Distinct amygdala-striatal and amygdala-cortical circuits encode and retrieve predictive learning to guide choice and decision-making

Abstract

It has long been known that Pavlovian cues can influence choice between instrumental actions, although how this is achieved at a neural level is not fully understood. Here we examined the neural processes engaged during the encoding and retrieval of the Pavlovian stimulus-outcome (S-O) associations prior to and during their influence on choice. Using a Pavlovian-instrumental transfer paradigm (PIT), we found, as previously reported, that a circuit connecting the basolateral amygdala (BLA) and nucleus accumbens shell (BLA[->]NAc-S) is necessary to encode specific S-O associations within the NAc-S. However, this circuit was not required for the retrieval of those associations: optogenetic inhibition of this circuit had no effect on the ability of specific S-O associations to influence choice between instrumental actions. The BLA also projects to the infralimbic cortex (IL) although, using circuit mapping, we found that this projection was largely independent of the projection to the NAc-S. Nevertheless, using a circuit-specific disconnection approach, we found that the BLA[->]IL circuit is necessary for both the encoding and retrieval of specific S-O associations to influence choice. Furthermore, expanding on this disconnection approach, optogenetic inhibition of the BLA[->]IL circuit in one hemisphere and the IL[->]NAc-S contralaterally provided evidence that the broader BLA[->]IL[->]NAc-S circuit is necessary to retrieve specific S-O associations to influence choice during PIT. These data reveal, therefore, evidence of an amygdala-cortico-striatal circuit necessary for the retrieval of predictive learning to influence choice that differs from the circuit involved in encoding those predictive associations.