Impaired auditory recognition of fear and anger following bilateral amygdala lesions

The amygdalar complex is a medial temporal lobe structure in the brain which is widely considered to be involved in the neural substrates of emotion. Selective bilateral damage to the human amygdala is rare, offering a unique insight into its functions. There is impairment of social perception after amygdala damage, with defective recognition of facial expressions of emotion1–4. Among the basic emotions, the processing of fear and anger has been shown to be disrupted by amygdala damage1,2,5. Although it remains puzzling why this not found in all cases6, the importance of the amygdala in negative emotion, and especially fear, has been confirmed by conditioning7, memory8 and positron emission tomography (PET) experiments9,10. Central to our understanding of these findings is the question of whether the amygdala is involved specifically in the perception of visual signals of emotion emanating from the face, or more widely in the perception of emotion in all sensory modalities11. We report here a further investigation of one of these rare cases, a woman (D.R.) who has impaired perception of the intonation patterns that are essential to the perception of vocal affect, despite normal hearing. As is the case for recognition of facial expressions, it is recognition of fear and anger that is most severely affected in the auditory domain. This shows that the amygdala's role in the recognition of certain emotions is not confined to vision, which is consistent with its being involved in the appraisal of danger and the emotion of fear12,13.