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

Abstract

<jats:title>Abstract</jats:title><jats:p>In their natural habitat, mice interact and communicate to regulate major functions, such as reproduction, group coordination, and protection. Nevertheless, little is currently known about their spontaneous emission of ultrasonic vocalizations (USVs), despite their broad use as a phenotypic marker in mouse models of neuropsychiatric disorders. Here, we investigated mouse spontaneous communication by coupling automatic recording, segmentation, and analysis of USVs to the tracking of complex behaviors. We continuously recorded undisturbed same-sex pairs of C57BL/6J males and females at 5 weeks and 3 and 7 months of age over three days. Males emitted only a few short USVs, mainly when isolated from their conspecific, whereas females emitted a high number of USVs, especially when engaged in intense dynamic social interactions. The context-specific use of call types and acoustic variations emerged with increasing age. The emission of USVs also reflected a high level of excitement in social interactions. Finally, mice lacking Shank3, a synaptic protein associated with autism, displayed atypical USV usage and acoustic structure, which did not appear in classical protocols, highlighting the importance of studying spontaneous communication. The methods are freely available for the research community (<jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://usv.pasteur.cloud">https://usv.pasteur.cloud</jats:ext-link>).</jats:p>

DLX5/6GABAergic expression affects social vocalization: implications for human evolution

“…In comparison to their normal controls, many Dlx5/6 VgatCre and Dlx5/6 VgaCre/+ mice emit a higher number of longer "complex" calls often not separated by any interruption. These long-modulated USVs are emitted prevalently when mice are engaged in socially-intense behaviours and more rarely during isolated behaviour (Ey, et al 2020). Therefore, the high-vocalization profile of Dlx5/6 VgatCre mice is predictive of an enhanced social behaviour and is in line with our finding of an increase in dynamic socialization of highvocalizing individuals.…”

“…The analysis of the specific types of calls emitted by each animal showed that high-vocalizing animals presented a significant increase in the number of complex vocalizations ("modulated + complex" according to (Ey, et al 2013)) which are the longer vocalization types emitted by mice and can last up to 0.15ms (Figure 3 B). Complex vocalizations have been recently associated to more social behaviours (Ey, et al 2020). Therefore, in this experimental paradigm, designed to detect social vocalization, we observed a new partially-penetrant phenotype characterized by an increase in the number calls, and differences in vocal repertoire and "prosody" (Lahvis, et al 2011).…”

“…courtship, aggression, fear), with the animal's developmental stage, with their genetic background and can be altered by induced genetic modifications. Although the link between USVs profiles and social activity is still incompletely analysed, a recent study has implemented artificial intelligence algorithms to associate USVs of individual mice to specific social actions (Ey, et al 2020;Sangiamo, et al 2020) unveiling a functional correlation between specific USVs and social behaviours. The generation of voluntary structured vocalizations requires the coordination of different levels of cognitive and motor activities and involves a complex and diffuse neural network ranging from the prefrontal and motor cortical areas for voluntary initiation of vocalization to several forebrain and brainstem regions (Jurgens 2002;Simonyan 2014) for the control of laryngeal movements and respiration.…”

Testosterone Increases the Emission of Ultrasonic Vocalizations With Different Acoustic Characteristics in Mice

“…Ey et al revealed that mice used call types in a context-specific manner in same-sex pairs. Interestingly, female pairs emitted more USVs than males when encountering the partner female [10]. Collectively, female mice have the potential to emit USVs, and the emission of USVs also reflects a high level of excitement in social interactions across different contexts [10,11].…”

“…Interestingly, female pairs emitted more USVs than males when encountering the partner female [10]. Collectively, female mice have the potential to emit USVs, and the emission of USVs also reflects a high level of excitement in social interactions across different contexts [10,11]. In the context of male and female sexual interactions in standard experimental settings, male mice are more excited and emit more USVs than females [12,13].…”