Abstract

Ultrasonic vocalizations are among the oldest evolutionarily forms of animal communication. In order to study the communication patterns in an aversive social situation, we used a behavioral model in which one animal, the observer, is witnessing as his cagemate, the demonstrator, is experiencing a series of mild electrical foot shocks. We studied the effect of the foot shock experience on the observer and the influence of a warning sound (emitted shortly before the shock) on USV communication. These experiments revealed that such a warning seems to increase the arousal level, which differentiates the responses depending on previous experience. This can be identified by the emission of characteristic, short 22 kHz calls of a duration below 100 ms. Two rats emitted calls that overlapped in time. Analysis of these overlaps revealed that in ‘warned’ pairs with a naive observer, 22 kHz calls were mixed with 50 kHz calls. This fact, combined with a high fraction of very high-pitched 50 kHz calls (over 75 kHz), suggests the presence of the phenomenon of social buffering. Pure 22 kHz overlaps were mostly found in ‘warned’ pairs with an experienced observer, suggesting a possible fear contagion with distress sharing. The results show the importance of dividing 22 kHz calls into long and short categories.

Highlights

  • The ultrasonic vocalizations (USVs) of animals are among the oldest evolutionarily forms of communication [1]

  • Most rodent vocal communication research focuses on appetitive sounds—in the so-called “50 kHz” class—that derive from a positive emotional state [2,3]

  • Many studies have shown that USV playback or synthetic sound presentation in the 22 kHz class activates the perirhinal cortex, periaqueductal grey matter, the amygdala, or the hypothalamus—the structures involved in defensive behavior [41,58,59]

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Summary

Introduction

The ultrasonic vocalizations (USVs) of animals are among the oldest evolutionarily forms of communication [1]. Rats emit sounds varying in frequency that are inaudible to humans and in a band above 20 kHz, reaching a frequency of up to 125 kHz. Most rodent vocal communication research focuses on appetitive sounds—in the so-called “50 kHz” class—that derive from a positive emotional state [2,3]. Ultrasonic vocalizations ranging from 30 to 125 kHz can be induced by addictive substances [4,5,6,7,8], positive social interaction [9,10,11,12,13,14,15], the anticipation of reward [16,17], and in response to a context associated with appetitive conditioning [4,17,18,19,20]. Jaak Panksepp, an author of the concept of affective neuroscience, classified seven basic emotions as a result of artificial stimulation of the mammalian brain: seeking, rage, fear, lust, care, panic/grief, and play [24]

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