Chemogenetic inhibition of amygdala to ventrolateral prefrontal cortex communication selectively impacts contingent learning

Contingent learning, the process by which specific courses of action become associated with subsequent outcomes, is dependent on the amygdala and ventrolateral prefrontal cortex (vlPFC). The amygdala and vlPFC are bidirectionally connected but it is unclear what the contribution of individual feedforward and feedback pathways is to contingent learning. Here we tested the role of amygdala projections to vlPFC in mediating two key components of contingent learning: signaling the outcome (reward/no reward) that follows a choice and maintaining representation of the choice that was made prior to outcome delivery. To test for these two aspects of contingent learning, we trained macaques to perform a probabilistic reward learning task where for separate stimulus pairs reward was either delivered immediately or after a trace interval. Inhibiting vlPFC-projecting amygdala neurons impacted contingent learning irrespective of whether there was a trace interval or not, and this effect was primarily driven by maladaptive learning on unrewarded trials. Notably, deficits in contingent learning caused by manipulating activity in the amygdala-vlPFC pathway were distinct from impairments in motivation and the ability to update the value of specific rewards in a reinforcer devaluation task. Thus, vlPFC-projecting amygdala neurons appear to play a specific role in contingent learning through signaling the outcomes of a choice, but not in maintaining a memory of the prior choice.

Amygdala; choices; learning; probability; reward; valuation; ventrolateral prefrontal cortex.