Abstract
BackgroundSocial 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 FindingsThe 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/SignificanceThese 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.
Highlights
Social signaling of imminent danger plays an adaptive role in many species
Subsequent studies found that ultrasonic vocalization (USV) playback and artificial 22-kHz sine waves increase cell activities in the amygdala, the hypothalamus, the periaqueductal grey matter and the perirhinal cortex [18,19,20], brain structures implicated in defensive behavior
Sender rats (SFC) robustly acquired conditioned fear, as assessed by freezing and 22-kHz USV, when presented with 10 pairings of a tone conditioned stimulus (CS: 2.9 kHz, 82 dB, 20 sec) that coterminated with a footshock unconditioned stimulus (US: 2 mA, 1 sec) (Fig. S1A and B)
Summary
Social signaling of imminent danger plays an adaptive (antipredatory) role in many species. Ants use chemical signals to communicate threat to their colony [1]; chickens emit alarm calls that evoke escape responses in cohorts [2]; ground squirrels produce predator alarm calls to warn nearby conspecifics [3]; and monkeys vocalize predator-specific alarm calls that provoke threat-specific defensive behavior in group members [4]. It is generally believed that social distress signals increase group fitness and promote survival of the species [5]. Social signalling of danger (or fear) has been investigated in laboratory rats (Rattus norvegicus). 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
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