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Right mesial temporal lobe epilepsy impairs empathy-related brain responses to dynamic fearful faces

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Abstract

Unilateral mesial temporal lobe epilepsy (MTLE) has been associated with reduced amygdala responsiveness to fearful faces. However, the effect of unilateral MTLE on empathy-related brain responses in extra-amygdalar regions has not been investigated. Using functional magnetic resonance imaging, we measured empathy-related brain responses to dynamic fearful faces in 34 patients with unilateral MTLE (18 right sided), in an epilepsy (extra-MTLE; n = 16) and in a healthy control group (n = 30). The primary finding was that right MTLE (RMTLE) was associated with decreased activity predominantly in the right amygdala and also in bilateral periaqueductal gray (PAG) but normal activity in the right anterior insula. The results of the extra-MTLE group demonstrate that these reduced amygdala and PAG responses go beyond the attenuation caused by antiepileptic and antidepressant medication. These findings clearly indicate that RMTLE affects the function of mesial temporal and midbrain structures that mediate basic interoceptive input necessary for the emotional awareness of empathic experiences of fear. Together with the decreased empathic concern found in the RMTLE group, this study provides neurobehavioral evidence that patients with RMTLE are at increased risk for reduced empathy towards others’ internal states and sheds new light on the nature of social-cognitive impairments frequently accompanying MTLE.

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Acknowledgments

The authors acknowledge Dr. Dominik Huber and Thekla Kaisen for technical assistance during fMRI acquisition, and Dr. Victoria Reed for the final edits of the manuscript. This work was supported by the Swiss Epilepsy Foundation.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical standards

All patients and controls provided written informed consent. The study was approved by the local ethics committee and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

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Authors and Affiliations

  1. Swiss Epilepsy Center, Bleulerstrasse 60, 8008, Zurich, Switzerland

    Gianina Toller, Thomas Grunwald, Hans-Jürgen Huppertz, Martin Kurthen & Hennric Jokeit

  2. Memory and Aging Center, Department of Neurology, University of California, San Francisco, USA

    Babu Adhimoolam & Katherine P. Rankin

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  1. Gianina Toller
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  2. Babu Adhimoolam
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Correspondence to Gianina Toller.

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Toller, G., Adhimoolam, B., Grunwald, T. et al. Right mesial temporal lobe epilepsy impairs empathy-related brain responses to dynamic fearful faces. J Neurol 262, 729–741 (2015). https://doi.org/10.1007/s00415-014-7622-2

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  • DOI: https://doi.org/10.1007/s00415-014-7622-2

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