Distinct cortical-amygdala projections drive reward value encoding and retrieval

Abstract

The value of an anticipated rewarding event is crucial information in the decision to engage in its pursuit. The networks responsible for encoding and retrieving this value are largely unknown. Using glutamate biosensors and pharmacological manipulations, we found that basolateral amygdala (BLA) glutamatergic activity tracks and mediates both the encoding and retrieval of the state-dependent incentive value of a palatable food. Projection-specific and bidirectional chemogenetic and optogenetic manipulations revealed the orbitofrontal cortex (OFC) supports the BLA in these processes. Critically, the function of ventrolateral (lOFC) and medial (mOFC) OFC[->]BLA projections was found to be doubly dissociable. Whereas activity in lOFC[->]BLA projections is necessary for and sufficient to drive encoding of a positive change in the value of a reward, mOFC[->]BLA projections are necessary and sufficient for retrieving this value from memory to guide its pursuit. These data reveal a new circuit for adaptive reward valuation and pursuit, indicate dissociability in the encoding and retrieval of reward memories, and provide insight into the dysfunction in these processes that characterizes myriad psychiatric diseases.