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

Abstract

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.

Additional Information

© 2015 National Academy of Sciences. Edited by Joseph E. LeDoux, New York University, New York, NY, and approved February 27, 2015 (received for review December 2, 2014). We thank Mike Tyszka, the California Institute of Technology Brain Imaging Center, and the Martinos Imaging Center at MIT for help with the neuroimaging. Funding support was supplied by the Della Martin Foundation, the National Institute of Mental Health, the Packard Foundation, and the Simons Foundation. Author contributions: R.P.S., J.T.E., and R.A. designed research; R.P.S., J.T.E., and R.H. performed research; R.H. and R.S. contributed new reagents/analytic tools; R.P.S. and N.D. analyzed data; and R.P.S., J.T.E., and R.A. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1422679112/-/DCSupplemental.

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