The associative basis of conditioned reinforcement

Abstract

Conditioned reinforcers are Pavlovian cues that support the acquisition and maintenance of new instrumental responses. Responding on the basis of conditioned rather than primary reinforcers is a pervasive part of modern life, yet we have a remarkably limited understanding of what underlying associative information is triggered by these cues to guide responding. Specifically, it is not certain whether conditioned reinforcers are effective because they evoke representations of specific outcomes or because they trigger general affective states that are independent of any specific outcome. This question has important implications for how different brain circuits might be involved in conditioned reinforcement. Here, we use specialized Pavlovian training procedures, reinforcer devaluation and transreinforcer blocking, to create cues that were biased to preferentially evoke either devaluation-insensitive, general affect representations or, devaluation-sensitive, outcome-specific representations, respectively. Subsequently, these cues, along with normally conditioned control cues, were presented contingent on lever pressing. We found that intact rats learned to lever press for cues that evoked either outcome- or affect-specific information to the same extent as for a normally conditioned cue. These results demonstrate that conditioned reinforcers can guide responding through either type of associative information. Further, we went on to investigate the neural basis of outcome- and affect-specific conditioned reinforcement within the orbitofrontal cortex and the basolateral amygdala, two areas previously implicated in conditioned reinforcement. Orbitofrontal cortex lesions impaired conditioned reinforcement mediated by outcome- but not affect-specific information. Additionally, preliminary neural recording results confirmed a role of orbitofrontal cortex in encoding outcome-specific information. However, consistent with extant literature, lesions to the basolateral amygdala, an area reciprocally connected with the orbitofrontal cortex, completely abolished conditioned reinforcement. The implications of these data, along with what we know regarding the contribution of other areas to conditioned reinforcement, will be discussed.