Invited Symposium: Neural Mechanism of Mammalian Vocalization
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Introduction / Copulation in Mice
It has been known for several decades that rodents of a variety of species produce vocalizations during copulation, mother-pup interactions and other "social situations". In rats and mice, the species emphasized in this paper, the vocalizations usually consist of a single frequency band. When the frequency band is lowered electronically to a humanly audible level, the calls resemble brief whistles. These vocalizations have often been shown to play a role in regulating concomitant reproductive and maternal behavior.
In this paper we review what is known about ultrasonic communication in the most studied rodent species: house mice (Mus musculus), Norway rats (Rattus norvegicus). Work on Golden hamsters (Mesocricetus auratus) and other species is also briefly reviewed.
Copulation in House Mice
Spectral Characteristics of Mouse Calls
Two different ultrasonic calls have been identified in mice. One is a pure tone with a mean frequency of around 70 kHz and a duration of from 50 to 300 msec (Sales and Pye, 1974). The second is a pure tone around 40 kHz with a duration of 10 to just over 100 msec.
When Do the Vocalizations Occur?
Ultrasonic calls occur almost exclusively during reproduction. Moreover, by observing dyads of male/male, female/female and male/female pairs, Whitney, Coble, Stockton and Tilson (1973) provided evidence that the 70 kHz vocalizations are produced mainly by the male in this circumstance. More recent evidence involving surgical devocalization has confirmed this finding and extended it to 40 kHz vocalizations as well (White, Prasad, Barfield and Nyby, 1998).
When a male and female are placed together, the male emits 70 kHz vocalizations almost continuously prior to first mount during which time he actively sniffs and investigates the female. After the first mount, the amount of vocalizations declines, although during the latter stages of copulatory behavior, the male intermixes both 70 and 40 kHz calls immediately before and during each mounting bout (Nyby, 1983; Sales and Pye, 1974; White et al, 1998).
Female mice sometimes emit substantial amounts of vocalizations in response to other females (Maggio and Whitney, 1985) but whether these vocalizations have functional significance or are simply inappropriate male-typical behavior is not clear.
Stimuli That Elicit Ultrasonic Vocalizations from Male Mice.
Male mice emit ultrasonic vocalizations not only to a female mouse but also to any chemosignal that signals the presence of a female (Nyby, Wysocki Whitney and Dizinno, 1977). Female urine , female vaginal secretions, female saliva, and even previously neutral cues that are reliably paired with a female, all elicit male vocalizations (Nyby, Whitney, Schmitz and Dizinno, 1978; Nyby et al, 1979, Nyby, Whitney, Dizinno, Schneider and Nunez, 1981; Byatt and Nyby, 1986). More recent work has demonstrated the existence of a powerful but ephemeral ultrasound-eliciting pheromone in female urine that degrades via oxidation within 15-18 hours (Sipos and Nyby, 1992; Sipos, Nyby and Serran, 1993; Sipos, Alterman, Perry, Nyby and Vandenbergh, 1995 ). Adult males innately vocalize to this pheromone although responsiveness can be further enhanced by sexual experience in adulthood. Although males will also vocalize to a much longer lasting pheromone in aged urine (over 24 hours old), responsiveness to this latter signal requires adult sexual experience and the male rapidly habituates to this chemosignal alone. Although the urinary chemosignals that elicit ultrasounds are not present in female urine until after puberty, these chemosignals are nonetheless ovarian independent and, following puberty, are present in the urine at all stages of the female's estrous cycle (Nyby et al 1979).
How Does the Male Detect the Female Signals which Elicit Vocalizations?
Although chemosignals that elicit vocalizations can be detected by either the vomeronasal system or the primary olfactory system, the vomeronasal system appears to play a more central role (Wysocki, Nyby, Whitney, Beauchamp, and Katz, 1982 ). For example, males who have had the vomeronasal system removed prior to having had sexual experience during adulthood are relatively unresponsive olfactorially to chemosignals that normally elicit ultrasounds. Denervation of the olfactory system prior to sexual experience, on the other hand, has little effect on vomeronasal responsiveness (Sipos, Wysocki, Nyby, Wysocki, and Nemura, 1995).
