Ultrasonic vocalizations in rats

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From a comparative perspective it could be most useful to examine ultrasonic vocalizations in closely related species. Many important questions could be asked and we have sufficient data to answer them. One such question is whether vocalizations are also a male prerogative in other species. Another is whether vocalizations influence copulatory behavior and/or the incentive properties of the

FIGURE 3.1 Ultrasonic vocalizations recorded from a sexually receptive female rat in response to exposure to an inaccessible male.

emitting animal. A third may be concerned with the stimuli required for activation of vocalizations. It could also be illuminative to determine their hormone dependency. If the answers to all these questions were similar to those obtained in studies on mice, we could conclude that the function and control of vocalizations have been conserved and that generalizations among species is meaningful. On the other hand, if there were important species differences, we would have to conclude that interspecies generalizations are meaningless or, still worse, they might be misleading. Let us begin with an analysis of vocalizations in rats. An example of a record of female rat precopulatory vocalizations are shown in Figure 3.1 and Figure 3.2 is a photograph of the experimental setup used for studying the emission of ultrasounds.

Abundant 22 kHz vocalizations following ejaculation in the male rat were the first high frequency sounds described in association with rat sexual behavior (Barfield and Geyer, 1972). The poetic spirit of Ron Barfield made him coin the expression 'post-ejaculatory song'. This song has been much studied and many functions have been attributed to it. The song is essentially limited to the absolute refractory period, the time following an ejaculation during which it is impossible to reactivate male sexual behavior. This interval constitutes about 75% of the post-ejaculatory interval. During the remaining 25% the male does not sing and it is possible to reactivate his behavior by stimuli heightening his arousal, like pinching his tail or applying electric shocks to his skin. Since the song coincides in time with a period where the male is unresponsive to the female, it was suggested that its function was to inhibit female sexual behavior and to maintain the female at some distance and consequently delay her sexual advances (Barfield and Geyer, 1975; Geyer and Barfield, 1980). Albeit interesting, this hypothesis turned out to be false. Devocalized males have post-ejaculatory intervals of the same length as vocalizing males and the female does not keep a longer distance between herself and a vocalizing male than between herself and a devocalized male (Thomas et al., 1982a). Furthermore, if the female is given the opportunity to escape from the male following the ejaculation she stays away for a longer time if the male is devocalized, which is exactly the contrary to what would be predicted from the hypothesis

FIGURE 3.2 The experimental setup employed for the recording of the vocalizations shown in Figure 3.1. The female was housed in the small cylinder, while the male was introduced into the larger one. At the bottom of each cylinder, facing the other, is an opening covered with wire mesh. This allows the experimental subjects to smell, see and hear each other. No physical interaction is possible, not even snout to snout, because there is a 1 cm separation between the cylinders. Note the microphone located just above each cylinder and the sound absorbing cover on the inside cylinder walls. This arrangement makes it possible to record sounds from both animals simultaneously and in separate channels. The microphone over each cage is so oriented that only sounds originating within that cage are recorded. The camera above each cage is synchronized with the sound recording equipment, which allows an analysis of the behavior displayed at the moment of vocalization.

FIGURE 3.2 The experimental setup employed for the recording of the vocalizations shown in Figure 3.1. The female was housed in the small cylinder, while the male was introduced into the larger one. At the bottom of each cylinder, facing the other, is an opening covered with wire mesh. This allows the experimental subjects to smell, see and hear each other. No physical interaction is possible, not even snout to snout, because there is a 1 cm separation between the cylinders. Note the microphone located just above each cylinder and the sound absorbing cover on the inside cylinder walls. This arrangement makes it possible to record sounds from both animals simultaneously and in separate channels. The microphone over each cage is so oriented that only sounds originating within that cage are recorded. The camera above each cage is synchronized with the sound recording equipment, which allows an analysis of the behavior displayed at the moment of vocalization.

mentioned above (Thomas et al., 1981). The fact that the female returns faster to a vocalizing male than to a devocalized male could actually suggest that the vocalizing male is more attractive. This is in line with other data showing that sexually receptive females display solicitations in response to castrated males when exposed to the 22 kHz vocalizations (Mcintosh et al., 1978). The results of this study as well as those of the Thomas et al. (1981, 1982a) studies suggest that these vocalizations enhance rather than inhibit female sexual behavior. We are now faced with a rather significant amount of contradictory data, making it impossible to arrive at a reasonably well-founded conclusion. However, a nicely designed study in a seminatural environment failed to detect any effect at all of the male's 22 kHz vocalizations on female behavior (Anisko et al., 1978). It would seem, then, that the most likely conclusion is that the post-ejaculatory song has no consequences for social or sexual behaviors.

