Amygdala lesions do not compromise the cortical network for false-belief reasoning

The amygdala plays an integral role in human social cognition and behavior, with clear links to emotion recognition, trust judgments, anthropomorphization, and psychiatric disorders ranging from social phobia to autism. A central feature of human social cognition is a theory-of-mind (ToM) that enabl...

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Main Authors: Spunt, Robert P., Elison, Jed T., Dufour, Nicholas, Adolphs, Ralph, Hurlemann, Rene, Saxe, Rebecca R.
Other Authors: Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Format: Article
Language:en_US
Published: National Academy of Sciences (U.S.) 2015
Online Access:http://hdl.handle.net/1721.1/99119
https://orcid.org/0000-0003-2377-1791
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author Spunt, Robert P.
Elison, Jed T.
Dufour, Nicholas
Adolphs, Ralph
Hurlemann, Rene
Saxe, Rebecca R.
author2 Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
author_facet Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Spunt, Robert P.
Elison, Jed T.
Dufour, Nicholas
Adolphs, Ralph
Hurlemann, Rene
Saxe, Rebecca R.
author_sort Spunt, Robert P.
collection MIT
description The amygdala plays an integral role in human social cognition and behavior, with clear links to emotion recognition, trust judgments, anthropomorphization, and psychiatric disorders ranging from social phobia to autism. A central feature of human social cognition is a theory-of-mind (ToM) that enables the representation other people's mental states as distinct from one's own. Numerous neuroimaging studies of the best studied use of ToM—false-belief reasoning—suggest that it relies on a specific cortical network; moreover, the amygdala is structurally and functionally connected with many components of this cortical network. It remains unknown whether the cortical implementation of any form of ToM depends on amygdala function. Here we investigated this question directly by conducting functional MRI on two patients with rare bilateral amygdala lesions while they performed a neuroimaging protocol standardized for measuring cortical activity associated with false-belief reasoning. We compared patient responses with those of two healthy comparison groups that included 480 adults. Based on both univariate and multivariate comparisons, neither patient showed any evidence of atypical cortical activity or any evidence of atypical behavioral performance; moreover, this pattern of typical cortical and behavioral response was replicated for both patients in a follow-up session. These findings argue that the amygdala is not necessary for the cortical implementation of ToM in adulthood and suggest a reevaluation of the role of the amygdala and its cortical interactions in human social cognition.
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spelling mit-1721.1/991192022-10-02T03:04:11Z Amygdala lesions do not compromise the cortical network for false-belief reasoning Spunt, Robert P. Elison, Jed T. Dufour, Nicholas Adolphs, Ralph Hurlemann, Rene Saxe, Rebecca R. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Dufour, Nicholas Saxe, Rebecca R. The amygdala plays an integral role in human social cognition and behavior, with clear links to emotion recognition, trust judgments, anthropomorphization, and psychiatric disorders ranging from social phobia to autism. A central feature of human social cognition is a theory-of-mind (ToM) that enables the representation other people's mental states as distinct from one's own. Numerous neuroimaging studies of the best studied use of ToM—false-belief reasoning—suggest that it relies on a specific cortical network; moreover, the amygdala is structurally and functionally connected with many components of this cortical network. It remains unknown whether the cortical implementation of any form of ToM depends on amygdala function. Here we investigated this question directly by conducting functional MRI on two patients with rare bilateral amygdala lesions while they performed a neuroimaging protocol standardized for measuring cortical activity associated with false-belief reasoning. We compared patient responses with those of two healthy comparison groups that included 480 adults. Based on both univariate and multivariate comparisons, neither patient showed any evidence of atypical cortical activity or any evidence of atypical behavioral performance; moreover, this pattern of typical cortical and behavioral response was replicated for both patients in a follow-up session. These findings argue that the amygdala is not necessary for the cortical implementation of ToM in adulthood and suggest a reevaluation of the role of the amygdala and its cortical interactions in human social cognition. Della Martin Foundation National Institute of Mental Health (U.S.) David & Lucile Packard Foundation Simons Foundation 2015-10-01T12:54:23Z 2015-10-01T12:54:23Z 2015-04 2014-12 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/99119 Spunt, Robert P., Jed T. Elison, Nicholas Dufour, Rene Hurlemann, Rebecca Saxe, and Ralph Adolphs. “Amygdala Lesions Do Not Compromise the Cortical Network for False-Belief Reasoning.” Proc Natl Acad Sci USA 112, no. 15 (March 30, 2015): 4827–4832. https://orcid.org/0000-0003-2377-1791 en_US http://dx.doi.org/10.1073/pnas.1422679112 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) National Academy of Sciences (U.S.)
spellingShingle Spunt, Robert P.
Elison, Jed T.
Dufour, Nicholas
Adolphs, Ralph
Hurlemann, Rene
Saxe, Rebecca R.
Amygdala lesions do not compromise the cortical network for false-belief reasoning
title Amygdala lesions do not compromise the cortical network for false-belief reasoning
title_full Amygdala lesions do not compromise the cortical network for false-belief reasoning
title_fullStr Amygdala lesions do not compromise the cortical network for false-belief reasoning
title_full_unstemmed Amygdala lesions do not compromise the cortical network for false-belief reasoning
title_short Amygdala lesions do not compromise the cortical network for false-belief reasoning
title_sort amygdala lesions do not compromise the cortical network for false belief reasoning
url http://hdl.handle.net/1721.1/99119
https://orcid.org/0000-0003-2377-1791
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