Wednesday, December 22, 2010

Fearful Emotions and the Brain

Recent research from the University of Iowa substantiates the important role the the amygdala serves in the perception of fear. But questions regarding the role of the amygdala in the expression of emotions have persisted. A recent study provides an answer.

For decades, investigators have been trying to identify how the brain encodes and decodes environmental and social stimuli related to various emotions (e.g., disgust, happiness, anger, sadness, surprise).  In the process they have debated whether or not there are just a few fundamental emotions from which all emotions may be derived, much like the manner in which primary colors may be combined with black to create a range of colors and hues, and if so, what might these basic emotion be.  Investigators have also sought to determine if such basic emotions are cultural universals.

One of the emotions that has been considered fundamental is the emotion of fear. Does the cover from the journal Nature above to the right appear to be an image that conveys fear?

An MRI of SM's brain.  The two arrows
indicate the damage to the amygdala
that exists in both hemispheres.
Ralph Adophs who is currently at Cal Tech has been investigating such questions for several decades and was among the first to publish findings from an exceptional case study -- a woman known as SM, with a rare condition called Urbach-Wiethe Disease.  SM has a specific impairment in the ability to process and perceive fearful stimuli. The primary region of the brain that is damaged by this disease is the amygdala.  

I first read about SM. during the mid 1990s, in a brief description of her that appeared in Nature in [Hamman et al., 1996].  Since then, studies with SM as well as other individuals with damage to the amygdala and studies in non-human primates and rodents have confirmed that the amygdala plays a prominent role in the perception of fear [e.g., LeDoux, 1994].

For example, in the cover article above, investigators confirmed that S.M. had great difficulty accurately perceiving  facial expressions of fear, but had no difficulty correctly identifying expressions associated with other emotions such as sadness [Adolphs et a., 2005].  When they compared the eye-movements of SM with those of controls, they found that unlike the controls, SM. did not fixate on the eyes. Apparently, the eyes, rather than the mouth or other facial  features, convey important aspects of facial expressions that help individuals identify expressions of fear. Just why SM is less likely to utilize these aspects of facial expressions is not clear, nor is it clear that this is a cause of her impairments of the result of them.  The investigators found that explicit instructions to focus on the eyes improved SM's ability to identify expressions of fear.  Subsequent work found that SM did not attend to eyes during conversations with people (Spezio et al., 2007).  It is intriguing that individuals with disabilities along the autism spectrum also tend not to attend to faces, particularly to the eyes [Pelphrey et al., 2002).

Students interested in assessing eye movements can do so using the Eye Gaze System we have in the Psychology Department here at Washington College 

But till now I've been unable to provide a satisfactory answer to a common question that I get from students when we discuss the case of SM and other individuals with similar impairments:  
  • Is SM unable to experience fear or is her impairment limited to identifying pictures of individuals whose expression clearly indicate fear to healthy control subjects?
  • The most recent research indicates that SM has a significant impairment in the ability to experience fear as well as in perceiving facial expressions most people regard as fearful. 

This latest research appears in the journal Current Biology  [Feinstein et al, 2010; doi:10.1016/j.cub.2010.11.042 ] What the investigators learned is that SM also fails to experience fear in situations that would normally be sufficient to elicit such emotion in most individuals. For example, even in situations in which her life had been threatened, her subjective report was that she felt little fear. In the laboratory, she also did not appear as fearful as healthy individuals when exposed to objects that normally elicit fear [see the Scienceblog: The woman who knows no fear].  

Some caution should be considered when interpreting the implications of this latest study:

  • This is a case study, and as with all case studies the findings may apply to the individual case but may not be representative of healthy individuals.  For example, there may be multiple regions of the brain that are normally involved in the perception and experience of fear.  Selective damage to these may also produce similar deficits to those exhibited by SM.
  • Other brain structures besides the amygdala are damaged in SM.  Cortical regions adjacent to the amygdala are also damaged. It may be that the combined injury is required to experience deficits in both the perception and expression of fear.
  • Visceral fear may not be the only emotion that involves processing by the amygdala.  Earlier research with SM indicated that she also has difficulty judging the trustworthiness of individuals based upon facial characteristics that others employ to arrive as such social assessments [Adolphs et al. 1998].

Cited Sources

Adolphs, R. et al. (1998) Nature, 395, 470-474.
Adolphs, R. et al., (2005). Nature, 433, 68-72.
Feinstein, J. S., et al. (2010)Curr. Biol. DOI: 10.1016/j.cub.2010.11.042
Hamman et al. (1996) Nature, 379, 497.
LeDoux, J.E. (June, 1994). Scientific American, 50-57.
Pelphrey K.A.  (2002) J Autism Dev Disord 32, 249 –261.
Spezio, M.L. et al. (2007). The Journal of Neuroscience, 27, 3994-3997.


  1. I can't tell, since I can't access the article - do you know if they ever looked for signs of physiological fear response, or did they just assess her subjective perception of fear?

  2. Meaghan asks a good question. From what I've read, the study did not assess any autonomic physiological indicators to determine if they may have occurred even in the absence of the subjective experience of fear.

    Previous studies of patients with unilateral or bilateral lesions of the amygdala (and adjacent damage) have found that they have impairments in conditioned (learned) autonomic responses of fear. For example Weike et al (2005) found that patients showed a diminished skin conductance response following pairings between images of neutral facial expressions (Conditioned Stimuli; CS) and electrical shock (Unconditioned Stimuli; UCS). Notably there had been no difference between the skin conductance response of patients and controls to the UCS; so patients exhibited a "normal" autonomic response to the aversive UCS.

    Such impairment in acquisition of a learned autonomic fear response could be because the patients do not attend to the salient elements of the CS (i.e., the eye) whereas the healthy controls do attend to these features. I wonder what the result may have been if CS other than faces had been employed.

    There may be an interesting and important dissociation between systems that mediate autonomic responses to inherently fearful stimuli and our learned fears.

    It is possible that damage to the amygdala results in impairments that are limited to learned autonomic responses - that patients would still exhibit strong autonomic response to inherently fearful stimuli and contexts (e.g., sudden unanticipated free-fall) even in the absence of subjective experience of fear. To my knowledge, no such experiment has been conducted. Someone who reads this may know better and contribute a description of that study.

    Even if SM's autonomic response to inherently fearful events/stimuli is un-impaired, it seems she has limited access to these, or may misinterpret them as an alternative emotion (e.g., anger, perhaps even happiness/amusement).

    Cited Sources
    Weike et al. (2005) Journal of Neuroscience, 25, 11117-11124