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Published April 21, 2017 | Published + Supplemental Material
Journal Article Open

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


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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© 2017 The Author(s). This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ Received 18 Jan 2016 | Accepted 6 Feb 2017 | Published 21 Apr 2017 We thank all patients for their participation and Farshad Moradi for providing the morphing algorithm. This research was supported by the Autism Science Foundation (to S.W.), the Simons Foundation (to R.A.), the Cedars-Sinai Department of Neurosurgery (to U.R.), an NSF CAREER award (1554105 to U.R.) and the NIMH Conte Center (P50MH094258 to R.A.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. Author Contributions: S.W., R.Y., R.A. and U.R. designed experiments; S.W., R.A. and U.R. wrote the paper. S.W., R.Y., J.M.T., S.Z., S.S., I.B.R., J.M.C., A.N.M. and U.R. performed research. S.W., R.Y., J.M.T., S.Z., C.K., Y.H. and U.R. analysed data. R.H. contributed two patients with amygdala lesions. All authors discussed the results and contributed toward the manuscript. The authors declare no competing financial interests.

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Supplemental Material - ncomms14821-s1.pdf

Supplemental Material - ncomms14821-s2.pdf


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