Back to basics: Making predictions in the orbitofrontal-amygdala circuit

Abstract

Underlying many complex behaviors are simple learned associations that allow humans and animals to anticipate the consequences of their actions. The orbitofrontal cortex and basolateral amygdala are two regions which are crucial to this process. In this review, we go back to basics and discuss the literature implicating both these regions in simple paradigms requiring the development of associations between stimuli and the motivationally-significant outcomes they predict. Much of the functional research surrounding this ability has suggested that the orbitofrontal cortex and basolateral amygdala play very similar roles in making these predictions. However, electrophysiological data demonstrates critical differences in the way neurons in these regions respond to predictive cues, revealing a difference in their functional role. On the basis of these data and theories that have come before, we propose that the basolateral amygdala is integral to updating information about cue-outcome contingencies whereas the orbitofrontal cortex is critical to forming a wider network of past and present associations that are called upon by the basolateral amygdala to benefit future learning episodes. The tendency for orbitofrontal neurons to encode past and present contingencies in distinct neuronal populations may facilitate its role in the formation of complex, high-dimensional state-specific associations.

Keywords: Associative learning; Basolateral amygdala; Orbitofrontal cortex; State-specific learning.

Figure 1. OFC and BLA neurons respond differentially to a reversal in contingencies

During initial training (pre-reversal; left panel) both OFC and BLA respond to cues predicting a rewarding outcome. However, when contingencies are reversed (post-reversal; right panel) these neuronal responses diverge. Specifically, the BLA neurons which were encoding the previously reward-predictive outcome now switch to start responding to now reward-predictive cue. In contrast, only about 20% of OFC neurons reverse their preference (Schoenbaum et al., 2003). Instead, a new population of neurons that were previously not cue-selective begin responding to the new contingency.