Dataset Information

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

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.

SUBMITTER: Brenes JC

PROVIDER: S-EPMC4105501 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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

Brenes Juan C JC Schwarting Rainer K W RK

PloS one 20140721 7

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. s ...[more]

PMID: 25047234

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Project description:Early life stress (ELS) induces long-term effects in later functioning and interacts with further exposure to other stressors in adulthood to shape our responsiveness to reward-related cues. The attribution of incentive salience to food-related cues may be modulated by previous and current exposures to stressors in a sex-dependent manner. We hypothesized from human data that exposure to a traumatic (severe) adult stressor will decrease the attribution of incentive salience to reward-associated cues, especially in females, because these effects are modulated by previous ELS. To study these factors in Long-Evans rats, we used as an ELS model of restriction of nesting material and concurrently evaluated maternal care. In adulthood, the offspring of both sexes were exposed to acute immobilization (IMO), and several days after, a Pavlovian conditioning procedure was used to assess the incentive salience of food-related cues. Some rats developed more attraction to the cue predictive of reward (sign-tracking) and others were attracted to the location of the reward itself, the food-magazine (goal-tracking). Several dopaminergic markers were evaluated by in situ hybridization. The results showed that ELS increased maternal care and decreased body weight gain (only in females). Regarding incentive salience, in absolute control animals, females presented slightly greater sign-tracking behavior than males. Non-ELS male rats exposed to IMO showed a bias towards goal-tracking, whereas in females, IMO produced a bias towards sign-tracking. Animals of both sexes not exposed to IMO displayed an intermediate phenotype. ELS in IMO-treated females was able to reduce sign-tracking and decrease tyrosine hydroxylase expression in the ventral tegmental area and dopamine D1 receptor expression in the accumbens shell. Although the predicted greater decrease in females in sign-tracking after IMO exposure was not corroborated by the data, the results highlight the idea that sex is an important factor in the study of the long-term impact of early and adult stressors.

Project description:Rats are highly social animals known to communicate with ultrasonic vocalizations (USV) of different frequencies. Calls around 50 kHz are thought to represent a positive affective state, whereas calls around 22 kHz are believed to serve as alarm or distress calls. During playback of natural 50-kHz USV, rats show a reliable and strong social approach response toward the sound source. While this response has been studied in great detail in numerous publications, little is known about the emission of USV in response to natural 50-kHz USV playback. To close this gap, we capitalized on three data sets previously obtained and analyzed USV evoked by natural 50-kHz USV playback in male juvenile rats. We compared different rat stocks, namely Wistar (WI) and Sprague-Dawley (SD) and investigated the pharmacological treatment with the dopaminergic D2 receptor antagonist haloperidol. These response calls were found to vary broadly inter-individually in numbers, mean peak frequencies, durations and frequency modulations. Despite the large variability, the results showed no major differences between experimental conditions regarding call likelihood or call parameters, representing a robust phenomenon. However, most response calls had clearly lower frequencies and were longer than typical 50-kHz calls, i.e., around 30 kHz and lasting generally around 0.3 s. These calls resemble aversive 22-kHz USV of adult rats but were of higher frequencies and shorter durations. Moreover, blockade of dopamine D2 receptors did not substantially affect the emission of response calls suggesting that they are not dependent on the D2 receptor function. Taken together, this study provides a detailed analysis of response calls toward playback of 50-kHz USV in juvenile WI and SD rats. This includes calls representing 50-kHz USV, but mostly calls with lower frequencies that are not clearly categorizable within the so far known two main groups of USV in adult rats. We discuss the possible functions of these response calls addressing their communicative functions like contact or appeasing calls, and whether they may reflect a state of frustration. In future studies, response calls might also serve as a new read-out in rat models for neuropsychiatric disorders, where acoustic communication is impaired, such as autism spectrum disorder.

Dataset Information

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

Publications

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

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