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Neurons in the human amygdala selective for perceived emotion

Wang, Shuo and Tudusciuc, Oana and Mamelak, Adam N. and Ross, Ian B. and Adolphs, Ralph and Rutishauser, Ueli (2014) Neurons in the human amygdala selective for perceived emotion. Proceedings of the National Academy of Sciences of the United States of America, 111 (30). E3110-E3119. ISSN 0027-8424. PMCID PMC4121793.

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The human amygdala plays a key role in recognizing facial emotions and neurons in the monkey and human amygdala respond to the emotional expression of faces. However, it remains unknown whether these responses are driven primarily by properties of the stimulus or by the perceptual judgments of the perceiver. We investigated these questions by recording from over 200 single neurons in the amygdalae of 7 neurosurgical patients with implanted depth electrodes. We presented degraded fear and happy faces and asked subjects to discriminate their emotion by button press. During trials where subjects responded correctly, we found neurons that distinguished fear vs. happy emotions as expressed by the displayed faces. During incorrect trials, these neurons indicated the patients’ subjective judgment. Additional analysis revealed that, on average, all neuronal responses were modulated most by increases or decreases in response to happy faces, and driven predominantly by judgments about the eye region of the face stimuli. Following the same analyses, we showed that hippocampal neurons, unlike amygdala neurons, only encoded emotions but not subjective judgment. Our results suggest that the amygdala specifically encodes the subjective judgment of emotional faces, but that it plays less of a role in simply encoding aspects of the image array. The conscious percept of the emotion shown in a face may thus arise from interactions between the amygdala and its connections within a distributed cortical network, a scheme also consistent with the long response latencies observed in human amygdala recordings.

Item Type:Article
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URLURL TypeDescription DOIArticle material CentralArticle
Wang, Shuo0000-0003-2562-0225
Mamelak, Adam N.0000-0002-4245-6431
Adolphs, Ralph0000-0002-8053-9692
Rutishauser, Ueli0000-0002-9207-7069
Additional Information:© 2014 National Academy of Sciences. Edited by Riitta Hari, Aalto University, Espoo, Finland, and approved May 28, 2014 (received for review January 7, 2014). Published ahead of print June 30, 2014. We thank all patients for their participation; Drs. Linda Philpott and William Sutherling for neurological referral and evaluation of the patients; the staff of the Huntington Memorial Hospital Epilepsy and Brain Mapping Program for excellent support with participant testing; Erin Schuman for providing some of the recording equipment; and Frederic Gosselin for advice on the bubbles method. This research was supported by grants from the Pfeiffer Family Foundation, the Simons Foundation, the Department of Neurosurgery at the Cedars-Sinai Medical Center, and the Conte Center from National Institute of Mental Health. Author contributions: R.A. and U.R. designed research; S.W., O.T., A.N.M., I.B.R., and U.R. performed research; S.W. and U.R. analyzed data; and S.W., R.A., and U.R. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at 1073/pnas.1323342111/-/DCSupplemental.
Funding AgencyGrant Number
Gustavus and Louise Pfeiffer Research FoundationUNSPECIFIED
Simons FoundationUNSPECIFIED
Cedars-Sinai Medical CenteUNSPECIFIED
National Institute of Mental Health (NIMH)UNSPECIFIED
Subject Keywords:human single unit; medial temporal lobe; limbic system; hippocampus; intracranial
Issue or Number:30
PubMed Central ID:PMC4121793
Record Number:CaltechAUTHORS:20140630-180911850
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:46582
Deposited By: George Porter
Deposited On:01 Jul 2014 14:44
Last Modified:09 Mar 2020 13:19

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