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Responses of Single Neurons in Monkey Amygdala to Facial and Vocal Emotions

¹National Institute of Neuroscience, National Center of Neurology and Psychiatry, Tokyo; ²Collaboration of Regional Entities on Science and Technology, Japan Science and Technology Agency, Saitama; and ³Primate Research Institute, Kyoto University, Aichi, Japan

Submitted 3 May 2006; accepted in final form 13 December 2006

The face and voice can independently convey the same information about emotion. When we see an angry face or hear an angry voice, we can perceive a person's anger. These two different sensory cues are interchangeable in this sense. However, it is still unclear whether the same group of neurons process signals for facial and vocal emotions. We recorded neuronal activity in the amygdala of monkeys while watching nine video clips of species-specific emotional expressions: three monkeys showing three emotional expressions (aggressive threat, scream, and coo). Of the 227 amygdala neurons tested, 116 neurons (51%) responded to at least one of the emotional expressions. These "monkey-responsive" neurons—that is, neurons that responded to monkey-specific emotional expression—preferred the scream to other emotional expressions irrespective of identity. To determine the element crucial to neuronal responses, the activity of 79 monkey-responsive neurons was recorded while a facial or vocal element of a stimulus was presented alone. Although most neurons (61/79, 77%) strongly responded to the visual but not to the auditory element, about one fifth (16/79, 20%) maintained a good response when either the facial or vocal element was presented. Moreover, these neurons maintained their stimulus-preference profiles under facial and vocal conditions. These neurons were found in the central nucleus of the amygdala, the nucleus that receives inputs from other amygdala nuclei and in turn sends outputs to other emotion-related brain areas. These supramodal responses to emotion would be of use in generating appropriate responses to information regarding either facial or vocal emotion.

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