The woman who knows no fear

A 44-year-old woman with a rare form of brain damage can literally feel no fear, according to a case study published yesterday in the journal Current Biology. Referred to as S.M., she suffers from a genetic condition called Urbach-Wiethe Disease. The condition is extremely rare, with fewer than 300 reported cases since it was first described in 1929, and is caused by a mutation in a gene on chromosome 1, which encodes an extracellular matrix protein. The symptoms vary widely, and in about 50% of cases there is calcification, or hardening, of structures in the medial temporal lobe of the brain. In S.M.’s case, it led to degeneration of the amygdala (below), a small, almond-shaped structure known to be involved in fear and other emotions.

S.M. has been studied extensively during the past two decades. Early investigations showed that her non-verbal visual memory was signficantly impaired but that otherwise she had an IQ in the low-average range. She also displayed inappropriate social behaviours, quickly becoming friendly with the experimenters and making sexual remarks, due to disturbed executive control. Subsequently, it was found that she was unable to recognize emotions in facial expressions, and a study published earlier this year showed that the brain damage had eliminated her monetary loss aversion – that is, she makes risky financial decisions that most of us would avoid because of a fear of losing money.

None of these previous studies assessed her experience of fear, however. Justin Feinstein of the University of Iowa and his colleagues therefore tested S.M.’s fear responses, using a very simple method – by trying to scare her. First, they took her to an exotic pet store and exposed her to snakes and spiders, which, she had told them, she “hated” and “tried to avoid”. Nevertheless, she seemed fascinated by the large collection of snakes, and was compelled to touch and poke the larger and more dangerous ones, as well as a tarantula, but had to be stopped in case she got bitten. Throughout the visit, she was asked to rate her fear on a scale of 0 to 10, and her ratings were never greater than 2.

Next, the researchers took S.M. on a Halloween visit to Waverly Hills Sanatorium in Louisville, Kentucky, which features people dressed as monsters, murderers and ghosts and is reported to be “one of the most haunted places in the world”. When they arrived, she voluntarily led the researchers and a goup of five strange women around the house, walking into dark corners and hallways without hesitation. The hidden monsters tried to scare her numerous times, unsuccessfully. Whereas the five other women in the group screamed loudly whenever they encountered one, S.M. laughed and smiled at them, and even scared one by poking it in the head because she was curious about how it felt. She rated her fear level at 0 throughout, saying instead that she found it exciting.

Finally, they showed her scenes from scary movies, such as The RingThe Blair Witch Project and The Shining, interspersed with clips that induce disgust, anger, surprise, and happiness. She laughed at a collage of scenes showing babies and small children doing funny things, was disgusted by a scene from Pink Flamingos in which a cross-dresser eats dog faeces, and expressed anger at a scene from Cry Freedom in which a group of children are shot and killed by soldiers. But she did not express fear at any point while watching the horror movie scenes – she told the researchers that she found them exciting, and even asked for the title of one of the movies so she could rent and watch it.

S.M. reports having experienced fear as a young child. She recalls being afraid of the dark, and remembers when her older brother jumped out from behind a tree while she walked through a cemetary, making her run away screaming and crying. She also appears to understand the concept of fear. She uses words such as afraidterrorpanic and frightened appropriately during conversations, and can recognize the emotion in other peoples’ voices.

But based on interviews with her and her three children, the authors suggest that she probably has not experienced fear at all throughout the whole duration of her adult life, despite having encountered an unusually high number of traumatic and life-threatening events. Aged 30, she had a knife held to her throat by a drug addict while she walked through a park at night, but did not panic and walked away calmly when he let her go. She has also been held at gun point, was nearly killed in an act of domestic violence, and has been the victim of numerous crimes in the poverty-stricken area in which she lives.

S.M. therefore seems unable to detect threats in her environment and, as a result, does not actively avoid potentially dangerous situations as most of us would. Feinstein and his colleagues argue that this is because the amygdala is essential in triggering a state of fear. The amygdala is but one component of a network of brain structures that normally generate an appropriate fear response, but in its absence this response cannot be mounted, so that the experience of fear is severely diminished. The researchers further suggest that she may be immune to the effects of post-traumatic stress disorder, and that interventions which target the amygdala could therefore be beneficial for sufferers of the condition.

Although earlier studies have provided some evidence of altered fear responses in patients with amygdala damage, this is the first to systematically test the experience of fear in a patient lacking both amygdalae. It has its limitations, however. As the authors point out, S.M.’s brain damage is not limited to the amygdala, so her lack of fear could be due to a combination of damage to this structure, adjacent structures such as the entorhinal cortex and connecting white matter. Furthermore, this is a case study involving a single patient, so it will be important to verify the findings in others with comparable damage.

Reference:

Feinstein, J. S., et al. (2010). The Human Amygdala and the Induction and Experience of Fear.Curr. Biol. DOI: 10.1016/j.cub.2010.11.042.