Rapid responses of amygdala neurons discriminate facial expressions
2017
The amygdala plays a critical role in detecting potential danger through sensory input. In the primate visual system, a subcortical pathway through the superior colliculus and the pulvinar is thought to provide the amygdala with rapid and coarse visual information about facial emotions. A recent electrophysiological study in human patients supported this hypothesis by showing that intracranial event-related potentials discriminated fearful faces from other faces very quickly (within ~74 ms). However, several aspects of the hypothesis remain debatable. Critically, evidence for short-latency, emotion-selective responses from individual amygdala neurons is lacking, and even if this type of response existed, how it might contribute to stimulus detection is unclear. Here, we addressed these issues in the monkey amygdala and found that ensemble responses of single neurons carry robust information about emotional faces, especially threatening ones, within ~50 ms after stimulus onset. Similar rapid response was not found in the temporal cortex from which the amygdala receives cortical inputs, suggesting a subcortical origin. Additionally, we found that the rapid amygdala response contained excitatory and suppressive components. The early excitatory component might be useful for quickly sending signals to downstream areas. In contrast, the rapid suppressive component sharpened the rising phase of later, sustained excitatory input (presumably from the temporal cortex) and might therefore improve processing of emotional faces over time. We thus propose that these two amygdala responses that originate from the subcortical pathway play dual roles in threat detection.
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