A fast pathway for fear in human amygdala.
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.
Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Technical University of Madrid, Madrid, Spain.|CEI Campus Moncloa, UCM-UPM, Madrid, Spain.
Constantino
C
Méndez-Bértolo
Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Technical University of Madrid, Madrid, Spain.|Department of Basic Psychology I, Complutense University of Madrid, Madrid, Spain.|Laboratory for Cognitive and Computational Neuroscience, Centre for Biomedical Technology, Technical University of Madrid, Madrid, Spain.
Stephan
0000-0003-0824-8759
S
Moratti
Epilepsy Unit, Department of Neurology, Hospital Ruber Internacional, Madrid, Spain.
Rafael
R
Toledano
Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Technical University of Madrid, Madrid, Spain.
Fernando
F
Lopez-Sosa
Department of Neurosurgery, Hospital Ruber Internacional, Madrid, Spain.
Roberto
R
Martínez-Alvarez
Neuroscience Research Centre, Cardiovascular and Cell Sciences Institute, St. George's, University of London, London, UK.
Yee H
YH
Mah
Laboratory for Neurology and Imaging of Cognition, Department of Neuroscience and Neurology, University Hospital and Medical School, University of Geneva, Geneva, Switzerland.
Patrik
P
Vuilleumier
Epilepsy Unit, Department of Neurology, Hospital Ruber Internacional, Madrid, Spain.
Antonio
A
Gil-Nagel
Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Technical University of Madrid, Madrid, Spain.|Department of Neuroimaging, Reina Sofia Centre for Alzheimer's Research, Madrid, Spain.
Bryan A
0000-0001-6476-4091
BA
Strange
D000328:Adult; D000679:Amygdala / Q000502:physiology*; D001931:Brain Mapping; D005145:Face / Q000502:physiology; D005149:Facial Expression; D005239:Fear / Q000502:physiology*; D005260:Female; D006240:Happiness; D006801:Humans; D008279:Magnetic Resonance Imaging / Q000379:methods; D008297:Male; D011930:Reaction Time / Q000502:physiology; D013647:Task Performance and Analysis; D014793:Visual Cortex / Q000502:physiology*