Early-Life Social Isolation Influences Mouse Ultrasonic Vocalizations during Male-Male Social Encounters

Abstract

Early-life social isolation has profound effects on adult social competence. This is often expressed as increased aggression or inappropriate displays of courtship-related behaviors. The social incompetence exhibited by isolated animals could be in part due to an altered ability to participate in communicatory exchanges. House mice (Mus musculus) present an excellent model for exploring this idea, because social isolation has a well-established influence on their social behavior, and mice engage in communication via multiple sensory modalities. Here, we tested the prediction that social isolation during early life would influence ultrasonic vocalizations (USVs) emitted by adult male mice during same-sex social encounters. Starting at three weeks of age, male mice were housed individually or in social groups of four males for five weeks, after which they were placed in one of three types of paired social encounters. Pair types consisted of: two individually housed males, two socially housed males, or an individually housed and a socially housed male (“mixed” pairs). Vocal behavior (USVs) and non-vocal behaviors were recorded from these 15-minute social interactions. Pairs of mice consisting of at least one individually housed male emitted more and longer USVs, with a greater proportional use of USVs containing frequency jumps and 50-kHz components. Individually housed males in the mixed social pairs exhibited increased levels of mounting behavior towards the socially housed males. Mounting in these pairs was positively correlated with increased number and duration of USVs as well as increased proportional use of spectrally more complex USVs. These findings demonstrate that USVs are part of the suite of social behaviors influenced by early-life social isolation, and suggest that altered vocal communication following isolation reflects reduced social competence.

Social experience alters socially induced serotonergic fluctuations in the inferior colliculus

“…Because the two housing treatments differed in timing but not amplitude, we further explored the relationship between a measure of the serotonergic trajectory, 50% rise time, and a measure of vocal behavior, the peak percentage of 50-kHz USVs normalized to all USVs. The 50-kHz USVs are behaviorally potent, corresponding to mounting behavior in male mice interacting with either males or females (Finton et al 2017;Hurley 2012, 2014;Keesom et al 2017). Figure 5 illustrates the relationship between 50% rise times and the peak proportion of 50-kHz USVs.…”

“…These distinctions were made because mice can distinguish between USVs with harmonic elements and USVs without harmonic elements (Neilans et al 2014). Additionally, USVs containing harmonic components are behaviorally significant, being related to mounting behavior directed toward both males (Keesom et al 2017) and females (Hanson and Hurley 2012).…”

“…Second, mice engage in complex social interactions that necessitate the exchange of signals across multiple modalities, with chemical and acoustic signals being particularly important (Arakawa et al 2008;Asaba et al 2014;Portfors 2007). Furthermore, the use of these signals is altered by social experience (Chabout et al 2012;Keesom et al 2017). In the inferior colliculus (IC), a mammalian auditory midbrain nucleus, endogenous fluctuations in serotonergic activity during social encounters between mice correlate with behavior (Hall et al 2011;Hanson and Hurley 2014;Keesom and Hurley 2016).…”

Evolutionary Consequences of Social Isolation

“…There is evidence that social isolation can change gene expression [30] and induce epigenetic modifications [17,31]. The experience of social isolation also clearly affects fitness traits, for example by altering: mate choice and reproductive success [18,32], immunity or disease state [13,33], endocrine profiles [34,35], cooperative predator detection [36], communication [37], social competence [38], and the microbiome [39]. In a number of species, social isolation increases the likelihood of same-sex sexual behaviour (e.g.…”

Social Isolation Rearing Induces Neuropsychiatric Diseases: Updated Overview

“…In fish, social isolation rearing induces continued fights [22]. In another experiment in rodents, social isolation rearing disturbed male-male social interaction [23]. …”