Abstract
The amygdala is thought to be essential for rapid, pre-conscious detection of fear through a putative subcortical pathway. Some fMRI studies have suggested such a pathway by showing amygdala activation to fear faces that were not consciously perceived (although this is debated), whereas electrophysiological studies generally demonstrate rather long response latencies in the amygdala. We tested subject SM, who has complete bilateral lesions of the amygdala, on three psychophysical tasks to characterize the stage of her impairment in visual processing of fear. First, we tested SM's ability to rapidly detect a fearful face in speeded spatial 2AFC and 4AFC tasks. While SM detected a fearful face as rapidly and accurately as controls on discrimination of fear/anger/threat from neutral stimuli in the 2AFC task, she was much slower in the 4AFC task, where a target fearful face was embedded among happy, sad, and neutral faces. Analysis of eye movements indicated that controls terminated search at the fearful face, while SM needed to inspect all faces, perhaps indicative of identifying fear by exclusion from any other emotion. Second, we investigated visual search among face morphs between fearful vs. neutral/happy/sad expressions. When asked to detect a more fearful morph among less fearful morphs, all subjects, including SM, detected the fearful face faster when the physical morph difference spanned a perceptual category boundary for fear. Finally, using Continuous Flash Suppression to suppress conscious perception of faces, we found that SM became aware of fearful faces more quickly than happy faces, just like has been reported for healthy subjects (Yang et al 2007 Emotion). We conclude that early, rapid, and pre-conscious processing of fearful faces might rely on visual cortex rather than the amygdala.
We thank Jessica Levine and Catherine Holcomb for help in testing subjects, and the Gordon and Betty Moore Foundation for funding support. NT is supported by Japan Society for the Promotion of Sciences.