How Do Mouse Vocalizations Affect Reproductive Behavior?
Vocalizations by male mice have been hypothesized to serve a number of different functions. The vocalizations may signal the presence of a dominant male and deter subordinates (Nyby, Dizinno and Whitney, 1976), attract females from a distance (Nunez, Pomerantz, Bean and Youngstrom, 1985) reduce female aggression and withdrawal following courtship (Whitney and Nyby, 1979) and help coordinate copulatory behavior (White et al, 1998). However, definitive explanations await future research.
Endocrine Regulation of Vocalization in Mice
Male mouse vocalizations are androgen dependent. Vocalization amounts are reduced by castration and restored by androgen replacement (Nyby, Dizinno and Whitney 1976; Dizinno and Whitney, 1977). Androgen appears to act following aromatization to estradiol although the 5 alpha reduction pathway of testosterone action may be operative in some strains (Nyby and Simon, 1987). As with other male-typical behaviors, the best site for intracranial androgenic restoration is the medial preoptic area (Nyby, Matochik and Barfield, 1992; Matochik, Sipos, Nyby and Barfield, 1994 ). Virtually complete restoration of behavior to castrates is seen with implants in this area although some restoration is seen in other hypothalamic areas as well (Nyby et al, 1992).
Copulation in Rats
Spectral Characteristics of Rat Calls
Sales (e.g. Sales and Pye, 1994) originally documented a variety of vocalizations in rats, including a brief call with an average spectral frequency of about 50 kHz, and duration of less than 50 msec. More recently, White, Cagiano, Moises and Barfield (1990) documented longer (100 msec), lower frequency (35 kHz) male vocalizations, intermixed with the 50 kHz calls, occurring shortly before ejaculation. Male rats emit long (500 msec to 3 sec) lower frequency calls after ejaculation (Barfield and Geyer, 1975).
Female rats emit vocalizations during copulation. Their calls have similar spectral characteristics to the male 50 kHz calls (Thomas and Barfield, 1985). Calls at lower spectral frequency levels were observed, but in relatively small amounts. Females generally do not call after receiving an ejaculation.
When Do the Vocalizations Occur?
During copulation, male and female rats generally approach each other and sniff. The female darts or runs away from the male at least once, with the male training behind. Then the male generally mounts the female from behind; at the same time the female becomes immobile in the "lordosis" posture, which allows the male to intromit. On most mounts, the male intromits for about 1/3 of a second. This sequence of behavior is repeated up to 15 times before the male ejaculates. Rats can copulate through several ejaculatory series, usually requiring fewer intromissions than the first series. After each ejaculation, there is a 5 minute period of quiescence, in which the male is often immobile and unresponsive to approaches by the female.
The male and female both emit 50 kHz vocalizations throughout the ejaculatory series. As the males were about to ejaculate, they emit the lower frequency pre-ejaculatory call (White et al, 1990). During the post ejaculatory quiescent period, male emit the 22 kHz vocalization, usually while lying still (Barfield and Geyer, 1975).
How Do Rat Vocalizations Affect Reproductive Behavior?
Male 50 kHz calling has been shown repeatedly to stimulate the female darting behavior that generally occurs before intromissions. For example, darting was facilitated when taped vocalizations were played to female rats prior to introduction of a male (Geyer and Barfield, 1978). McIntosh, Barfield and Geyer (1978) found that 50 kHz calls increased darting in females receiving minimal sexual stimulation from a castrated male. When females were presented with both devocalized and vocally intact males, they directed more darts towards the intact male; they also directed more darts towards a devocalized male if taped vocalizations were played in his vicinity (Thomas, Talalas and Barfield, 1982; Thomas Howard and Barfield, 1982a). When female rats were unable to vocalize, they increased their rate of darting and running prior to intromissions. Playback of tape recorded vocalizations restored female darting to control levels (White and Barfield, 1987; 1989).
Taken together, studies of 50 kHz vocalizations in rats suggest that the call stimulates proceptive (solicitation) behavior in rats, such as darting. Female calling may also solicit male sexual behavior; when the female is unable to produce one type of proceptive behavior (calling), she engages in a different type (darting). Calling may also coordinate the sequence of behaviors that lead to intromission.
