Amygdala experiments of Paul Whalen

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Chapter 1 endnote 42, from How Emotions are Made: The Secret Life of the Brain by Lisa Feldman Barrett.
Some context is:

Since the wide-eyed, fearful facial configurations of the basic emotion method occur rarely in everyday life, they are novel when test subjects view them in brain-imaging experiments. These findings, and others like them, provide an alternative explanation for the original experiments that don’t require the amygdala to be the brain locus of fear.

Various brain imaging experiments led people to assume that the amygdala was important for fear. One of the earliest and most important of those experiments, however, was later called into question by the original scientist. In 1998, the neuroscientist Paul Whalen demonstrated that fearful faces, presented extremely rapidly, were associated with an increase in neural firing within the amygdala even though subjects did not consciously register the fearful faces. Each trial of the experiment showed a fearful face immediately followed by neutral face, preventing subjects from consciously seeing the fearful faces. (This technique is called “backward masking.” When two stimuli are presented in rapid succession, the second stimulus is supposed to interrupt the brain’s processing of the first.) This was considered definitive evidence that the amygdala was the brain locus of fear, because amygdala neurons were responsive to fear faces, even when subjects had no awareness of seeing them.[1]

Twelve years later, however, Whalen wondered: what if you presented a fearful face rapidly, but followed it with something other than a neutral face? If the amygdala is necessary for fear, then you should observe the same effect, no matter what the fearful faces were masked with. Whalen ran an experiment where subjects were presented with fearful faces, followed by scrambled images of the same face. This time, there was no increase in amygdala response.[2] This meant — in his original experiment as well — that the amygdala was not responding to the fearful faces per se, but instead responding to the pair of images (fear face + mask). Once again, evidence for the amygdala as the home of fear had dissolved with a closer look.

We now know that in the first experiment, the brain merged the fearful and neutral faces, and the amygdala responded to the novelty of this merged image. This phenomenon is called stimulus integration or amalgamation. In Whalen’s later experiment, the brain merged a fearful face and a scrambled face, and the amygdala did not respond to this unrealistic image.

Notes on the Notes

  1. Whalen, Paul J., Scott L. Rauch, Nancy L. Etcoff, Sean C. McInerney, Michael B. Lee, and Michael A. Jenike. 1998. "Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge." Journal of Neuroscience 18 (1): 411-418.
  2. Kim, M. Justin, Rebecca A. Loucks, Maital Neta, F. Caroline Davis, Jonathan A. Oler, Emily C. Mazzulla, and Paul J. Whalen. 2010. "Behind the Mask: The Influence of Mask-Type on Amygdala Response to Fearful Faces." Social Cognitive and Affective Neuroscience, 5 (4): 363-368.