In addition to the post-ejaculatory 22 kHz vocalizations described above, the male rat occasionally emits pre-ejaculatory vocalizations of the same frequency. These pre-ejaculatory calls are of shorter duration than those emitted during the post-ejaculatory interval. The first description of these calls comes from a study where rats were allowed to copulate until exhaustion (Brown, 1979). When approaching the fifth ejaculation males began to emit these calls. The appearance of the 22 kHz calls coincided with an increase in the number of mounts without intromission. The males actually mounted more but intromitted less. An analysis of the behavior of the female partner showed that this was caused by a lessened tendency to display lordosis in response to male mounting. Furthermore, the females showed more aggressive responses (turning away, kicking and boxing) when pursued by the male. This is most interesting since aggressive encounters are another situation associated with emission of 22 kHz calls (Lore et al., 1976). Thus, it is quite possible that the pre-ejaculatory calls are unrelated to copulatory behavior. Instead, they may be a simple side effect of aggressive behaviors on the part of the female. It can also be noted that these vocalizations are emitted in several other stressful situations like exposure to a cat (Blanchard et al., 1991), handling (Brudzynski and Ociepa, 1992), defeat (Corrigan and Flannelly, 1979) or isolation (Francis, 1977). Whatever their function may be, it is probably related to something entirely different from copulatory behavior. In fact, playback of 22 kHz vocalizations has been reported to reduce locomotor activity for a short time immediately following the end of the playback period (Brudzynski and Chiu, 1995). During playback, however, there was no change in activity. If we try to relate this observation to the post-ejaculatory song and the initial proposal concerning its possible function, we face a considerable intellectual challenge. It was, as mentioned a few lines above, shown that the song lasted until the end of the relative refractory period. During that period, the listening female displayed low activity or even immobility (Geyer and Barfield, 1980). When the song ended, she resumed activity, which is exactly the opposite of what was found in the playback experiment. We seem to be forced to admit that the behavioral consequences of the 22 kHz vocalizations are not clear-cut. A possible explanation for these contradictory observations is that there are several types of 22 kHz calls, one specific for the post-ejaculatory interval, another for aggressive encounters, and so on. A small problem with this explanation is that there is no evidence for the existence of such differences. On the contrary, 22 kHz calls emitted under various circumstances seem to be quite similar both in duration and magnitude (Adler and Anisko, 1979). Sonograms and power spectra of calls emitted in response to stimuli as diverse as handling, footshock or intracerebral injections of carbachol are also very similar (Brudzynski et al., 1991).

