African four-striped grass mice (Rhabdomys pumilio), a diurnal-crepuscular muroid rodent,in the behavioral laboratory

African four-striped grass mice,Rhabdomys pumilio, are potentially valuable animals for laboratory studies of behavior. In nature, they live in the grasslands of much of Africa. In the laboratory, striped mice adapt well to a number of behavioral testing situations. Ten male grass mice tested in running wheels displayed a mean of approximately 10,000 revolutions per day, with a diurnal-crepuscular pattern characterized by sharp peaks near the time of light onset and offset and a generally greater level of wheel running in light than in darkness. The retinal anatomy of this species is characterized by a cone-like organization of the outer segment layer and unusual thickness of the inner plexiform layer, suggesting an unusual high amount of retinal data processing for a muroid rodent. The copulatory pattern ofR. pumilio is characterized by no lock, no intravaginal thrusting, multiple intromissions preceding ejaculation, and multiple ejaculations. The number of intromissions preceding the first ejaculation is unusually high, and postejaculatory intervals are unusually long. Grass mice display intermediate levels of open-field activity, but little climbing or digging.     

Effect of the interintromission interval on lordotic response and attack latency in golden hamsters (Mesocricetus auratus)

After 12-15 ejaculatory series, each consisting of several short intromissions (2- to 3-s vaginal penetration) and an ejaculation, male golden hamsters adopt an altered copulatory pattern consisting of long intromissions (5- to 25-s penetration with intravaginal thrusting). Receptivity declines and the tendency for the female to attack the male increases at about the time of this shift in copulatory pattern. Because the mean interintromission interval (III) between short intromissions is about 8 s compared to 100 s between long intromissions, it is possible that females detect this difference and adjust their mating accordingly. When the III between short intromissions from a rested male was experimentally increased to 100 s by use of a halter and lead device, the duration of lordosis was significantly less than that displayed by females paired with control males (8-s III) and virtually the same as that displayed by females paired with males that produced only long intromissions. This suggests that the female uses the temporal patterning of intravaginal stimulation as one criterion for terminating mating with a particular male.     

Determinants of mating success in the golden hamster (Mesocricetus auratus): I. Male capacity

Rested adult golden hamsters produced a mean of 13 ejaculations and then showed a modified copulatory pattern consisting of long intromissions (10-30 s of intravaginal thrusting) during which no sperm transfer occurs. When a second (fresh) female was introduced, 58% of the males produced at least one more ejaculation, and 17% of the males produced one further ejaculation when placed with a third female. In similar three-female tests conducted 24 hr later, all males ejaculated (M = 4 ejaculations); this level of ejaculatory output was maintained over a subsequent 10-day period of daily testing. Four ejaculations ensured a nearly 100% pregnancy rate and maximum litter size in the first females. Second and third females, however, received fewer ejaculations and subsequently showed reduced fertility and produced smaller litters. Most males showed high levels of long intromissions on all days and with all females. The physiological significance of these long intromissions may be to trigger the progestational response. Examination of the rate of recovery from sexual exhaustion indicated that 2 or 8 hr of rest resulted in fewer than 50% of the males being capable of one further ejaculation. However, most of these single ejaculations were accompanied by long intromissions and resulted in successful pregnancies. Four to eight days were required for full recovery of ejaculatory capacity. This study showed that the male golden hamster has a higher ejaculatory output and more rapid recovery from sexual exhaustion than other small rodents that have been studied. Thus, the limits of male capacity appear to vary widely among species.     

Detailed analysis of the male copulatory motor pattern in mammals: hormonal bases

Data obtained, using a polygraphic technique, on the characteristics of the motor and genital copulatory responses of male rabbits, rats, mice, hamsters, and guinea pigs are reviewed. This methodology provided detailed information, not accessible to other analyses, on the frequency and dynamic organization of copulatory pelvic thrusting trains of the species studied. This comparative analysis showed that: (1) The male rat may display two types of ejaculatory responses, differing in the dynamic organization of the pelvic thrusting train, and in the duration of the intravaginal thrusting period preceding ejaculation. (2) In the guinea pigs and small rodents, but not in rabbits, pelvic thrusting at ejaculatory responses persists during intromission, and a period of fast intravaginal thrusting is associated with ejaculation. (3) The motor copulatory pattern of the rabbit, but not of the rat, hamster, or guinea pig, is affected by castration and hormone treatment, suggesting that, in rabbits, androgen acts both on motivation and on the spinal neural systems related to copulation.     

