People who lack a brain structure thought to be critical for fear can still experience the emotion
The patient known as S.M. has not experienced fear since she was a child, and has fascinated brain researchers for many years. Several years ago, one team noted that she makes risky financial decisions in experimental economics games, because she isn’t afraid of losing money. Another tried everything they could to frighten the life out of her – but failed. They showed her clips from some of scariest horror films ever made, asked her to handle large spiders and snakes, and took her to haunted house. On no occasion did she show the smallest sign of fear, even when faced with traumatic events and potentially life-threatening threats.
Now in her mid-forties, S.M. is one of fewer than 300 people to be diagnosed with Urbach-Wiethe disease, a genetic condition that causes a brain structure called the amygdala to gradually harden up and shrivel away. This small, almond-shaped bundle of neurons, located deep within the brain on the inner surface of the temporal lobe, plays an important role in emotions, and is thought to be an essential component of the brain’s fear circuit. Now, though, the researchers have found something that can drive S.M. into a panic, and made her feel some kind of fear for the first time in decades: a whiff of carbon dioxide.
Inhaling carbon dioxide makes most people gasp for breath and can cause panic attacks, and this response is also thought to involve the amygdala. Justin Feinstein of the University of Iowa and his colleagues therefore reasoned that people with amygdala damage would not react in this way. To test this prediction, they asked S.M., two identical twin sisters with Urbach-Wiethe disease, and 12 healthy controls to inhale the gas through a mask. And to their surprise, the brain-damaged patients became fearful and panicky immediately after inhalation, even more so than the participants with intact brains.
S.M., for example, started to frantically wave her hand near the mask about 8 seconds after inhalation, and then screamed for help. “It felt like my throat was closing up… I couldn’t breathe,” she told the researchers in an interview afterwards. When asked how it had made her feel, she replied: “Panic, mostly, because I didn’t know what the hell was going on.” She described the feeling as the worst one she’d ever had, and expressed surprise at her reaction, because she couldn’t remember having reacted in that way ever before.
The twin sisters responded similarly. One said that she became “overwhelmed by the panic and fear of dying,” and that inhaling the gas evoked “a strong fear of suffocation,” unlike anything she had ever experienced before. The other also said she experienced panic and feared suffocation, describing the feeling she had experienced as “totally new”.
The study clearly shows that the amygdala is not needed for the fearful response to carbon dioxide, or even for sensing the gas in the first place. It seems to be far more important for responses to threats from the outside world. The stimuli signalling a threat of suffocation – an increase in blood acidity – come from inside the body instead.
“The findings don’t allow us to speak about the exact brain areas responsible for the patients’ preserved experience of fear,” says Feinstein, “but we are in the process of examining this further using functional neuroimaging.” He suspects that parts of the brainstem, which controls breathing and other involuntary behaviours, and the insular cortex, which is involved in bodily awareness, may play an important role in generating the response.
“This is a novel and important paper,” says Joseph LeDoux of New York University. “It adds to a growing body of work showing that there are different systems for responses to different kinds of threats. The mechanisms that produce reactions to threats are different from those that generate fearful feelings. There is lots of evidence that the amygdala contributes to fear responses, but very little evidence that it generates the conscious experience of fear.”
“Fear” is a highly subjective experience that’s hard to describe, and we cannot know exactly how the three brain-damaged patients experienced it. Indeed, LeDoux argues that using words such as “fear” and “pleasure” to describe our feelings is problematic, and that it’s time to rethink the emotional brain. Rather than being functions of the brain with their own pathways, fear and pleasure should be thought of as the end results of a system of survival circuits that together regulate functions such as arousal and motivation to meet our basic needs. These survival circuits are present in other animals, and what we call “emotions” may be our interpretation of the accompanying changes in physiology and behaviour.
Reference: Feinstein, J.S., et al. (2013). Fear and panic in humans with bilateral amygdala damage. Nature Neurosci., doi: 10.1038/nn.3323
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