Males also emit vocalizations with a frequency around 50 kHz (Sales, 1972). Sexually experienced males start calling as soon as they are introduced into the mating test cage, before any female is present (Barfield et al., 1979; Bialy et al., 2000). These calls are absent in males lacking sexual experience, showing that learning is necessary for them to occur. Once copulation has been initiated, the male vocalizes before he mounts, intromits and ejaculates. The amount of vocalization is largest during the 10 seconds preceding ejaculation, somewhat lower in the period preceding an intromission and still lower before a mount (McIntosh and Barfield, 1980). These observations prompted the suggestion that the 50 kHz vocalizations somehow reflect the male's level of arousal. This may well be the case, but the crucial question is not what the vocalizations might reflect but what their effect on other animals, for example the copulation partner, might be. Since heterosexual copulation is an interaction between at least one male and one female, any functionally relevant effect of the male's vocalizations must be on this interaction. Because most calling occurs just before a sexual interaction, be it mount, intromission or ejaculation, it might be speculated that the calls' function would be to stop the female and facilitate the assumption of the lordosis posture. Chasing the female around the mating cage is one of the main tasks of the male in most copulation tests in rats and, as soon as the female interrupts a run and suddenly stops, the male frequently proceeds with a mount. This mount may or may not be associated with vaginal penetration (intromission) and intromission may or may not be associated with ejaculation. In any case, the female must stop running before the male can make a successful mount. It seems quite reasonable to assume that the male's calls could have such a stopping function and thereby facilitate the sexual interactions. This does not seem to be the case, though. A devocalized male mounts, intromits and ejaculates just as fast as a calling male, he makes the same number of mounts and intromissions and he has the same post-ejaculatory interval. If we focus on the female rather than on the male behaviors, it is found that the number of darts per unit time is lower in females copulating with devocalized males (Thomas et al., 1981). However, this effect has no functional significance since no aspect of the sexual interaction is modified. We are forced to conclude that the male rat's 50 kHz vocalizations have no influence on copulatory behavior. That is exactly the conclusion we arrived at with regard to vocalizations in the male mouse. In contrast to the lack of a role in the control of copulatory behavior, I convinced you that the vocalizations enhanced the male mouse's incentive value. We will now see if this is the case also in rats.

It is not. A devocalized male rat is just as attractive as a vocalizing male. Furthermore, a devocalized male presented together with taped vocalizations is not more attractive than another male presented together with tape hiss (Thomas et al., 1982b; White and Barfield, 1990). According to these studies, then, vocalizations do not contribute to a male rat's incentive value. However, results from an experiment in a Y maze seem to contradict this assertion (Barfield et al., 1979). Female rats were allowed to choose between one arm in which male calls were played back and another without sound. The subjects preferred the arm with sound, an observation that could suggest that the calls have incentive properties. Unfortunately, this experiment does not provide conclusive evidence. It only shows that sound is preferred over no sound, but it is possible that any sound would have had the same effect as the male's tape-recorded vocalizations. We are forced to conclude that there is slight evidence for the hypothesis that male ultrasonic vocalizations have positive incentive properties. The negative evidence seems to be more convincing.

When discussing the mice data a couple of paragraphs ago, I mentioned that the female is silent during sexual encounters. That extraordinary quality is not found in rats. In fact, females vocalize as much as males and their vocalizations are indistinguishable from those of males, at least with regard to frequency, duration and amplitude (Thomas and Barfield, 1985). Studies of the possible behavioral consequences of female vocalizations have shown that females show more darting when they are devocalized than when they emit sounds. This effect may be caused by the fact that the male approaches and pursues a silent female more than a vocalizing female. Darting is a response activated by the male's approach or by direct tactile stimulation of the female's posterior. Thus, more frequent approaches and pursuits on the part of the male may lead to enhanced display of darting. The increased female darting as well as the enhanced male pursuit can be eliminated by playback of tape-recorded calls (White and Barfield, 1987, 1989). A reasonable interpretation of the fact that the female's vocalizations reduce the male's approaches to and pursuit of her would be that the sounds somehow keep the male away, i.e. they function as negative incentives. Furthermore, such a proposal is consistent with the data obtained in paced mating tests. As mentioned some pages ago, the female displays avoidance behaviors after intromissions and ejaculation and, when the female can pace sexual interaction, the intervals between successive intromissions is longer than when the male is in control. It may also be remembered that paced mating is associated with higher fertility than male-controlled mating (Coopersmith and Erskine, 1994). Ultrasonic vocalizations may contribute to slow down the copulatory interactions by keeping the male away for some time, thereby keeping the interintromission interval closer to that assuring maximal fertility. Instead of making this rather obvious proposal, White and Barfield (1989) suggest that 'female vocalizations may function proceptively, to stimulate male sexual responses' (p. 232). While the data show that devocalization enhances male sexual responses, the authors conclude the opposite. They continue by proposing that 'when the female is unable to vocalize, she increases her rate of other proceptive behaviors such as darting' (p. 232). Here we have a nice example of anthropomorphism blended with teleology. First, it is assumed that the female thinks that her silence makes her less attractive and that she consequently has to enhance her attractivity by some other means, for example by darting and running more. Just as a distasteful woman may enhance her attractiveness by buying haute couture clothes from Christian Dior and perfumes from Chanel. Second, the rat needs to be cognizant of the purpose of her behavior. Although the female rat may be flattered by being attributed such exquisite intellectual capacities, both assumptions are completely unfounded.

