From Play to Aggression: High-Frequency 50-kHz Ultrasonic Vocalizations as Play and Appeasement Signals in Rats

When rats engage in playful interactions, they emit appetitive 50-kHz ultrasonic vocalizations (USVs). We investigated the role of 50-kHz USVs in the playful behavior of both juvenile and adult rats. A cohort of juvenile rats was surgically devocalized and allowed to interact with either devocalized or intact partners as juveniles and again as adults. A substantial decrease in playful motivation was seen for pairs of devocalized rats, as well as all intact rats housed with devocalized ones. In pairs in which at least one partner could vocalize, there was no difference in the number of playful interactions as compared to controls. Further investigation revealed that, within the playful episode itself, 50-kHz USVs are more likely to appear before a playful attack is launched than after, regardless of the attacking partner's ability to vocalize, and when one partner is pinned on its back by another, it is the rat that is on top that is more likely to emit 50-kHz USVs. These findings suggest that, for juveniles, 50-kHz USVs may have a critical function in maintaining and facilitating playful motivation, but a more limited role in signaling playful actions. In adults, however, whatever the motivational role of such calling may be, the various kinds of USVs appear to serve critical communicatory functions. For instance, when pairs of adult males that are unfamiliar with one another encounter each other in a neutral arena, they play together, but if one partner is devocalized, there is a significantly higher likelihood that the interaction will escalate to become aggressive. While the relative roles of appetitive 50-kHz and aversive 22-kHz USVs in this context remain to be determined, our overall findings for play in both juveniles and adults suggest that 50-kHz USVs likely have multiple functions, with different functions being more prevalent at some ages and contexts than others.