The human amygdala parametrically encodes the intensity of specific facial emotions and their categorical ambiguity

Shuo Wang (), Rongjun Yu (), J. Michael Tyszka, Shanshan Zhen, Christopher Kovach, Sai Sun, Yi Huang, Rene Hurlemann, Ian B. Ross, Jeffrey M. Chung, Adam N. Mamelak, Ralph Adolphs and Ueli Rutishauser ()
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Shuo Wang: Computation and Neural Systems, California Institute of Technology
Rongjun Yu: National University of Singapore
J. Michael Tyszka: California Institute of Technology
Shanshan Zhen: School of Psychology, Center for Studies of Psychological Application, and Key Laboratory of Mental Health and Cognitive Science of Guangdong Province, South China Normal University
Christopher Kovach: University of Iowa
Sai Sun: School of Psychology, Center for Studies of Psychological Application, and Key Laboratory of Mental Health and Cognitive Science of Guangdong Province, South China Normal University
Yi Huang: School of Psychology, Center for Studies of Psychological Application, and Key Laboratory of Mental Health and Cognitive Science of Guangdong Province, South China Normal University
Rene Hurlemann: University of Bonn
Ian B. Ross: Epilepsy and Brain Mapping Program, Huntington Memorial Hospital
Jeffrey M. Chung: Cedars-Sinai Medical Center
Adam N. Mamelak: Cedars-Sinai Medical Center
Ralph Adolphs: Computation and Neural Systems, California Institute of Technology
Ueli Rutishauser: California Institute of Technology

Nature Communications, 2017, vol. 8, issue 1, 1-13

Abstract: Abstract The human amygdala is a key structure for processing emotional facial expressions, but it remains unclear what aspects of emotion are processed. We investigated this question with three different approaches: behavioural analysis of 3 amygdala lesion patients, neuroimaging of 19 healthy adults, and single-neuron recordings in 9 neurosurgical patients. The lesion patients showed a shift in behavioural sensitivity to fear, and amygdala BOLD responses were modulated by both fear and emotion ambiguity (the uncertainty that a facial expression is categorized as fearful or happy). We found two populations of neurons, one whose response correlated with increasing degree of fear, or happiness, and a second whose response primarily decreased as a linear function of emotion ambiguity. Together, our results indicate that the human amygdala processes both the degree of emotion in facial expressions and the categorical ambiguity of the emotion shown and that these two aspects of amygdala processing can be most clearly distinguished at the level of single neurons.

Date: 2017
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DOI: 10.1038/ncomms14821

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