Detailed Analysis of the Male Copulatory Motor Pattern in Mammals: Hormonal Bases

Scandinavian Journal of Psychology, 2003, 44, 279–288

DetailedBlackwell Publishing Ltd analysis of the male copulatory motor pattern in mammals: Hormonal bases

GABRIELA MORALÍ, MARÍA ASUNCIÓN PÍA SOTO, JOSÉ LUIS CONTRERAS, MARCELA ARTEAGA, MARÍA DOLORES GONZÁLEZ-VIDAL and CARLOS BEYER Unidad de Investigación Médica en Farmacología, Centro Médico Nacional Siglo XXI, IMSS, Mexico, División CBS, Universidad Autónoma Metropolitana, Mexico, Centro de Investigación en Reproducción Animal, CINVESTAV-UAT, Ixtacuixtla, Tlaxcala, Mexico

Moralí, G., Soto, M. A. P., Contreras, J. L., Arteaga M., González-Vidal M. D., and Beyer C. (2003). Detailed analysis of the male copulatory motor pattern in mammals: Hormonal bases. Scandinavian Journal of Psychology, 44, 279–288. 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. Key words: Sexual behavior, polygraphic analysis, motor copulatory pattern, pelvic thrusting. Gabriela Moralí, Unidad de Investigación Médica en Farmacología, Coord. Invest. Salud IMSS, Coahuila 5 Col. Roma, PO Box A-047, Mexico 06703 DF, Mexico. E-mail: [email protected]

Sexual behavior in mammals involves the participation of an the vagina. The internal genital component comprises the arousal mechanism that drives the individual to the search contractile autonomic and somatic activities of the various for and onset of sexual interaction with a partner, and a organs involved in seminal emission and ejaculation. A full consummatory mechanism that allows the individual to understanding of the functional signiﬁcance of copulatory perform this interaction (Beach, 1967). A modulatory behavior requires precise information on the interactions mechanism may act on motivation and performance, by between these three components. inhibiting the expression of sexual behavior under some Knut Larsson has been one of the pioneers in exploring circumstances (Beyer, 1974). several of the factors determining the expression of mascu- Extensive literature has been devoted to the general line sexual behavior of the laboratory rat, and in describing description of sexual behavior patterns; data on their incid- some general and detailed characteristics of the copulatory ence and temporal course allow an evaluation of arousal behavioral patterns (Larsson, 1956, 1959, 1963, 1969, 1979; and performance in terms of endocrine, neural, ontogenetic, Carlsson & Larsson, 1962). In several of his valuable social, and environmental factors involved in the expression and fruitful visits to our laboratory in Mexico City in the of this behavior. However, there have been few studies of the early 1980s, he directed his interest, among many other “morphology” of the various behavioral patterns involved areas of research, to an innovative, reliable methodology in copulation. developed and implemented by some of us (Carlos Beyer, Male copulation in mammals includes the activation of José Miguel Cervantes, José Luis Contreras, and Javier three interacting components: a motor component, an external Almanza), and followed by us and our students. This genital component, and an internal genital component methodology provides objective and detailed images of (Moralí & Beyer, 1992). The motor component typically signals generated in relation to copulatory pelvic thrusting, involves those muscles that allow the male to climb, clasp, and allows an analysis of some of its dynamic aspects and mount its partner, and to execute the copulatory rhythmic (rhythmicity and vigor) and its temporal relation to penile– pelvic thrusting movements against the female’s rump that vaginal contacts and to seminal vesicle pressure. The applica- either induce or intensify the adoption of the receptive tion of this methodology in rabbits, rats, mice, hamsters, posture by the female and that facilitate intravaginal penile and guinea pigs has been, since then, a subject of interest in insertion and, eventually, ejaculation. The external genital our laboratory, as have the effects on these phenomena of component involves the penile vascular and muscular some hormonal and pharmacological manipulations. The responses involved in penile erection and insertion into collaborative work with Knut led to some of the results

280 G. Moralí et al. Scand J Psychol 44 (2003) presented here, as well as a close academic and personal relationship with him.