In mice, male 70 kHz vocalizations attract females. It is unlikely that either male or female rat vocalizations attract partners. Vocalizations occur at a high rate in the presence of a gonadally intact, sexually competent partner. Odor or vocal cues, in the absence of a partner, are less effective in evoking calls from rats of either sex (Geyer and Barfield, 1978; White, Colona and Barfield, 1991; White, Gonzales and Barfield, 1993).
The lower frequency calls occurring prior to ejaculation facilitated lordosis in the female. When male rats were devocalized, females were more likely to move away from the male when he mounted, without maintaining a lordosis posture long enough for him to intromit. Playback of taped male vocalizations increased female immobility in females paired with devocalized females, especially when pre-ejaculatory calls were used (White and Barfield, 1990). Pre-ejaculatory vocalizations may play an important role in facilitating pregnancy; Toner, Attas and Adler (1987) found that female immobility during ejaculation promoted sperm transport to the uterus.
In addition, Adler and his colleagues (e.g. Adler, 1969) demonstrated that progesterone emission in females, required for pregnancy, will not occur unless the female has received a minimum number of intromissions. Given a choice between two or more males, females which have received very few intromissions may not accept intromissions from a male emitting pre-ejaculatory vocalizations. This idea remains to be tested.
Little is known about the behavioral function of the postejaculatory 22 kHz vocalization. (Some interesting hypotheses around evolution and thermoregulation, which are not mutually exclusive with the behavioral analyses presented in this paper, have been proposed by Blumberg and his colleagues). Initially, it was thought that 22 kHz vocalizations may affect the female's behavior, either keeping her in the general vicinity of the male, or keeping her away from his immediate proximity while he was unable to engage in sexual behavior. However, several studies showed that female approaches to the male were not affected by postejaculatory vocalizations (e.g. Thomas, Howard and Barfield, 1982b). Instead, the 22 kHz vocalization may affect the behavior of subordinate males present when the dominant male ejaculates, and who may disrupt transport of sperm if they copulate with the female that the more dominant male has just inseminated. Thomas and Barfield (unpublished observations) found dominant male normally tolerated copulatory behavior by subordinates, but not during the post-ejaculatory interval when the male emitted 22 kHz vocalizations. Instead of engaging in the quiescent behavior that usually occurs in the post-ejaculatory interval, the male attacked the subordinate if he attempted to copulate with the female that he has just inseminated.
Endocrine Regulation of Vocalization in Rats
Geyer, Barfield and McIntosh (1978) found minimal 50 kHz calling in castrated male rats paired with estrous females. Similarly, Geyer and Barfield (1978) observed that ovariectomized female receiving estrogen and progesterone were more effective in eliciting vocalizations from males than unprimed OVX females. In females paired with devocalized males, Matochik, White and Barfield found maximal levels of 50 kHz calling when the female was in the proestrus/early estrus phase of the estrous cycle. White, Colona and Barfield (1991) found that odor cues from gonadally intact adult males elicited more calls from females than odor cues from castrated males or juvenile males.
Copulation in Other Species
Sales (e.g. Sales and Pye, 1974) spectrographed the occurrence of vocalizations in several other rodent species. In general, calls of most murid rodents are similar to those of rats and mice. Calls of cricketed rodents have somewhat more complex spectral characteristics. In addition, Holman (1980) documented the occurrence of ultrasonic calls in the gerbil. Detailed functional analyses were done in two other rodent species, hamsters and desert woodrats.
Floody and Pfaff (1977a,b) and Floody, Pfaff and Lewis (1977) analyzed vocalizations in both male and female hamsters (see also Cherry, 1989). One call, emitted by both males and females, with spectral characteristics which made the call easy to detect at a distance, was shown to attract conspecifics from a distance. This call is emitted in response to odor and other sensory cues left by a conspecific, and likely attracts the conspecific to the caller. The second call, which is less easily perceived from a distance, is only emitted by the male. During copulation, hamster females maintain lordosis for hundreds of seconds, while the male mounts and intromits repeatedly; male calling increases the duration of the female's lordosis response. Floody also suggested that the calls may inhibit aggressive behavior in the dominant hamster female.