Interaction between penile reflexes and copulation in male rats

Intact, unanesthetized male rats were place in a supine position, with the penile sheath continuously retracted. Three forms of penile reflex were displayed: erections, cups, and flips. The reciprocal relation between copulation and the penile reflexes occurring in supine tests was explored in four experiments. In Experiment 1, sexual exhaustion depressed all penile reflexes, but the reflexes returned to baseline levels within 8 hr, long before copulatory potential. In Experiment 2, reflexes were depressed to exhaustion levels after fewer ejaculations than were required for sexual exhaustion, an indication that reflexes are more readily evoked during copulation than in supine tests. Experiment 3 determined that a rat's penile-reflex potential may be enhanced by placing the rat in a copulation-test cage, by allowing the male a few antecedent intromissions, or by allowing an antecedent ejaculation. The display of penile reflexes within 1 min after ejaculation suggests that the period of reduced sexual arousability following ejaculation is not due to reduced excitability in the spinal mechanisms controlling penile reflexes. In Experiment 4, 1 hr of penile-reflex elicitation had no effect on subsequent copulatory behavior. Thus, sexual stimulation may increase or decrease penile-reflex potential, but a reciprocal influence was not detectable.     

A comparative study of rodent ultrasonic vocalizations during copulation

The temporal patterning of ultrasonic vocalizations (USVs) during copulation was recorded for male-female pairs of Djungarian hamsters (Phodopus campbelli), prairie voles (Microtus ochrogaster), and montane voles (Microtus montanus). Each species appears to utilize a single major frequency band for USVs, centered around 31 kHz for the vole species and 71 kHz for hamsters. Djungarian hamsters exhibited low rates of USVs prior to introduction of the female and following ejaculation, but a high USV rate during periods of copulatory activity. Both vole species called at high rates during all stages of the copulatory sequence, although calling rates decreased following ejaculation. Anesthetization trials, where one pair member was awake and the other anesthesized, suggest that it is the male of each species that produces most USVs. The results were compared with six other muroid species for which data on the temporal patterning of USVs during copulation are available. These data extend our knowledge of the patterning of USVs during copulatory behavior and suggest the need for additional comparative investigations.     

INTROMISSION FREQUENCY AND INTROMISSION DURATION IN THE MALE RAT MATING BEHAVIOR

C arlsson , S. G. & L arsson , K. Intromission frequency and intromission duration in the male rat mating behavior. Scand, J. Psychol ., 1962, 3 , 189–191.—The male rat attains ejaculation after repeatedly mounting and penetrating the receptive female. By artificially prolonging the intervals of rest separating the intromissions the male is made to ejaculate after fewer intromissions than occurs when he copulates ad libitum . It was found that the reduction in intromission frequency was accompanied by an increase in intromission duration.     

Copulation and intermale aggression in rats

Attack behavior of reliably aggressive male Long-Evans rats against unfamiliar male intruders was observed immediately following copulation to one or more ejaculations. Compulatory series to five ejaculations did not differ from copulation to a single ejaculation or from a noncopulatory control in affecting aggressive behavior. Repetitive biting attacks occurred in all conditions, with comparable wounding. Evidently, the male postejaculatory state of insensitivity to sexual stimuli does not extend to stimuli eliciting intermale aggression. A second experiment determined the attack-eliciting capacity of foreign males placed in the home cage of an actively copulating male. As intromissions increased and the interval to ejaculation decreased, the probability of intermale aggression and interruption of copulation diminished. The results are discussed in reference to sexual and aggressive strategies of the copulating male.     

