat. In a gentle voice she tells him, "If you're going to kill me, you're gonna have to go through my God's angels first." The man is so freaked out by this statement and the women's calm demeanor that he immediately lets her go. The next day, she takes another solitary walk through the park, as if nothing had happened.1 The woman described above, who is still alive today, is a famous case study in the neuroscience of human emotion. If you didn't know any better, little about her would strike you as odd - extremely outgoing and somewhat coquettish, but certainly not pathological. In fact, professional psychologists naive to her case don't seem to notice much about her that is strange. After speaking to her about her life and experiences, which include many personal hardships, they describe her as being a "survivor" with "exceptional coping skills." After learning that this woman is patient S.M., the same psychologists reinterpret their assessments of the woman: she is now said to display, "an abnormally low level of negative emotional phenomenology".2

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Patient S.M. represents one of several fascinating case studies in neuroscience (not unlike the famous patient H.M.). Individuals such as S.M. have very specific brain abnormalities that make them invaluable to neuroscientists. In the case of S.M., a rare genetic disorder known as Urbach–Wiethe disease led to complete destruction of the amygdala on both sides of her brain (Figure 1). Even more unusual was the fact that she did not sustain damage to neighboring brain structures, giving researchers a chance to assess what specific roles the human amygdala might play in generating emotional experience.

In a classic study, "Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala"3, Adolphs et al. conducted one of the earliest neuroscientific assessments of S.M. Simply put, S.M. displays deficits in the ability to discern people's emotional state from their facial expressions. Most of us don't even notice how acute this ability normally is because it is so effortless. S.M. has a pronounced inability to recognize fear in facial expressions as well trouble recognizing multiple emotions in a single facial expression. This deficit also extends to stimuli other than faces (see below), but she doesn't seem to suffer from any perceptual (sensory) deficits. Her ability to recognize the personal identity of a face remains intact, for example.

The amygdala has been extensively studied for its role in regulating emotion, especially fear and fear conditioning, in both rats and primates. Rare patients like S.M. complement animal studies because she displays fully intact cognitive capabilities, and can verbally report the quality of her emotional experiences. She does not report feeling fearful in contexts that most people do: when watching horror films, encountering creepy animals, or recounting previous traumatic experiences.

Despite the amygdala's well-known role in fear and fear learning, we know from animal studies that this is not all that the amygdala does. It also plays a crucial role in reward processing and reinforcement4. Many researchers view the amygdala, especially the basolateral amygdala, as playing a critical role in assigning and updating the value of external stimuli, both good and bad. This view may help explain S.M.'s peculiar behavior, such as the unusual calm she displayed when held at knifepoint in the park. In this situation, most people would have an intense experience of fear. Moreover, we would display a strong aversion to that park in the future. The amygdala may play a crucial role in attaching negative value to such a context, leading us to avoid it forever after. S.M. lacks this ability, and had no problem casually strolling into the same context the following day.

Neuroscientists often talk about "brain states." These can be thought of, roughly, as different global patterns of activity that occur under different physiological circumstances. The quality of these patterns constrains the types of behaviors we will tend to display. Classic examples of different brain states are those we see across sleep-wake cycles, as measured by EEG. We might be able to think in similar terms about different emotional states. The amygdala may be a key brain area involved in generating such states, taking sensory information about the external world (e.g. an emotional expression or scary context) and using past experiences to attach a positive or negative value to that sensory information. In the case of a fear-generating stimulus, the amygdala would take the "negative value" that it has learned to attach to that stimulus, and use it to trigger the appropriate set of physiological changes, including changes to the composition of our hormonal milieu (i.e. "fight-or-flight" response). These systemic changes may result in larger-scale changes in neural activity patterns that can then be interpreted by the brain as a "fear state," prompting us to behave accordingly. In the case of S.M., however, no such state is triggered, and she does not experience fear.

To echo president Roosevelt's famous quote, we may quite literally have nothing to fear but fear itself.

References

1. Sohn, E. The No-Fear Woman (And What Her Brain Reveals). (2010)

2. Tranel, D., et al. Altered experience of emotion following bilateral amygdala damage. Cogn Neuropsychiatry. 11(3):219-32 (2006).

3. Adolphs, R., et al. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature. 372(6507):669-72 (1994).

4. Murray, EA. The amygdala, reward and emotion. Trends Cogn Sci. 11(11):489-97 (2007).