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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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.
The authors declare no competing financial interests.
Integrated supplementary information
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.
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).
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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