Life-span changes in the copulatory behavior of male rats (Rattus norvegicus)

The copulatory behavior of 5-, 10-, 15-, and 20-month-old sexually naive male rats (Long-Evans) was studied during 2-hr tests with receptive females. There was no apparent change in sexual arousal as measured by latency to initiate copulation across age, with subjects from all groups exhibiting comparable latencies to first mount and first mount with intromission. The numbers of ejaculations achieved were also similar across ages. Significant age differences were found for frequency of mounts, with 20-month-olds having the highest mean frequency. The persistent mounting by older males appeared to account for significant group differences in interintromission interval and ejaculation latency. It is suggested that motor deficits may impair the ability of older males to achieve intromission, increasing the number of mount bouts as well as the number of mounts per bout, thus extending the length of each copulatory series.     

Effects of vagino-cervical stimulation upon sociosexual behaviors in female rats

The role of vagino-cervical stimulation in the control of feminine copulatory behavior in the behaviorally estrous rat was examined in a complex environment that allowed the test female to pace her contacts with sexually active males, sexually passive males and ovariectomized females. Manipulations of vagino-cervical stimulation by administration of a topical anesthetic or by probing with a glass rod, immediately before testing in the complex environment, did not significantly alter any aspect of behavior in behaviorally estrous females. Transection of the pelvic nerve increased the number of intromissions and ejaculations that the females received and increased the amount of time that the females spent with the sexually active males. The present results implicate the pelvic nerve in the modulation of motivation for coital contacts in the female rat.     

Sexual exhaustion and recovery in the male rat

Twelve male rats were left with receptive females and allowed to copulate and ejaculate until they reached a criterion of “sexual exhaustion” They were then retested after 1, 3, 6 and 15 days of sexual inactivity. Following these observations males were tested once each day or once every other day and allowed to achieve a single ejaculation.

In the course of a period of unlimited access to the receptive female males usually need approximately 10 intromissions to produce the initial ejaculation, but successive ejaculations are produced by fewer and fewer intromissions. The time to recover from the effects of an ejaculation increases progressively as exhaustion is approached.

Very few animals copulate when tested 24 hours after sexual exhaustion. Considerably more recovery is evident in tests conducted after a 3-day rest, but it is not complete and rats are not capable of achieving as many ejaculations as they tend to achieve after longer periods of inactivity. As measured by ejaculation-frequency, the curve of sexual recovery is negatively accelerated and probably reaches asymptote after 7 to 10 days of rest.

Various other measures in addition to ejaculation-frequency support this conclusion. Males allowed to ejaculate once each day or every other day are somewhat less responsive than fully rested animals, but do not show any progressive loss in sexual excitability or capacity.

A working hypothesis is proposed to explain most of the findings. It postulates the existence of an Arousal Mechanism which is distinct from a Copulatory Mechanism. The ways in which these hypothetical mechanisms are affected by sexual performance and sexual rest arc discussed.     

Organization of mating behavior in male hamsters (Mesocricetus auratus)

Factor analysis was applied to standard measures of sexual behavior in 73 male hamsters (Mesocricetus auratus) as they interacted with hormone-primed females. The results suggest that 5 factors, or conceptual mechanisms, function in the organization of the behaviors observed in the first 2 copulatory series. Of these, the 3 that relate to the behaviors in the first copulatory series were compared to those emerging from prior analyses of other rodents. These comparisons revealed similarities and differences in factor structure across species. Whereas all of these analyses identify factors related to the initiation and efficiency of copulatory behavior, hamsters seem to differ from other species in the measures that best define these factors. In addition, the copulatory rate factor that has been prominent in previous analyses of rats seems to be absent in hamsters. These results suggest that male sexual behavior in hamsters is organized differently from that in other rodents. In more general terms, they suggest that even species with generally similar copulatory patterns can show significant differences in behavioral organization, in turn suggesting the need for additional factor analytic studies to better establish the extent of these species differences.     

The DBA/1Bg and DBA/2Bg Y chromosomes compared for their effects on male sexual behavior

Mount, intromission, and ejaculation number and latency were measured in male mice of the DBA/1Bg, DBA/2Bg, and DBA/2.DBA/1-YBg congenic strains. The DBA/2 and DBA/2.DBA/1-Y congenic strains differ in the source of their Y chromosome. Fifty percent of the DBA/2 and 13 percent of the DBA/2.DBA/1-Y males mounted at least once in the test of male copulatory behavior. There were no other significant differences between these two congenic strains. This finding suggests that the Y chromosome has an effect on the proportion of mice that mount in this test.     

