Attribution and expression of incentive salience are differentially signaled by ultrasonic vocalizations in rats.

Juan C Brenes,Rainer K W Schwarting,Ralph E Mistlberger

doi:10.1371/journal.pone.0102414

Juan C Brenes, Rainer K W Schwarting + Show 1 more

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https://doi.org/10.1371/journal.pone.0102414

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Abstract

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.

Highlights

Having affective representations in terms of pleasures and desires is a fundamental part of our subjective experience
food ad libitum (FAL) phase: When tested without deprivation, there was a transitory increase in the latency to drink and a transitory reduction in the time spent drinking which fully recovered on the following FAL days
On the following FAL days, milk intake partially recovered between about 25% to 43% of the maximal intake achieved under food deprivation (FD) (G: F1,22 = 17.08, p = .0001; DxG: F3,66 = 10.03, p = .0001)

Summary

Introduction

Having affective representations in terms of pleasures and desires is a fundamental part of our subjective experience. The increased percentage of 50-kHz calls induced by the tone cue indicated that attribution of incentive salience to reward-related stimuli had successfully taken place during FD, even thought it was not clearly translated into an overall elevation of 50-kHz calls To account for such an inhibition in USVs utterance, we assume that the ability of food CS cues to elicit appetitive 50-kHz calls was possibly suppressed by FD, an effect that occurred independently from learning acquisition. The three preceding experiments showed that restoring FAL feeding conditions after FD increased spontaneous USVs in controls and potentiated total call number and food cues-induced appetitive 50-kHz calls in reward rats This may suggest that FD itself was able to suppress USVs at the time when animals were expecting the food reward. We adapted the procedure of Experiment 1 in which the higher suppression in calling was observed

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