Ultrasonic vocalizations as indices of affective states in rats.

Abstract

Adult rats spontaneously vocalize in ultrasonic frequencies. Although these ultrasonic vocalizations (USVs) have been described as by-products of locomotor activity or social signals, accumulating evidence suggests that they may also index anticipatory affective states. Converging ethological, pharmacological, and brain stimulation research indicates that whereas long low-frequency (> 0.3-s, approximately 22-kHz) USVs occur during anticipation of punishment or avoidance behavior, short, high-frequency (< 0.3-s, approximately 50-kHz) USVs typically occur during anticipation of reward or approach behavior. Thus, long 22-kHz USVs may index a state of negative activation, whereas short, 50-kHz USVs may instead index a state of positive activation. This hypothesis has theoretical implications for understanding the brain circuitry underlying mammalian affective states and clinical applicability for modeling hedonic properties of different psychotropic compounds.

“Laughing” rats and the evolutionary antecedents of human joy?

“…The former is primarily seen in affectively negative situations, while the latter is much more evident in positive ones (for a comprehensive review of the background evidence for this and other points made in this paper, see Ref. [40]). In our experience, there is no situation where the 50-kHz chirps are more frequent than when young rats are being tickled by a human experimenter.…”

“…However, in the context of play these vocalizations were much higher than ever observed in the other social contexts. Indeed, these vocalizations were especially frequent when animals were anticipating the opportunity to play, and we came to recognize that such vocal measures could be used as to measure positive affective expectancies [14,40,66].…”

“…One prong of our subsequent work on this vocalization pattern was premised on the possibility that such sounds may be used as a general index of affectively positive incentive motivation [14,39,40], perhaps even a measure of craving of various rewards, including pharmacological ones [66]. We have now extensively developed that idea and feel that it has opened up a new avenue of inquiry into the study of the positive affective experiences of another species [40,66].…”

“…We have now extensively developed that idea and feel that it has opened up a new avenue of inquiry into the study of the positive affective experiences of another species [40,66]. It is important to emphasize that the levels of this vocalization were by far the highest in the context of playful interactions.…”

“…Although all scientists can agree that affective states cannot be measured directly-that has been obvious for a long time-there are a variety of compelling indirect theoretical strategies that offer credible scientific approaches for penetrating into the nature of such mental experiences [55]. Although positive affects, such as joy, may be more difficult than the varieties of fear and anxiety, we proceeded to provisionally hypothesize that 50-kHz chirping could be used as a measure of positive social affect in rodents, and perhaps other appetitive anticipatory processes as well [40,66].…”