Effects of female odors on the sexual behavior of male hamsters

A series of experiments was undertaken to investigate the effects of removal of several scent glands and scent-producing organs of female hamsters on the copulatory performance of male hamsters. In the first experiment it was shown that males engage in less copulatory activity toward females lacking vaginal secretions than toward females with these odors. Eliminating visual cues by observing pairs under infrared illumination did not change the performance of males toward these two kinds of females. The results of Experiment 2 indicated the importance of flank, ear, and Harderian glands as well as vaginal secretions--males showed the highest levels of copulatory behavior toward females with a full complement of odors and the lowest levels toward those lacking three of four sources of scent. Similar results were obtained in the third experiment in which anesthetized females were used as stimulus animals to increase the importance of chemical cues and to reduce variability due to the behavior of females. The sexual behavior of males was greatest toward females with all sources of scent present, lower toward those lacking vaginal secretions, and still lower toward those lacking vaginal secretions and other sources of odors. In the fourth experiment we asked whether any one of the nonvaginal scent glands was particularly important in stimulating male sexual behavior, but we found no differences in male performance toward females that lacked vaginal secretions or that in addition lacked one of the other scent glands. In the fifth experiment males displayed higher levels of sexual behavior toward vaginectomized females than toward vaginectomized females that had been deodorized by a cleaning procedure, again indicating the importance of nonvaginal odors in stimulating copulatory performance. Thus these experiments demonstrate the importance of vaginal secretions in the sexual arousal of male hamsters, a role for nonvaginal odors in sexual arousal of males, and the lack of necessity of these odors for male copulatory behavior. These results have implications for theories of olfactory communication in mammals and for interpretations of experiments in which lesions of the olfactory system lead to deficits in male copulatory performance.     

Facilitation of the effect testosterone on male sexual behavior in rats deprived of REM sleep

The possibility of rapid eye movement sleep deprivation (REMd) altering the effect of testosterone on masculine sexual behavior was investigated. Adult castrated male Wistar rats with no sexual experience were randomly assigned to the following three groups: REMd (using the water tank technique) for 7 days, large platform control for 7 days, and undisturbed sleep control. All subjects were treated with 1 mg testosterone propionate daily for 14 days. Masculine sexual behavior was assessed 3 consecutive days prior to steroid administration and was evaluated daily during the treatment. Frequencies and latencies of mounts, intromissions, and ejaculations, as well as the postejaculatory refractory period were recorded. One hundred percent of the REMd subjects presented mounts, intromissions, and ejaculations sooner than the control group. In almost all parameters, a clear facilitation of sexual activity was observed in the REMd group.     

Conditioning of appetitive and consummatory sexual behavior in male Japanese quail.

Two different types of stimulus objects, a live female quail artificially adorned with bright orange feathers and an inanimate toy dog, served as conditioned stimuli. For subjects in experimental groups, the conditioned stimuli were presented shortly before access to a sexually receptive normal female quail. For subjects in control groups, exposure to the conditioned stimuli was unpaired with copulatory opportunity. Subjects in the experimental but not in the control groups quickly came to approach the location of the conditioned stimulus objects. When an adorned female quail served as the conditioned stimulus, the conditioned approach behavior was controlled by a combination of the presence of the orange adornments and the visual cues of the head and neck of the female bird, and the approach behavior persisted as the adorned female moved to new locations. When the toy dog served as the conditioned stimulus, the conditioned approach behavior was limited to the spatial cues that surrounded the toy dog during conditioning trials. Although both types of stimulus objects evoked conditioned approach behavior, only the adorned female stimulus supported copulatory behavior. This last finding indicates that copulatory behavior can become redirected toward novel stimuli as a result of conditioning, but only under special circumstances. The results are consistent with the suggestion that appetitive components of reproductive behavior are more susceptible to conditioning than consummatory components. Possible reasons for this are discussed, together with implications of the results for the contribution of conditioning processes to sexual selection.     

