Abstract

A fast, subcortical pathway to the amygdala is thought to have evolved to enable rapid detection of threat. This pathway's existence is fundamental for understanding nonconscious emotional responses, but has been challenged as a result of a lack of evidence for short-latency fear-related responses in primate amygdala, including humans. We recorded human intracranial electrophysiological data and found fast amygdala responses, beginning 74-ms post-stimulus onset, to fearful, but not neutral or happy, facial expressions. These responses had considerably shorter latency than fear responses that we observed in visual cortex. Notably, fast amygdala responses were limited to low spatial frequency components of fearful faces, as predicted by magnocellular inputs to amygdala. Furthermore, fast amygdala responses were not evoked by photographs of arousing scenes, which is indicative of selective early reactivity to socially relevant visual information conveyed by fearful faces. These data therefore support the existence of a phylogenetically old subcortical pathway providing fast, but coarse, threat-related signals to human amygdala.

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Acknowledgements

We thank the electroencephalography technicians at the Hospital Ruber Internacional. This work was supported by Project grant SAF2011-27766 from the Spanish Ministry of Science and Education and Marie Curie Career Integration Fellowship (FP7-PEOPLE-2011-CIG 304248) to B.A.S., a PICATA fellowship of CEI Moncloa (UCM-UPM) to C.M.-B., and a Ramón y Cajal fellowship (RYC-2009-04974) to S.M. This work was supported by Project grant SAF2011-27766 from the Spanish Ministry of Science and Education, Marie Curie Career Integration Fellowship (FP7-PEOPLE-2011-CIG 304248), and BIAL Foundation Grant 119/12 to B.A.S.

Author information

Author notes

    • Constantino Méndez-Bértolo
    •  & Stephan Moratti

    These authors contributed equally to this work.

Affiliations

  1. Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Technical University of Madrid, Madrid, Spain.

    • Constantino Méndez-Bértolo
    • , Stephan Moratti
    • , Fernando Lopez-Sosa
    •  & Bryan A Strange
  2. CEI Campus Moncloa, UCM-UPM, Madrid, Spain.

    • Constantino Méndez-Bértolo
  3. Department of Basic Psychology I, Complutense University of Madrid, Madrid, Spain.

    • Stephan Moratti
  4. Laboratory for Cognitive and Computational Neuroscience, Centre for Biomedical Technology, Technical University of Madrid, Madrid, Spain.

    • Stephan Moratti
  5. Epilepsy Unit, Department of Neurology, Hospital Ruber Internacional, Madrid, Spain.

    • Rafael Toledano
    •  & Antonio Gil-Nagel
  6. Department of Neurosurgery, Hospital Ruber Internacional, Madrid, Spain.

    • Roberto Martínez-Alvarez
  7. Neuroscience Research Centre, Cardiovascular and Cell Sciences Institute, St. George's, University of London, London, UK.

    • Yee H Mah
  8. Laboratory for Neurology and Imaging of Cognition, Department of Neuroscience and Neurology, University Hospital and Medical School, University of Geneva, Geneva, Switzerland.

    • Patrik Vuilleumier
  9. Department of Neuroimaging, Reina Sofia Centre for Alzheimer's Research, Madrid, Spain.

    • Bryan A Strange

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Contributions

C.M.-B., S.M., P.V., A.G.-N. and B.A.S. designed the experiments. C.M.-B., F.L.-S. and R.T. collected data and C.M.-B., S.M. and B.A.S. performed analyses. R.T. and A.G.-N. monitored patients and performed clinical evaluation. R.M.-A. performed surgical electrode implantation. Y.H.M. designed and performed electrode contact localization. B.A.S., C.M.-B., S.M. and P.V. wrote the paper with input from all of the other authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Bryan A Strange.

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https://doi.org/10.1038/nn.4324