Individual differences in anticipatory activity to food rewards predict cue-induced appetitive 50-kHz calls in rats

Abstract

Reward-related stimuli come to acquire incentive salience through Pavlovian learning and become capable of controlling reward-oriented behaviors. Here, we examined individual differences in anticipatory activity elicited by reward-related cues as indicative of how animals attribute incentive salience to otherwise neutral stimuli. Since adult rats can signal incentive motivation states through ultrasonic vocalizations (USVs) at around 50- kHz, such calls were recorded in food-deprived rats trained to associate cues with food rewards,which were subsequently devalued by satiation. We found that the extent to which animals developed conditioned anticipatory activity to food cues while food deprived determined the level of cue-induced appetitive USVs while sated. Reexposure to reward cues after a free-testing period reinstated USVs, invigorated reward seeking and consumption, and again, increases in calling occurred only in animalswith high levels of cue-induced anticipatory activity. Reward-experienced rats systemically challenged with the catecholamine agonist amphetamine or with the dopamine receptor antagonist flupenthixol showed attenuated responses to these drugs, especially for USVs and in subjects with high levels of cue-induced anticipatory activity. Our results suggest that individuals prone to attribute incentive salience to reward cues showed heightened reward-induced USVs which were reliably expressed over time and persisted despite physiological needs being fulfilled. Also, prone subjects seemed to undergo particular adaptations in their dopaminergic systemrelated with incentive learning. Our findings may have translational relevance in preclinical research modeling compulsive disorders, which may be due to excessive attribution of incentive salience to reward cues, such as overeating, pathological gambling, and drug addiction.