Adult male mice emit context-specific ultrasonic vocalizations that are modulated by prior isolation or group rearing environment

Abstract

Social interactions in mice are frequently analysed in genetically modified strains in order to get insight of disorders affecting social interactions such as autism spectrum disorders. Different types of social interactions have been described, mostly between females and pups, and between adult males and females. However, we recently showed that social interactions between adult males could also encompass cognitive and motivational features. During social interactions, rodents emit ultrasonic vocalizations (USVs), but it remains unknown if call types are differently used depending of the context and if they are correlated with motivational state. Here, we recorded the calls of adult C57BL/6J male mice in various behavioral conditions, such as social interaction, novelty exploration and restraint stress. We introduced a modulator for the motivational state by comparing males maintained in isolation and males maintained in groups before the experiments. Male mice uttered USVs in all social and non-social situations, and even in a stressful restraint context. They nevertheless emitted the most important number of calls with the largest diversity of call types in social interactions, particularly when showing a high motivation for social contact. For mice maintained in social isolation, the number of calls recorded was positively correlated with the duration of social contacts, and most calls were uttered during contacts between the two mice. This correlation was not observed in mice maintained in groups. These results open the way for a deeper understanding and characterization of acoustic signals associated with social interactions. They can also help evaluating the role of motivational states in the emission of acoustic signals.

Figure 1. Number of calls and vocal repertoire uttered in five behavioral contexts.

A- Calls were recorded during social interaction task, novelty exploration, and restraint stress and analyzed off line. B- Total number of calls emitted in 4 minutes: SIT-isolated (n = 17), SIT-grouped (n = 8), EXPLO-isolated (n = 15), EXPLO-grouped (n = 8) and RESTRAINT (n = 16). C- Distribution and spectrograms of the ten call types typically emitted by adult male mice. Data not shown, proportion of “other” calls: 1.4±0.8% in SIT-isolated, 4.5±1.3% in SIT-grouped, 9.5±4.1% in EXPLO-grouped, 3.1±1.3% in EXPLO-isolated and 16.3±3.1% in Restraint stress. (Time and frequency criterion were used to distinguish these categories, see methods). Data are presented as means ± SE. *: p<0.005; **: p<0.0001 for chi-square and Mann-Whitney paired comparisons.

Figure 2. Acoustic characteristics of calls emitted in five behavioral contexts.

A- Calls durations in all conditions. B- Calls durations for all call types in all conditions. C- Frequency features (“min”, “max”, “start” and “end” frequencies) of calls in all conditions. Data are presented as means ± SE. *: p<0.005; **: p<0.0001 for Mann-Whitney paired comparison.

Figure 3. Correlation between behavioral contexts and calls emission.

Correlation between the number of calls of the 3 main categories (“Short”, “Jump” and “Upward”) and duration of contact during social interaction in isolated or non-isolated mice. **: p = 0.005 for Spearman rank correlation test and NS: p>0.05.

Figure 4. Behavioral contexts associated with calls emission during social interactions in isolated and non-isolated mice.

Proportion of calls emitted during contacts and independently of social contact. Inset proportion of social contacts types (oro-oral sniffing, oro-flank sniffing, oro-genital sniffing and other contact) associated with the emission of the 3 main calls types (short, jump and upward). Data are presented as Means ± SE, **: p<0.005 for Wilcoxon signed-rank test.

Figure 5. Interpretative schema of involvement of calls in motivational/emotionnal process.

Proposition of the link between parameters of the calls and motivational/emotionnal processes in adult male mice.