• Open Access

Amygdala damage affects event-related potentials for fearful faces at specific time windows

Authors

  • Pia Rotshtein,

    Corresponding author
    1. School of Psychology, University of Birmingham, Edgbaston, Birmingham, United Kingdom
    2. Wellcome Centre for Neuroimaging at UCL, University College London, London, United Kingdom
    • School of Psychology, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
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  • Mark P. Richardson,

    1. Department of Clinical Neuroscience, King's College London Institute of Psychiatry, London, United Kingdom
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  • Joel S. Winston,

    1. Wellcome Centre for Neuroimaging at UCL, University College London, London, United Kingdom
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  • Stefan J. Kiebel,

    1. Wellcome Centre for Neuroimaging at UCL, University College London, London, United Kingdom
    2. Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
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  • Patrik Vuilleumier,

    1. Laboratory for Neurology and Imaging of Cognition, Department of Neuroscience and Clinic of Neurology, University of Geneva Medical Centre, Geneva, Switzerland
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  • Martin Eimer,

    1. School of Psychology, Birkbeck College, London, United Kingdom
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  • Jon Driver,

    1. Wellcome Centre for Neuroimaging at UCL, University College London, London, United Kingdom
    2. UCL Institute of Cognitive Neuroscience, University College London, London, United Kingdom
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  • Raymond J. Dolan

    1. Wellcome Centre for Neuroimaging at UCL, University College London, London, United Kingdom
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Abstract

The amygdala is known to influence processing of threat-related stimuli in distant brain regions, including visual cortex. The time-course of these distant influences is unknown, although this information is important for resolving debates over likely pathways mediating an apparent rapidity in emotional processing. To address this, we recorded event-related potentials (ERPs) to seen fearful face expressions, in preoperative patients with medial temporal lobe epilepsy who had varying degrees of amygdala pathology, plus healthy volunteers. We found that amygdala damage diminished ERPs for fearful versus neutral faces within the P1 time-range, ∼100–150 ms, and for a later component at ∼500–600 ms. Individual severity of amygdala damage determined the magnitude of both these effects, consistent with a causal amygdala role. By contrast, amygdala damage did not affect explicit perception of fearful expressions nor a distinct emotional ERP effect at 150–250 ms. These results demonstrate two distinct time-points at which the amygdala influences fear processing. The data also demonstrate that while not all aspects of expression processing are disrupted by amygdala damage, there is a crucial impact on an early P1 component. These findings are consistent with the existence of multiple processing stages or routes for fearful faces that vary in their dependence on amygdala function. Hum Brain Mapp, 2010. © 2009 Wiley-Liss, Inc.

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