Social Transmission of Fear in Rats: The Role of 22-kHz Ultrasonic Distress Vocalization

BACKGROUND: Social alarm calls alert animals to potential danger and thereby promote group survival. Adult laboratory rats in distress emit 22-kHz ultrasonic vocalization (USV) calls, but the question of whether these USV calls directly elicit defensive behavior in conspecifics is unresolved. METHODOLOGY/PRINCIPAL FINDINGS: The present study investigated, in pair-housed male rats, whether and how the conditioned fear-induced 22-kHz USVs emitted by the ‘sender’ animal affect the behavior of its partner, the ‘receiver’ animal, when both are placed together in a novel chamber. The sender rats’ conditioned fear responses evoked significant freezing (an overt evidence of fear) in receiver rats that had previously experienced an aversive event but not in naïve receiver rats. Permanent lesions and reversible inactivations of the medial geniculate nucleus (MGN) of the thalamus effectively blocked the receivers’ freeezing response to the senders' conditioned fear responses, and this occurred in absence of lesions/inactivations impeding the receiver animals' ability to freeze and emit 22-kHz USVs to the aversive event per se. CONCLUSIONS/SIGNIFICANCE: These results—that prior experience of fear and intact auditory system are required for receiver rats to respond to their conspecifics' conditioned fear responses—indicate that the 22-kHz USV is the main factor for social transmission of fear and that learning plays a crucial role in the development of social signaling of danger by USVs.