The conclusion of the devocalization study I presented in the preceding paragraph is nicely supported by a most interesting observation: deafening of the male rat has the same effect as devocalization of the female. Both female darts and male pursuits are increased (White and Barfield, 1987). Here it is difficult to imagine that the female enhances her darting because she wants to make herself more attractive. It is unlikely that the females know that their partner is deaf, however exquisite their intelligence may be. Thus, the change in female behavior must be secondary to deafness-induced changes in male behavior. This proposal also applies to the White and Barfield (1989) experiment. The devocalized female did not modify her behavior because she was silent. She did so because her silence had modified the male's behavior.

Before leaving the role of female vocalizations, it must be insisted upon the fact that their effects on male copulatory behavior are minor. Despite the effects on approach and pursuit, they do not modify any of the fundamental parameters of male behavior, such as the number of pre-ejaculatory intromissions or the ejaculation latency. I would even venture to conclude that female rat ultrasonic vocalizations are of no functional significance with regard to copulatory behavior.

Despite the slight evidence for a role of ultrasonic vocalizations in rat sexual behavior, I will briefly examine the stimuli required for their activation and their dependence on gonadal hormones. Such an analysis could shed some light on the question of whether they are sexual responses or not. It is also easily done, because data from rats are quite scarce.

As might be expected, olfactory stimuli seem to be important for the activation of ultrasonic vocalizations both in male and female rats. Bedding soiled by a member of the opposite sex is more efficient than clean bedding (Geyer and Barfield, 1978) and exposure to an invisible and untouchable, devocalized male is sufficient for enhancing vocalizations in females (White et al., 1991). Moreover, odors from an intact male or a sexually receptive female are more effective than odors from a castrated male or an ovariectomized female for stimulating vocalizations. All these data clearly suggest that olfactory stimuli are sufficient for enhancing vocalizations in rats. Whether they are necessary or not is unknown. I have not been able to find any study determining whether anosmic rats vocalize or not, making it impossible to conclude anything at all concerning the necessity of olfactory stimuli. An observation of some importance in this context is that a living, sexually receptive female is far more efficient than her odor for stimulating vocalizations (Geyer and Barfield, 1978), at least in sexually experienced males. This would suggest that, although olfaction is sufficient, other stimuli contribute in a significant way. The other stimuli are not auditory, since adding tape-recorded vocalizations to the presence of a devocalized male does not change his capacity to stimulate vocalizations in female rats (White et al., 1991). On the contrary, if male vocalizations are played back in the absence of any male, then female vocalizations are slightly stimulated (White et al., 1993). This finding is important, because it shows that the female somehow responds to the male's vocalizations when no other stimulus emitted by the male is present. Such a situation could easily occur in the wild. A female rat may be walking around and a distant male may start to vocalize at some point. The female would vocalize in response, thereby establishing some kind of contact. She could easily localize the calling male and approach him and the male could also approach the calling female. What then might follow should be left in the obscure, for simple decency. The only problem with this nice story is that there are not much data supporting it. At the same time, there are no data contradicting it.

Compared to mice, relatively little is known about the stimulus control of ultrasonic vocalizations associated with sexual behavior in rats. We know that olfactory stimuli are sufficient both in rats and mice and we also know that they are necessary in mice. Whether this is also the case in rats is, as mentioned, unknown. Furthermore, we know that sexual experience is not necessary for vocalizations in mice. The role of experience in rats is not well known. All rat studies I have knowledge of, except one, have employed sexually experienced animals, probably because the possible importance of learning was of no concern for the scientists involved. The exception study (McGinnis and Vakulenko, 2003) employed an original procedure in which the male subject first was exposed to a female behind a wire net for 5 min. The female was then removed and vocalizations were recorded during the following 5 min. In this procedure, sexually inexperienced males vocalize equally after exposure to an ovariectomized or a sexually receptive female. However, they vocalize more following exposure to the receptive female than following exposure to a male. After the acquisition of sexual experience, exposure to the receptive female induces more vocalizations than exposure to the ovariec-tomized female. If we assume that the after-effects of exposure to a female are identical to exposure itself, then these data suggest that a female is a weak unconditioned stimulus for the activation of ultrasonic vocalizations in male rats. At the same time, they show that learning greatly enhances the response. Whether these conclusions also apply to vocalizations in the female is not known.