In desert woodrats (Neotoma lepida) the behavioral function of a rasping call with components audible to humans, produced shortly before intromission was investigated. The male generally produces the call after approaching and sniffing the female, usually as he pursues the female as she dart away. The call generally continues until intromission. When the male is devocalized, the female was less likely to assume the lordosis posture; playback of tape recordings of the audible component of the male woodrat call increased the likelihood that the female would assume a lordosis posture when mounted by a devocalized male than when tape noise was played (White and Fleming, 1987). v
Maternal Behavior
Detailed studies of the spectral characteristics and behavioral function of pup produced calls have been conducted. These will not be outlined in detail here, due to space limitations. However, infant produced calls have some similarities to the vocalizations produced by adult rodents during copulation. Early work was reviewed by Sales and Pye (1974) and Sales and Smith (1978).
The spectral characteristics of infant calls are rather similar to the calls produced by adults during copulation. Calls from murid rodent pups have simpler structures that those of cricetid rodents. Rats and mice, however, also produce a long broadband call with harmonically related bands in the humanly audible and ultrasonic ranges (Elwood and McCauley, 1983; Ihnat, White and Barfield, 1995; White, Adox, Reddy and Barfield, 1992). Infant calling generally occurs in the time period between birth and weaning (about 3 weeks); the amount of calling varies with age.
Infants cannot regulate their own body temperature, and are especially vulnerable to cold stress shortly before they develop homiothermy (6 to 14 days in mice). At that time, they are especially likely to emit ultrasonic vocalizations in response to cold and isolation, although they also do so at an earlier age. Maternal females will approach a source of pup ultrasounds and odor cues (e.g. Allin and Banks, 1972; Noirot, 1972; Sales and Pye, 1974).
These same authors observed that rats, mice and other rodents also called when handled by the mother, especially 5 days after birth and later. These calls were louder than the vocalization produced by cold stress. In addition, several authors reported that rats and mice broadband vocalizations which were associated with handling (e.g. Noirot, 1971; Okon, 1972; Ehret and Bernecker, 1986; Elwood and McCauley, 1983 and others). Later, Ihnat et al (1995) reported that broadband calls also occurred concurrently with maternal contact, such as nuzzling the pup, retrieval of the pup back to the nest, and stepping on the pup. White et al (1992) reported that maternal contact behaviors increased after the pup was devocalized. These authors agreed with the earlier authors in suggesting that calls emitted during handling are associated with maternal contact, and possibly may reduce rough or aversive contact by the mother.
Summary and References
Rodents of various species emit vocalizations both as infants and as adults during social activity such as copulation.
Rats, hamsters and woodrat vocalizations all promote lordosis behavior in the female. It remains to be seen whether this is the case in the mouse. Female immobility during ejaculation is critical for sperm transport, suggesting that male calls may play a role in pregnancy induction. On the other hand, the female be better able to avoid a male if she has not received enough intromissions to achieve an endocrine state conducive to pregnancy; this situation is possible in rats, which copulate in groups in the natural environment.
In rats, vocalizations may coordinate the complex sequence of behavior patterns that occur between the male and female. This may also contribute to successful pregnancy induction, since both the number and timing of intromissions contribute to the onset of a progestional state.
Male mice and hamsters of both sexes vocalize in response to odor and other cues left by potential partners, who, in turn, will approach a source of vocalizations. Pups of several species call in response to cold or isolation, and, in turn, maternal females will approach a source of calls.
Calling by male mice may reduce aggressive behavior in the female. Female mice are resistant to mount attempts by the male, but it remains to be seen if male calls promote receptivity. (Although it is worthwhile to further investigate the role of male vocalizations on receptivity in mice, it is also important to examine mouse reproductive behavior in a more naturalistic environment, as Adler, McClintock and others have done with rats; such a study may well reveal circumstances in which the female is more receptive, as well as the role of male vocalizations). Floody and Pfaff have suggested that male hamster vocalizations may reduce aggressive behavior in the female. The broadband calls (and other calls induced by handling) reduce contact by the mother; this contact may be rough or aversive, although caution should be exercised in concluding that this is the case.
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