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, Ueli RUTISHAUSER*

*Corresponding author for this work

Research output: Journal PublicationsJournal Article (refereed)peer-review

111 Citations (Scopus)

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.

Original languageEnglish
Article number14821
JournalNature Communications
Volume8
DOIs
Publication statusPublished - 21 Apr 2017
Externally publishedYes

Bibliographical note

We thank all patients for their participation and Farshad Moradi for providing the morphing algorithm.

Funding

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.

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