Fear is an innate emotion that is triggered by environmental stimuli perceived as potentially threatening or harmful. This emotion is so basic to human existence that its expression on a human face can be accurately recognized by anyone in the world. Thus, fear is a highly evolved, universal emotion whose existence is critical to survival.

Fear has long been thought to arise due to activity of cells in the amygdala, an almond-shaped brain structure located in the medial temporal lobe. In 1939, Heinrich Klüver and Paul Bucy reported that surgical removal of both temporal lobes (including the amygdalae) in monkeys produced a dramatic behavioral condition now referred to as the Klüver-Bucy syndrome. After surgery, the monkeys, who previously feared humans, no longer showed such fear. They also showed a number of other behavioral changes, including hyperorality (a compulsion to examine objects by mouth), hypersexuality (excessive sexual behavior), hypermetamorphosis (excessive tendency to react to visual stimuli), and visual agnosia (inability to recognize familiar objects). The exact role of the amygdala in human fear, however, has not been fully established (perhaps) until now.

For over two decades, researchers at the University of Iowa have been studying an extraordinary woman known only as patient SM, who acquired damage to both amygdalae (due to a rare congenital genetic condition known as Urbach-Wiethe disease). The researchers sought to examine the induction and experience of fear in SM (now a 44-year old woman) in a variety of experimental settings. Specifically, the researchers exposed SM to live snakes and spiders, took her on a tour of a haunted house, and showed her clips from several scary movies (including The Ring, Halloween, Seven, and Silence of the Lambs). SM provided her written consent to participate and the researchers took great pains to only expose SM to situations capable of inducing fear with little risk of direct harm. Additional studies were conducted utilizing self-report questionnaires (over a period of three years) and experience sampling (over three months). In experience sampling studies, SM provided input to a computerized emotional diary, in which she rated her current emotional state utilizing a set of 50 randomly presented emotional terms. The emotional terms included a wide range of both positive and negative emotional states and were derived from the Positive and Negative Affect Schedule – Expanded Form (PANAS-X).

In a study published in the January 11, 2011 issue of Current Biology, the researchers report that SM did not show fear in any of the aforementioned scenarios. When taken to an exotic pet store, SM voluntarily held a large snake for three minutes even though she has often said that she “hates” them and “tries to avoid them.” She seemed fascinated with the snake and said, “this is so cool!” while holding it. SM asked the store employee 15 times if she could also hold a larger, more dangerous snake, but this was not allowed to avoid the possibility of her being harmed. SM also attempted to touch a tarantula but was stopped so that she would not be bitten. When asked why she would want to touch a dangerous snake in spite of claiming to hate snakes, SM indicated that she was overcome with “curiosity.” When taken to a Halloween haunted house at the Waverly Hills Sanatorium in Louisville, Kentucky (ranked as “one of the most haunted places in the world”), SM voluntarily led a group of five strangers through the haunted house and showed no signs of fear or hesitation. “This way guys, follow me!” she repeatedly exclaimed. Ironically, SM scared one of the monsters by poking it in the head because she was “curious.” When asked about her experience at the haunted house, SM likened it to the excitement felt while riding a roller coaster — an activity she claims to enjoy. When shown a set of 10 different fear-inducing film clips, SM showed no behavior indicative of fear. She found the fear-inducing films to be exciting and, in one case, asked the name of the movie so that she could rent it later that day. Interestingly, SM commented that most people would fear the content of the films even though she did not. Importantly, SM was also shown a number of other film clips intended to evoke disgust, anger, happiness, and surprise and, in each case, reported experiencing high levels of the respective emotions during the films. It is also worth noting that, over the past two decades, SM has consistently performed in the normal range in terms of IQ, memory, language, and perception.

In support of these behavioral observations, SM scored consistently below normal on eight well-validated self-report questionnaires intended to evaluate the level of fear a person may experience in a variety of scenarios (such as public speaking or dying). In addition, in studies of experience sampling, SM’s PANAS-X score was at the lowest possible level. SM consistently rated feeling the lowest possible levels of the following: “afraid,” “scared,” “fearful,” “nervous,” “guilty,” and “ashamed.” She also reported feeling the highest average rating for “fearless.” Importantly, for all basic emotions other than fear, SM reported experiencing them on numerous occasions to varying degrees — from “a little” to “quite a bit.”

Despite SM’s apparent deficit, she does understand what fear is and reports having felt fear on multiple occasions before the age of 10 — likely around the time that her congenital condition resulted in amygdala damage. During adulthood, SM had multiple experiences that may be considered traumatic (such as being held up at knife point and gun point and being nearly killed in an act of domestic violence) to which she responded with a marked lack of fear or urgency. It is clear that SM’s impaired ability to detect dangerous situations likely contributes greatly to her high incidence of life-threatening experiences. Regardless, SM appears unaware of her deficit and is unable to elaborate about why she is being studied (other than to indicate that the researchers studying her want to understand how her brain damage affects her behavior).

Several limitations of this study limit the conclusions that can be drawn from its findings. First, brain imaging indicates that SM’s brain damage is not entirely limited to the amydgalae and extends into nearby brain regions. Second, this study provides only preliminary evidence about whether SM’s experience of emotions other than fear is in the normal range. Third, SM is a single case and, ideally, these findings should be replicated in other similar cases.

In sum, these findings indicate that patient SM exhibits a significant deficit in the ability to experience fear across a wide variety of situations. As SM is capable of experiencing other emotions normally, she is not emotionless, but rather fearless. This case study, when coupled with data acquired in amydgala-damaged animals, indicates that the amygdala is critical for triggering the experience of fear. As indicated by the authors, SM’s unique case suggests that, without the amygdala, the evolutionary value of fear is lost.

SM’s amygdala damage appears to render her immune to the effects of post-traumatic stress disorder (PTSD), an intriguing hypothesis that is supported by results from recent studies in amygdala-damaged war veterans. “This finding points us to a specific brain area that might underlie PTSD,” said senior study author Daniel Tranel, Ph.D., Director of University of Iowa’s Interdisciplinary Graduate Program in Neuroscience. “Psychotherapy and medications are the current treatment options for PTSD and could be refined and further developed with the aim of targeting the amygdala,” said Dr. Tranel.

References

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Elfenbein HA, & Ambady N (2002). On the universality and cultural specificity of emotion recognition: a meta-analysis. Psychological bulletin, 128 (2), 203-35 PMID: 11931516

Feinstein JS, Adolphs R, Damasio A, & Tranel D (2011). The human amygdala and the induction and experience of fear. Current biology : CB, 21 (1), 34-8 PMID: 21167712

Klüver H, and Bucy PC. (1939). Preliminary analysis of functions of the temporal lobe in monkeys. Archives of Neurology & Psychiatry 42: 979-1000.

Koenigs M, Huey ED, Raymont V, Cheon B, Solomon J, Wassermann EM, & Grafman J (2008). Focal brain damage protects against post-traumatic stress disorder in combat veterans. Nature neuroscience, 11 (2), 232-7 PMID: 18157125