There is only one aspect of ultrasonic vocalizations in which rats and mice appear to be equally well known: their dependence on gonadal hormones. Castrated male rats vocalize a lot less than intact males (Geyer et al., 1978) and ovariectomized females vocalize less than females rendered sexually receptive by treatment with estradiol and progesterone (Thomas and Barfield, 1985). Just as is the case with the induction of lordosis, sequential treatment with estradiol and progesterone is the most efficient procedure for stimulating vocalizations in ovariectomized females (Matochik et al., 1992a). Further support for a role of ovarian hormones is provided by a study of variations in vocalizations in response to a male during the estrus cycle. The amount of vocalizations emitted during proestrus - early estrus is far above that observed at any other stage of the cycle (Matochik et al., 1992b). There is, then, solid evidence for a role of ovarian hormones in the control of female rat vocalizations. The situation in the male is not as clear-cut. Although there is no doubt that castration reduces vocalizations, there is some confusion concerning the crucial hormone. An early study comparing the ability of testosterone, dihydrotestosterone and estradiol with regard to capacity to restore vocalizations in castrated males showed that only testosterone was effective (Matochik and Barfield, 1991). Since testosterone is aromatized to estradiol and reduced to dihydrotestosterone and since neither estradiol nor dihydrotestosterone was active by itself, these data suggest that estrogen and androgen receptors must be stimulated simultaneously. The ineffectiveness of estradiol was confirmed several years later (Cooke et al., 2003), but the more recent study found that dihydrotestosterone re-established vocalizations. The combination of dihydrotestosterone and estradiol was no more effective than dihydrotestos-terone alone. These results clearly contradict the Matochik and Barfield (1991) data. One replicable observation is that estradiol does not affect vocalizations in the male rat. The role of the androgen receptor is unclear with one study finding it necessary but not sufficient and another study finding it necessary and sufficient. A third study, showing that an androgen receptor antagonist, hydroxyflutamide, blocks testosterone-induced restoration of vocalizations in castrated animals when implanted into the ventromedial nucleus of the hypothalamus (Harding and McGinnis, 2004) confirms that the androgen receptor is necessary. However, whether it is sufficient or not for allowing the male rat to produce ultrasonic vocalization in response to a female is an unsettled issue. Nevertheless, there is no doubt that these vocalizations are not produced by males lacking gonadal hormones.

There are some curious differences between rats and mice with regard to the intracerebral localization of androgen effects on ultrasonic vocalizations. While several studies have established that androgens within the medial preoptic area activate vocalizations in male mice this does not seem to be the case in rats. Although there are no data on the effects of local administration of androgens to the preoptic area in castrated male rats, there is a study evaluating the effects of local administration of an androgen receptor antagonist (Harding and McGinnis, 2004). Intrapreoptic hydroxyflutamide did not reduce the capacity of testosterone to restore vocalizations in castrated males. This indicates that the preoptic area is not the site of action of androgens. As was mentioned in the preceding paragraph, the androgen antagonist was efficient when administered into the ventromedial nucleus, suggesting that this might be an important structure for vocalization in rats. This notion is supported by the observation that even rather small lesions of this nucleus reduce vocalizations (Harding and McGinnis, 2005). If these observations were to be confirmed, we are facing an intriguing species difference between male rats and mice.

Ultrasonic vocalizations have also been studied in hamsters, voles and other rodents. I do not consider it necessary to exhaust either myself or the reader with a review of any of these other species. The purpose of the analysis of vocalizations can be attained with the already extensive discussion of mice and rats.

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