Highlights
Summary
Although clinical observations suggest that humans with amygdala damage have abnormal fear reactions and a reduced experience of fear, these impressions have not been systematically investigated. To address this gap, we conducted a new study in a rare human patient, SM, who has focal bilateral amygdala lesions. To provoke fear in SM, we exposed her to live snakes and spiders, took her on a tour of a haunted house, and showed her emotionally evocative films. On no occasion did SM exhibit fear and she never endorsed feeling more than minimal levels of fear.
Likewise, across a large battery of self-report questionnaires, three months of real-life experience sampling, and a life history replete with traumatic events, SM repeatedly demonstrated an absence of overt fear manifestations and an overall impoverished experience of fear. Despite her lack of fear, SM is able to exhibit other basic emotions and experience the respective feelings. The findings support the conclusion that the human amygdala plays a pivotal role in triggering a state of fear, and that the absence of such a state precludes the experience of fear itself.
Results and Discussion
The amygdala is involved in multiple aspects of fear processing, ranging from fear conditioning to the modulation of attention and memory for fear-related stimuli all the way to fear recognition and the induction of fear-related behaviors.
Much less is known about the amygdala’s role in the conscious experience of fear, in large part because non-human animals with amygdala lesions are unable to verbally report on their internal subjective experience and humans with focal bilateral amygdala damage are extremely difficult to find. An exception is patient SM, a 44-year-old woman who is one of the best characterized human cases with bilateral amygdala damage. SM’s neuropsychological profile has been stable for the past two decades. She performs within the normal range on standardized tests of IQ, memory, language and perception, yet is severely impaired in fear conditioning, in recognizing fear in facial expressions, and in aspects of social behavior thought to be mediated by emotions related to fear.
Importantly, none of the previous studies specifically assessed the induction and experience of fear in patient SM, and it is these two aspects of fear which form the basis for the current report. We define fear induction as the exposure to stimuli capable of triggering a state of fear. The success of an induction was measured by the presence of overt behavioral manifestations of fear1, especially signs of avoidance behavior or withdrawal in response to fear-provoking stimuli. Fear experience, on the other hand, is the subjective feeling of fear, and was measured by SM’s self-report of her internal experience. We predicted that without the amygdala, the action sequence that constitutes a state of fear would fail to be induced in SM, thereby preempting her experience of fear.
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