Research reportFemale urine-induced male mice ultrasonic vocalizations, but not scent-marking, is modulated by social experience
Introduction
Rodents communicate primarily via olfactory and acoustic signals. A major source of olfactory communicative signals is contained in scent marks. Scent-marking, the deposition of urine traces in strategic environmental locations, is used by mice to demarcate territories, orchestrate aggressive behavior, recognize individuals, maintain family organization, communicate danger, and to attract mates [1], [2], [3], [4]. Male mice scent marks serve to indicate territorial boundaries [5], [6], advertising the mouse's ability to dominate it and hence the likelihood to maintain the territory against intruders [7], [8], [9] and aid in the orchestration of aggressive behavior [10], [12], [13], [14], [15]. They also allow the recognition of individuals and hence maintenance of family organization [16], [17]. Male scent marks attract female mice [18], [19], [20], [21], [22], [23], [24]. Furthermore, they induce estrous [25] and accelerate the onset of puberty [26]. Scent marks from unfamiliar males can interrupt the establishment of pregnancy in female mice [27].
In addition to the deposition of scent marks, rodents emit ultrasonic vocalizations as acoustic communicative signals [28], [29], [30], [31], [32]. Dependent on species, age, sex and affective state, different types of ultrasonic vocalizations can be detected that appear to serve different communicative purposes. Pup isolation-induced ultrasonic vocalizations elicit maternal retrieval behavior in mice and rats [33], [34], [35], [36]. Anxiety-induced ultrasonic vocalizations serve an alarm function and elicit freezing behavior in rats [37], [38], [39], [40]. Interaction-induced ultrasonic vocalizations elicit social approach behavior in mice and rats [39], [41]. Males exposed to females or female urine emit ultrasonic vocalizations that facilitate mating behavior in mice and rats [42], [43], [44], [45], [46], [47], [48], [49], [50]. In mice, ultrasonic calling is specifically seen in males exposed to female urine as male urine is ineffective [51], [52], [53], [54], [55], [56], [57].
Despite the evidence for a communicative function of rodent scent marks and ultrasonic vocalizations, relatively little is known about the impact of social factors on scent-marking and ultrasonic vocalizations. One of the best known phenomena of social modulation of male scent-marking in response to female scents is its dependence on social status. Dominant males scent mark more than subordinate males [11], [19], [58], [59] and social defeat leads to a reduction in male scent-marking [60]. Importantly, females prefer scent marks deposited by dominant males [19], [21]. Relatively little, however, is known about the social status for the production of ultrasonic vocalizations in response to female scents [61], [62]. Here, one of the best known phenomena of social modulation is the dependence on previous female experience [51], [52], [53], [63], [64], [65], [66]. Typically, male mice do not emit ultrasonic vocalizations when exposed to female urine if they have not been in contact with females previously. However, some findings appear to be inconsistent with a critical familiarity or learning component. In some reports, male mice that had no previous female experience reliably emitted ultrasonic vocalizations to female urine, although mostly to a lower extent [46], [57], [64], [65]. These inconsistencies in male ultrasonic calling might be due to a second modulating factor, freshness of the female urine [64], [65], [66]. For both factors, however, little is known about their effect on the time course of the male's ultrasonic vocalization response.
The first aim of the present study was a more detailed characterization of the effects of these two factors, prior exposure to a female and freshness of the female urine, on male ultrasonic vocalizations elicited by female urine. The second aim was to test whether those two factors affect olfactory communication as well as acoustic responses. The third aim was to test the hypothesis that vocalization and scent-marking responses to female urine are linked. We recently reported that mice who deposit high numbers of scent marks in response to female urine emit more ultrasonic vocalizations than mice who deposit low numbers of scent marks [67]. This link between the two systems was seen under optimal conditions, namely male mice with previous female experience exposed to fresh female urine. The present experiments were designed to understand whether this link holds true under less optimal conditions.
The fourth aim of the present study addressed social cues mediating scent-marking between two inbred strains of mice which differ on sociability. We reported that scent-marking as well as the emission of ultrasonic vocalizations by male mice in response to female urine is dependent on the sociability of the strain [67]. C57BL/6J (B6) is a highly social strain of mice, while BTBR T+tf/J (BTBR) is a low sociability strain that may represent a mouse model of autism [68], [69], [70], [71], [72], [73], [74]. We found that adult male BTBR deposited fewer scent marks and emitted extremely low numbers of ultrasonic vocalizations as compared to adult male B6. The question addressed in the present study is whether this strain difference is specific to exposure to female urine, relevant to sexual mating [18], [19], [20], [21], [22], [23], [24]. Male/male scent countermarking represents a different domain of mouse communication, relevant to territoriality [5], [7], [8], [9], [10], [11], [12], [13], [14], [15] and dominance hierarchies [12], [58], [59], [60]. We therefore tested whether a similar strain difference is seen in scent countermarking in response to male urine.
Section snippets
Animals and housing
Subjects were adult male C57BL/6J (B6) and BTBR T+tf/J (BTBR) mice. For the male subject + female urine spot experiment, N = 45 male B6 mice were used. For the male subject + male urine scent marks experiment, N = 40 male B6 and N = 40 male BTBR mice were used. Breeding pairs were purchased from The Jackson Laboratory (Bar Harbor, ME, USA) and bred at the National Institute of Mental Health in Bethesda, MD, USA. About 2 weeks after pairing for breeding, the females were individually housed and
Male subject + female urine spot: ultrasonic vocalizations
As shown in Fig. 2, emission of ultrasonic vocalizations was dependent on experimental condition in male B6 mice. When comparing the total number of ultrasonic vocalizations emitted during the entire 5 min of female B6 urine exposure, a significant effect of experimental condition was detected by One-Way ANOVA (F2,44 = 3.336, p = 0.045; Fig. 2A). Males with previous female experience exposed to fresh female urine emitted 438.33 ± 109.39 calls, while much lower call numbers were detected in the two
Discussion
Emission of female urine-elicited ultrasonic vocalizations in adult male mice was dependent on previous female experience. Male mice with a previous 5 min exposure to an adult female mouse approximately 1 week before the test session displayed an overall higher ultrasonic vocalization response than male mice with no previous exposure to an adult female mouse. Further, the latency to vocalize was shorter and the rate of vocalizations was more sustained in males with previous exposure to a female.
Acknowledgment
Supported by the National Institute of Mental Health Intramural Research Program.
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