The primate amygdala and reinforcement: a dissociation between rule-based and associatively-mediated memory revealed in neuronal activity.

To investigate the role of the primate amygdala in stimulus-reinforcement association learning, the activity of single amygdala neurons was recorded in macaques during two memory tasks. In a visual discrimination task, a population of neurons (17/659) was analyzed which responded differentially to a visual stimulus which always indicated that the primary reinforcer fruit juice could be obtain if the monkey licked, and a different visual stimulus that indicated that the primary reinforcer aversive saline would be obtained if the monkey licked. Most (16/17) of these neurons responded more to the reward-related than the aversive visual stimulus. In a recognition memory task, the majority (12/14 analyzed) of these neurons responded equally well to the trial unique stimuli when they were shown as novel and the monkey had to not lick in order to avoid saline, and when they were shown a second time as familiar and the monkey used the rule that if he licked, fruit juice would be obtained. The responses of these amygdala neurons thus reflect the direct associations of stimuli with reinforcement, but do not reflect the reward value of the stimuli when this must be assessed based on a rule (in the recognition memory task, that a stimulus will be punished the first time it is shown, and rewarded the second). This finding also shows that these amygdala neurons respond to relatively novel stimuli in the same way as they do to stimuli that have become rewarding by stimulus-reinforcement association learning. This provides a neural basis for relatively novel stimuli to be treated as rewarding, and approached.