Relaying Aversive Ultrasonic Alarm Calls Depends on Previous Experience. Empathy, Social Buffering, or Panic?

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.

Keywords: 22 kHz calls; 50 kHz calls; aversive state; communication; distress; emotional contagion; fear contagion; social buffering; ultrasonic vocalization.

Figure 1

A graphic representation of the experimental design.

Figure 2

Illustration of the training: pre-exposure to the electric foot shocks. To exclude the rats’ aversive conditioning response, the training cage differed from the test cage in terms of smell, light intensity, and shape. Depending on the experimental group, ‘unwarned’ or ‘warned,’ (the group names are according to the test day procedure), a 1.75 kHz sound signaling a foot shock was emitted or not emitted, respectively.

Figure 3

Illustration of the test session. To exclude the rats’ aversive conditioning response, the test cage differed from the training cage in terms of smell, light intensity, and shape. Depending on the experimental group, ‘warned’ or ‘unwarned,’ a 1.75 kHz sound signaling a foot shock was delivered or not delivered, respectively.

Figure 4

Scatterplot of the basic properties of the recorded USV calls, illustrating their mean frequency and duration. Each panel collects all vocalizations recorded for pairs of a certain class. Each of the presented groups were represented by four pairs of rats (eight animals per group). Color denotes the call fraction. Note that the duration is shown on a logarithmic scale.

Figure 5

Fraction of short (<100 ms) 22 kHz calls in the different experimental groups. Brackets mark significant differences identified by the Conover–Iman test. * p < 0.05; ** p < 0.01; *** p < 0.001.

Figure 6

Fraction of 50 kHz calls with a frequency above 75 kHz in different experimental groups. Brackets mark significant differences identified by the Conover–Iman test. * p < 0.05; ** p < 0.01; *** p < 0.001.

Figure 7

Mean frequency of 50 kHz calls in different experimental groups. Brackets mark significant differences identified by the Conover–Iman test. * p < 0.05; *** p < 0.001.

Figure 8

An example of overlapping ultrasonic vocalization presented on a spectrogram.

Figure 9

Fractions of temporal USV overlaps which belong to a certain class: 22 kHz—two 22 kHz calls overlapping, 50 kHz—two 50 kHz calls overlapping, mixed—22 and 50 kHz calls overlapping in different experimental groups. The left panels show the count normalized by the episode count, while the right panels show the count normalized by the total count of temporally overlapping USVs. Brackets mark significant differences identified by the Conover–Iman test. * p < 0.05; ** p < 0.01; *** p < 0.001.