Attribution and Expression of Incentive Salience Are Differentially Signaled by Ultrasonic Vocalizations in Rats

During Pavlovian incentive learning, the affective properties of rewards are thought to be transferred to their predicting cues. However, how rewards are represented emotionally in animals is widely unknown. This study sought to determine whether 50-kHz ultrasonic vocalizations (USVs) in rats may signal such a state of incentive motivation to natural, nutritional rewards. To this end, rats learned to anticipate food rewards and, across experiments, the current physiological state (deprived vs. sated), the type of learning mechanism recruited (Pavlovian vs. instrumental), the hedonic properties of UCS (low vs. high palatable food), and the availability of food reward (continued vs. discontinued) were manipulated. Overall, we found that reward-cues elicited 50-kHz calls as they were signaling a putative affective state indicative of incentive motivation in the rat. Attribution and expression of incentive salience, however, seemed not to be an unified process, and could be teased apart in two different ways: 1) under high motivational state (i.e., hunger), the attribution of incentive salience to cues occurred without being expressed at the USVs level, if reward expectations were higher than the outcome; 2) in all experiments when food rewards were devalued by satiation, reward cues were still able to elicit USVs and conditioned anticipatory activity although reward seeking and consumption were drastically weakened. Our results suggest that rats are capable of representing rewards emotionally beyond apparent, immediate physiological demands. These findings may have translational potential in uncovering mechanisms underlying aberrant and persistent motivation as observed in drug addiction, gambling, and eating disorders.