Penile responses of rats (Rattus norvegicus) in extended ex copula tests

Prolonged tests of rats' penile responses outside the context of copulation (ex copula) were undertaken to facilitate analysis of these penile components of copulatory behavior. Penile erections and flips were evoked for 1 hr following penile sheath retraction (SR), and rats were retested for 30 min after a rest interval of 5 min to 4 hr. The number of penile responses declined sharply over the course of the hour. Following a 5-min rest, there was little likelihood of additional responses. Within 2 hr some measures of penile response potential approached their original high asymptotes; other measures were still depressed after 4-hr rest. In control tests, the penile sheath was unretracted (SU) during the first 60 min, and hence few or no penile responses occurred. This condition caused no reduction in the number of erections and flips in the subsequent 30-min SR test; hence the reduction in response potential during and after SR tests was due to the responses displayed, not to the conditions of restraint. Ejaculation occurred frequently in the SU condition but rarely in SR tests, results suggesting that sheath retraction may normally inhibit ejaculation in ex copula tests, and perhaps during copulation as well.     

Contextual conditioning and the control of copulatory behavior by species-specific sign stimuli in male Japanese quail

Three experiments were conducted to identify species-specific sign stimuli sufficient to elicit copulatory behavior in male Japanese quail and to determine how learning is involved in the control of behavior by these sign stimuli. In Experiment 1, sexually experienced subjects were tested for copulatory behavior with a live female quail and with a model consisting of a female quail's head and neck mounted in front of a foam pad. Comparable levels of copulatory behavior were observed in the two tests, indicating that static visual cues provided by a female quail's head and neck are sufficient to elicit copulatory behavior in this species. Experiment 2 showed that male birds that previously received numerous opportunities to copulate with a live female quail in the test situation were significantly more likely to copulate with the head + neck model than were sexually inexperienced subjects. Experiment 3 showed that prior sexual experience with live quail facilitated responding to the head + neck model only if the sexual experience was provided in the same place where subjects were later tested with the model. This last finding suggests that sexual experience facilitates control of copulatory behavior by species-specific sign stimuli through contextual conditioning. Contextual conditioning may lower the threshold for sexual behavior with the result that a stimulus as impoverished as an immobile model containing only the head and neck of a female quail becomes sufficient to elicit normal levels of copulatory behavior. The results are also discussed as an example of conditioned stimulus facilitation of responding to an unconditioned stimulus.     

Relative contributions of the male and the female to sexual behavior and reproductive success in the Japanese quail (Coturnix japonica)

Two contrasting investigative techniques provided evidence consistent with the interpretation that female quail (Coturnix japonica) regulate male copulatory behavior by the duration of their immobility and through this behavioral mechanism they also control the rate of fertilization of their eggs. In Experiment 1, copulation tests with males and females from different genetic lines showed that the type of female that participated in a copulatory test significantly influenced the latency of the male's grab, mount, and cloacal contact responses and also determined the efficiency of the male's copulatory behavior. These measures of male performance were correlated with female immobility in Experiment 2, which used a more homogeneous population of quail. Furthermore, 2 of these measures (copulatory efficiency and the latency to make cloacal contact) were correlated with fertilization rate.     

Suppression of precocial copulation by progesterone implants in the male chick forebrain.

Precocial copulation in 2-wk.-old male chicks, described behaviorally as free mount, tread, posterior contact, waggle, peek, and seize, was developed through hand-training experience and androgen treatment. Crystalline progesterone was then implanted in various forebrain or midbrain regions. Results indicated that progesterone inhibited copulatory behavior when placed in the periventricular areas of the preoptic-hypothalamic continuum. Progesterone implants in the preoptic lateral forebrain bundle regions also suppressed precocial copulation. Forebrain implants of cholesterol did not result in copulatory inhibition. The suppression of copulatory behavior was not accompanied by loss of weight or deficits in general activity or comb growth. These data indicate that brain regions responsible for progesterone-induced copulatory inhibition are similar in neuroanatomical distribution to those involved in testosterone-induced copulatory activation.