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Nat Commun. 2017 Apr 21;8:14821. doi: 10.1038/ncomms14821.

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

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Computation and Neural Systems, California Institute of Technology, Pasadena, California 91125, USA.
Humanities and Social Sciences, California Institute of Technology, Pasadena, California 91125, USA.
Department of Psychology, National University of Singapore, Singapore 117570, Singapore.
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, Guangzhou 510631, China.
Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125, USA.
Department of Neurosurgery, University of Iowa, Iowa City, Iowa 52242, USA.
Division of Medical Psychology, University of Bonn, Bonn 53105, Germany.
Epilepsy and Brain Mapping Program, Huntington Memorial Hospital, Pasadena, California 91105, USA.
Departments of Neurosurgery and Neurology, Cedars-Sinai Medical Center, Los Angeles, California 90048, USA.


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.

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