Ultrasonic communication in rats: can playback of 50-kHz calls induce approach behavior?

Abstract

Rats emit distinct types of ultrasonic vocalizations, which differ depending on age, the subject's current state and environmental factors. Since it was shown that 50-kHz calls can serve as indices of the animal's positive subjective state, they have received increasing experimental attention, and have successfully been used to study neurobiological mechanisms of positive affect. However, it is likely that such calls do not only reflect a positive affective state, but that they also serve a communicative purpose. Actually, rats emit the highest rates of 50-kHz calls typically during social interactions, like reproductive behavior, juvenile play and tickling. Furthermore, it was recently shown that rats emit 50-kHz calls after separation from conspecifics. The aim of the present study was to test the communicative value of such 50-kHz calls. In a first experiment, conducted in juvenile rats situated singly on a radial maze apparatus, we showed that 50-kHz calls can induce behavioral activation and approach responses, which were selective to 50-kHz signals, since presentation of 22-kHz calls, considered to be aversive or threat signals, led to behavioral inhibition. In two other experiments, we used either natural 50-kHz calls, which had been previously recorded from other rats, or artificial sine wave stimuli, which were identical to these calls with respect to peak frequency, call length and temporal appearance. These signals were presented to either juvenile (Exp. 2) or adult (Exp. 3) male rats. Our data clearly show that 50-kHz signals can induce approach behavior, an effect, which was more pronounced in juvenile rats and which was not selective to natural calls, especially in adult rats. The recipient rats also emitted some 50-kHz calls in response to call presentation, but this effect was observed only in adult subjects. Together, our data show that 50-kHz calls can serve communicative purposes, namely as a social signal, which increases the likelihood of approach in the recipient conspecific.

Figure 1. Exemplary spectrograms of the four types of acoustic stimuli presented, namely (from top to down): natural 50-kHz calls, artificial 50-kHz sine wave tones, natural 22-kHz calls, and background noise.

Figure 2. Locomotor activity of juvenile rats in Exp. 1.

Bars depict the distance travelled during test phases without acoustic presentation (nothing), presentation of noise (noise), artificial 50-kHz sine wave tones (50-kHz tones), and natural 50-kHz calls (50-kHz calls). Values reflect means±SEM per minute. Animals of all stimulus orders were collapsed, i.e. n = 12. Comparisons with p<.05 are marked with asterisks: *.

Figure 3. Stimulus-directed locomotor activity of juvenile rats in Exp. 1.

The time spent on the proximal arms in front of the loudspeaker is given for playback of natural 22-kHz calls (white bar) and natural 50-kHz calls (black bar) is depicted on the left. On the right, the time spent on the proximal arms in front of the loudspeaker is given for the 10 min after cessation of playback of natural 22-kHz calls (open symbols) and natural 50-kHz calls (filled symbols). Values reflect means±SEM per minute. In both cases, animals of all stimulus orders were collapsed, i.e. n = 12. Comparisons with p<.05 are marked with asterisks: *.

Figure 4. Locomotor activity of juvenile rats in Exp. 2.

Bars depict the distance travelled during test phases without acoustic presentation (nothing), presentation of noise (noise), artificial 50-kHz sine wave tones (50-kHz tones), and natural 50-kHz calls (50-kHz calls). Values reflect means±SEM per minute. Animals of all stimulus orders were collapsed, i.e. n = 19. Comparisons with p<.05 are marked with asterisks: *.

Figure 5. Stimulus-directed locomotor activity of juvenile rats in Exp. 2.

The number of entries into the distal (black bars) or proximal (white bars) arms from the loudspeaker is given for habituation (HAB), inter-stimulus-intervals (ISI), and playback of acoustic stimuli, i.e. natural 50-kHz calls (50-kHz calls), artificial 50-kHz sine wave tones (50-kHz tones), and background noise (noise) in the upper figure. The time spent on the distal (black bars) or proximal (white bars) arms from the loudspeaker is given for habituation (HAB), inter-stimulus-intervals (ISI), and playback of acoustic stimuli, i.e. natural 50-kHz calls (50-kHz calls), artificial 50-kHz sine wave tones (50-kHz tones), and background noise (noise) in the bottom figure. Values reflect means±SEM per minute. In both cases, animals of all stimulus orders were collapsed, i.e. n = 19. Comparisons with p<.05 are marked with asterisks: *.

Figure 6. Locomotor activity of adult rats in Exp. 3.

Bars depict the distance travelled during test phases without acoustic presentation (nothing), presentation of noise (noise), artificial 50-kHz sine wave tones (50-kHz tones), and natural 50-kHz calls (50-kHz calls). Values reflect means±SEM per minute. Animals of all stimulus orders were collapsed, i.e. n = 36. Comparisons with p<.05 are marked with asterisks: *.

Figure 7. Stimulus-directed locomotor activity of adult rats in Exp. 3.

The number of entries into the distal (black bars) or proximal (white bars) arms from the loudspeaker is given for habituation (HAB), inter-stimulus-intervals (ISI), and playback of acoustic stimuli, i.e. natural 50-kHz calls (50-kHz calls), artificial 50-kHz sine wave tones (50-kHz tones), and background noise (noise) in the upper figure. The time spent on the distal (black bars) or proximal (white bars) arms from the loudspeaker is given for habituation (HAB), inter-stimulus-intervals (ISI), and playback of acoustic stimuli, i.e. natural 50-kHz calls (50-kHz calls), artificial 50-kHz sine wave tones (50-kHz tones), and background noise (noise) in the bottom figure. Values reflect means±SEM per minute. In both cases, animals of all stimulus orders were collapsed, i.e. n = 36. Comparisons with p<.05 are marked with asterisks: *.

Figure 8. Ultrasonic calling of adult rats in Exp. 3.

Bars depict the number of 50-kHz calls emitted by the subject under study during test phases without acoustic presentation (nothing), presentation of noise (noise), artificial 50-kHz sine wave tones (50-kHz tones), and natural 50-kHz calls (50-kHz calls). Values reflect means±SEM per minute. Animals of all stimulus orders were collapsed, i.e. n = 36. Comparisons with p<.05 are marked with asterisks: *