Patient SM

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Chapter 1 endnote 33, from How Emotions are Made: The Secret Life of the Brain by Lisa Feldman Barrett.
Some context is:

But then, a funny thing happened. Scientists found that SM could see fear in body postures and hear fear in voices. [,..] SM also had difficulty seeing fear in scenes only when they contained faces; see Adolphs and Tranel 2003. SM’s difficulties have other explanations not related to fear.

Much of our understanding of the neural basis of fear comes from studying Patient SM.  For an interesting description of her life and struggles, see Feinstein et. al (2016).[1]

Perceiving fear

SM has difficulty seeing fear in a very specific situation: when she is asked to overtly identify a face that's portraying a stereotyped fear expression (i.e., a facial configuration for fear used in the basic emotion method).[2] In laboratory experiments where she was presented with posed facial configurations and asked to explicitly identify them, SM didn’t look at the eyes in the photographs. This is significant because in fear poses, the eyes are distinctively wide, showing lots of sclera (the white of the eye),[3] and neurons in the amygdala are particularly sensitive to sclera.[4] When SM was directed to pay attention to the eyes, she could explicitly identify stereotyped fear faces as effectively as neurotypical subjects could.[3] Scientists also found that SM had difficulty identifying facial configurations of surprise, which also show lots of sclera.[5]

Additionally, SM improved when she was put under time pressure. She could pick out a face posing a stereotyped fear pose in an array of happy, sad, and calm faces when instructed to do it rapidly. Also, when shown two basic emotion configurations for an extremely short time (about 40 milliseconds), she could identify the one showing more fear, anger, or threat.[6] So, SM could clearly identify fearful configurations under some circumstances, even without her amygdalae. Interestingly, other patients who have amygdalae damaged by Urbach-Wiethe disease show no changes in fear-related behavior (such as Patient AM, discussed in chapter 1), or they spend a longer time looking at the widened eyes of stereotyped fear poses and have no difficulty correctly categorizing those faces as fearful.[7][8][9]

SM is able to perceive fear in bodies posed to look fearful, and in vocalizations that depict fear (e.g., screams).[10][11] She is able to identify threatening scenes except when they contain posed fear faces.[12] In her everyday life, SM is able to perceive fear in friends—for example, she ventures out during a storm to help a scared friend in need and calls the police for others in danger.[1]

Experiencing fear

As discussed in chapter 1, SM has difficulty in experiencing fear in many typical circumstances (e.g., horror movies, haunted houses). But she experiences fear in many other circumstances, particularly when the feeling is intense. She experiences fear when asked to breathe air with higher concentrations of CO2 (and she continues to experience fear after repeated exposure to CO2 even when neurotypical subjects habituate somewhat). SM avoids breaking the law for fear of getting in trouble. And she is able “learn fear” in the real world; for example, she is averse to seeking medical treatment or visiting the dentist because of intense pain she experienced on a previous occasions.[1]

Interestingly, SM spontaneously reports feeling worried, but she does not use the word "fear" to describe her experiences. The average person in the U.S. avoids breaking the law or going to the dentist out of fear, so it is easy to infer that SM would also be feeling fear. With this observation in mind, it may be important to consider that SM has had difficulties sustaining long-term relationships with people in her life, a fact that is distressing to her. There is one clear exception to this rule, however: SM has sustained a relationship with the scientists who have studied her for almost two decades. SM relies on them—she calls them for support (e.g., when she is worried or afraid, such as when did not want to return to the doctor for painful medical treatment), and they help her with the details of daily life (financial and otherwise).[1] It would be interesting to examine whether SM is aware of their hypothesis that the amygdala contains the circuitry for fear.

Notes on SM's brain

It should be noted (but rarely is) that SM’s brain shows abnormalities that extend beyond the amygdala, including the anterior entorhinal cortex and ventromedial prefrontal cortex, both of which show dense, reciprocal connections to the amygdala and very likely play a role in SM’s specific behavioral profile.[13][14]

Notes on the Notes

  1. 1.0 1.1 1.2 1.3 Feinstein, Justin S., Ralph Adolphs, and Daniel Tranel. 2016. "A tale of survival from the world of Patient S.M." In Living Without an Amygdala, edited by David G. Amaral & Ralph Adolphs, 1-38. New York: Guilford.
  2. Adolphs, Ralph, Daniel Tranel, Hanna Damasio, and Antonio Damasio. 1994. "Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala." Nature 372 (6507): 470-474.
  3. 3.0 3.1 Adolphs, Ralph, Frederic Gosselin, Tony W. Buchanan, Daniel Tranel, Philippe Schyns, and Antonio R. Damasio. 2005. "A mechanism for impaired fear recognition after amygdala damage." Nature 433 (7021): 68-72.
  4. Whalen, Paul J., Jerome Kagan, Robert G. Cook, F. Caroline Davis, Hackjin Kim, Sara Polis, Donald G. McLaren et al. 2004. "Human amygdala responsivity to masked fearful eye whites." Science 306 (5704): 2061.
  5. Adolphs, Ralph, James A. Russell, and Daniel Tranel. 1999. "A role for the human amygdala in recognizing emotional arousal from unpleasant stimuli." Psychological Science 10 (2): 167-171.    
  6. Tsuchiya, Naotsugu, Farshad Moradi, Csilla Felsen, Madoka Yamazaki, and Ralph Adolphs. 2009. "Intact rapid detection of fearful faces in the absence of the amygdala." Nature neuroscience 12 (10): 1224–1225.
  7. Terburg, David, B. E. Morgan, E. R. Montoya, I. T. Hooge, H. B. Thornton, A. R. Hariri, J. Panksepp, D. J. Stein, and J. Van Honk. 2012. "Hypervigilance for fear after basolateral amygdala damage in humans." Translational Psychiatry 2 (5): e115.
  8. See also: De Gelder, Beatrice, David Terburg, Barak Morgan, Ruud Hortensius, Dan J. Stein, and Jack van Honk. 2014. "The role of human basolateral amygdala in ambiguous social threat perception." Cortex 52: 28-34.
  9. See also Van Honk, J., D. Terburg, H. Thornton, D. J. Stein, and B. Morgan. "Consequences of selective bilateral lesions to the basolateral amygdala in humans." In Living Without an Amygdala, edited by David G. Amaral & Ralph Adolphs, {{{pages}}}. New York: Guilford.
  10. Adolphs, Ralph, and Daniel Tranel. 1999. "Intact recognition of emotional prosody following amygdala damage." Neuropsychologia 37 (11): 1285-1292.
  11. Atkinson, Anthony P., Andrea S. Heberlein, and Ralph Adolphs. 2007. "Spared ability to recognise fear from static and moving whole-body cues following bilateral amygdala damage." Neuropsychologia 45 (12): 2772-2782.
  12. Adolphs, Ralph, and Daniel Tranel. 2003. "Amygdala damage impairs emotion recognition from scenes only when they contain facial expressions." Neuropsychologia 41 (10): 1281-1289.
  13. Boes, Aaron D., Sonya Mehta, David Rudrauf, Ellen Van Der Plas, Thomas Grabowski, Ralph Adolphs, and Peg Nopoulos. 2012. "Changes in cortical morphology resulting from long-term amygdala damage." Social cognitive and affective neuroscience 7 (5): 588-595.    
  14. Hampton, Alan N., Ralph Adolphs, J. Michael Tyszka, and John P. O'Doherty. 2007. "Contributions of the amygdala to reward expectancy and choice signals in human prefrontal cortex." Neuron 55 (4): 545-555.