Aversive-Bias and Stage-Selectivity in Neurons of the Primate Amygdala during Acquisition, Extinction, and Overnight Retention

Extensive evidence implicates the amygdala as a major station for acquisition, extinction, and consolidation of emotional memories. Most of this work relies on fear-conditioning in rodents and imaging in humans. Few studies have explored coding of value in the primate amygdala, but the circuitry that underlies extinction and overnight retention remains largely unexplored. We developed a learning paradigm for nonhuman primates (macaca fascicularis) and recorded the activity of single neurons during the different stages of acquisition, extinction, and overnight consolidation of pleasant and aversive tone-odor associations. We find that many neurons become phase-locked to respiratory cycles in a stage-dependent manner, emphasizing the flexibility of amygdala neurons to represent the current state and change their spontaneous activity accordingly. We suggest that these changes can serve to increase neuronal sensitivity to an upcoming event and facilitate learning mechanisms. We further show formation of aversive-bias during the acquisition of associations and during overnight retention, in the sense that neurons preferentially code for the aversive conditioned stimuli, even if they initially homogenously represent value of the reinforcer. Our findings show flexible representations in the primate amygdala during the different cycles of learning and memory, and suggest selective potentiation of aversive information.