Ultrashort-range, high-frequency communication by female mice shapes social interactions

Abstract

Animals engage in complex social encounters that influence social groups and resource allocation. During these encounters, acoustic signals, used at both short and long ranges, play pivotal roles in regulating the behavior of conspecifics. Mice, for instance, emit ultrasonic vocalizations, signals above the range of human hearing, during close-range social interactions. How these signals shape behavior, however, is unknown due to the difficulty in discerning which mouse in a group is vocalizing. To overcome this impediment, we used an eight-channel microphone array system to determine which mouse emitted individual vocal signals during 30 minutes of unrestrained social interaction between a female and a single male or female conspecific. Females modulated both the timing and context of vocal emission based upon their social partner. Compared to opposite-sex pairings, females in samesex pairs vocalized when closer to a social partner and later in the 30 minutes of social engagement. Remarkably, we found that female mice exhibited no immediate changes in acceleration (movement) to male-emitted vocal signals. Both males and females, in contrast, modulated their behavior following female-emitted vocal signals in a context-dependent manner. Thus, our results suggest female vocal signals function as a means of ultrashort-range communication that shapes mouse social behavior. Acoustic signaling is a vital means of both intra-and inter-species communication across the animal kingdom, allowing the transfer of information without limitations of light availability or physical proximity between individuals 1,2. Unlike other communication modalities, acoustic communication is effective over a wide range of distances, and vocalizations are often grouped into two categories: short-and long-range signals 3. Short-range sounds are emitted by most species that vocalize (e.g., marmosets 4 , rats 5 , and moths 6), often used for interpersonal communication and to promote social cohesion 7,8. Long-range signals, while not ubiquitous, are common across the animal kingdom (e.g., wolves 9 , whales 10 , and birds 11). These signals are generally used to warn others, communicate with distant members, or indicate territoriality 9,12,13. Research on long-distance calling often focuses on males 14,15 , even though many species show long-range calling from both sexes 16-19. In some species, females actually emit more long-distance calls than males 20,21. Female elephants, for instance, are more vocal than males and emit long-range calls to communicate with social partners 22. These signals are believed to facilitate social recognition over great distances 23. However, in many animal species the function and range of female-emitted signals is less clear. In mice, the propagation and behavioral impact of female-emitted signals is less established. Adult mice (Mus musculus), while predominately silent in isolation 24 , emit ultrasonic vocalizations, signals spanning 30-110 kHz in frequency 25 , during aggressive and affiliative behaviors 26-30. ...

Spontaneous social communication in laboratory mice - placing ultrasonic vocalizations in their behavioral context

“…In the vast majority of previous studies investigating mouse social communication, USVs were triggered by social deprivation (e.g., two weeks of isolation) and recorded in the first minutes or hours of interaction (Neunuebel et al, 2015;Sangiamo et al, 2020;Warren et al, 2018bWarren et al, , 2020). The USV types were either classified in a pre-determined repertoire (Scattoni et al, 2010) or simplified for modeling to reduce the complexity of the signals (e.g., ignoring harmonic components or frequency jumps or normalizing over duration; (Neunuebel et al, 2015;Sangiamo et al, 2020;Warren et al, 2018bWarren et al, , 2020). In our study, we provide a complementary approach by determining a large set of acoustic variables to avoid masking the complexity of the signals and leave the door open for any user to design their own classification.…”

“…In paired interactions, USVs trigger no behavioral variations in female-female interactions, but males accelerate when the females accelerate while vocalizing in male-female interactions (Warren et al, 2018b(Warren et al, , 2020).…”

Classifying sex and strain from mouse ultrasonic vocalizations using deep learning

“…Similar to humans, mice vocalize frequently during social interactions [2][3][4][5][6]. The complexity of the vocalizations produced during social interactions can be substantial [7][8][9]. Experiments replaying male mouse courtship songs to adult females suggest that at least females are able to guess the sex of other mice based on the properties of individual vocalizations [10,11].…”

Corticostriatal control of defense behavior in mice induced by auditory looming cues

“…The white noise is commonly used as a general-purpose testing sound. It is very different from the communication sounds (either short-range or long-range) of mice 31 in terms of frequency range and spectrotemporal structures. For example, mouse communication sounds consist of ultrasonic frequency-modulated (FM) sweeps [31][32][33] .…”

“…It is very different from the communication sounds (either short-range or long-range) of mice 31 in terms of frequency range and spectrotemporal structures. For example, mouse communication sounds consist of ultrasonic frequency-modulated (FM) sweeps [31][32][33] . Defense-like behaviors triggered by crescendo sounds are most likely responses to the danger signals cued by the temporal change of sound intensity rather than potential physical harms due to a loud sound, since decrescendo stimuli of the same peak intensity failed to induce either freezing or escape.…”