A fast pathway for fear in human amygdala

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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Figure 1: Experimental face stimuli.
Figure 2: Fast-latency human amygdala responses to BSF and LSF fearful faces.
Figure 3: Amygdala iERPs to fearful faces originate from lateral amygdala.
Figure 4: Fast responses to fear are not observed in fusiform gyrus.
Figure 5: Fast-latency amygdala responses are not evoked by complex emotional pictures.

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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

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.

Correspondence to Bryan A Strange.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Structural MRIs.

Coronal and transverse sections of pre-electrode insertion T1 weighted MRIs, illustrating radiologically normal amygdala in the 10 patients for which iERPs are presented. Red arrows indicate the amygdala in which stereotactic electrodes were inserted. L/R: Left/Right.

Supplementary Figure 2 Electrode contact localization in the amygdala for all patients.

Post-operative CT images from each patient have been coregistered with their corresponding pre-operative MRI scan and superimposed to display amygdala contacts in transverse section. In the case of bilateral amygdala implantation, transverse sections are slightly rotated to enable viewing of both left and right contacts in the same cut. Electrode contacts included in each patient’s averaged iERP are indicated in red. Note that post-operative CT quality for Patient 05 precluded adequate coregistration, thus for this patient electrode contacts were localised on post-operative MRI scan (electrode trajectory is visible in the left temporal lobe and correctly targets the amygdala on that side).

Supplementary Figure 3 Amygdala iERPs according to electrode laterality (experiment 1).

Averaged iERPs from 10 amygdalae of 8 patients (total of 26 contacts) to (a) all spatial frequency and (b) broadband and LSF faces are plotted for fearful, happy, and neutral faces separately for both pools of left (n = 6; seventeen contacts) and right (n = 4; nine contacts) amygdala electrodes.

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Méndez-Bértolo, C., Moratti, S., Toledano, R. et al. A fast pathway for fear in human amygdala. Nat Neurosci 19, 1041–1049 (2016). https://doi.org/10.1038/nn.4324

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