METHODS FOR THE ANALYSIS OF THE MOTOR AND GENITAL COMPONENTS OF MALE SEXUAL BEHAVIOR Several techniques, including high-speed cinematography (Bermant, 1965; Stone & Ferguson, 1940) and videotape recording (Sachs & Barfield, 1976) with subsequent analysis in slow motion, have been used to quantitatively describe the motor components of male sexual behavior. However, these techniques do not give quantitative information on the Fig. 1. Polygraphic records of three consecutive copulations of a dynamic aspects of copulatory movements, such as their male rabbit. Upper tracings, marked T, time signal and marks vigor and rhythmicity. introduced by an observer when intromission occurred. Middle The “accelerometric” technique developed at our laborat- tracings, marked PM, frequency and characteristics of pelvic movements recorded with an accelerometer. Each intromission ory has allowed the precise quantification of some motor was preceded by a variable period of mounting. Lower tracings, aspects of copulatory activity, initially of rabbits (Contreras marked SVP, seminal vesicle pressure. Note that pelvic thrusting is & Beyer, 1979; Beyer et al., 1980; Soto et al., 1984) and rats not associated with SVP changes, and that 100–300 ms after the (Beyer et al., 1981, 1982; Moralí et al., 1983, 1985), and then onset of intromission a gradual contraction of the seminal vesicles of mice (Wang et al., 1989), hamsters (Arteaga & Moralí, occurred, which outlasted copulation. Modified from Contreras & Beyer (1979). 1997), and guinea pigs (Moralí, González-Vidal & Cervantes, submitted). With this technique, the accurate measurement of several parameters of the male copulatory motor pattern a determination of the moment during insertion when is achieved by placing an acceleration transducer on the ejaculation occurs. male’s back. In relation to the rapid acceleration changes By using a similar device, it has been possible to combine that occur during the forward–backward displacements of the accelerometric technique with the detection of genital the male’s pelvis at copulation, the accelerometer generates contacts during the copulatory activity displayed by rats electrical signals that can be easily recorded on a polygraph (Moralí et al., 1983; Moralí & Beyer, 1992), hamsters or on an oscilloscope (Fig. 1). (Arteaga & Moralí, 1997), and guinea pigs (Moralí, The accelerometric technique allows the precise measure- González-Vidal & Cervantes, submitted). This methodology ment of the following parameters: (1) duration of individual has allowed us to obtain information on the precise timing pelvic thrusts; (2) frequency of pelvic thrusting, that is, of penile insertion in relation to pelvic thrusting, to deter- number of pelvic thrusts per second; (3) acceleration or mine the occurrence of fast pelvic thrusting during penile vigor of pelvic movements, represented by the amplitude insertion at ejaculation, and, by showing the moment during of the signals; and (4) duration of mounting trains, that is, insertion when ejaculation occurs, to ascertain the exact the uninterrupted series of pelvic thrusts. When combined duration of the period of penile stimulation required for the with power spectrum analysis, this technique also gives male to ejaculate (Figs. 3, 4, and 5). information on the periodicity or rhythmicity of pelvic There is little information on the complex interactions thrusting (Fig. 2). As can be seen, for a selected range of between the copulatory movements and the activity of the frequencies (1–50 Hz), a spectrum is provided whose peak genital organs, controlled by autonomic organs, Information and dispersion give an estimation of the periodicity of the about the activity of the internal genitalia, essential for a thrusting train. precise timing of the occurrence and duration of seminal Pierce and Nuttall (1961) and Rubin and Azrin (1967) emission and ejaculation, has been obtained by chronically designed an electric circuit that can be connected by sub- implanting a catheter in the seminal vesicles. Changes in cutaneous electrodes to a male and a female individual, tone or contractions of these organs result in alterations in and that is closed when moist contact between the penis pressure that are continuously recorded with a polygraph and the vagina of the copulating pair is established. The use linked to a pressure transducer (Figs. 1 and 3). of this device permitted these authors to determine the Therefore, through the use of the polygraphic methodology precise duration of penile insertions during intromission described above, and in combination with observational and ejaculatory patterns in the rat (Pierce & Nuttall, 1961; techniques, it is possible not only to quantitatively analyze Carlsson & Larsson, 1962) and in the rabbit (Rubin & the male copulatory motor pattern and to recognize subtle Azrin, 1967). This technique, however, does not provide differences between and within species, but also to relate information about the copulatory motor activities them- these events to penile–vaginal interactions and reflex selves. Furthermore, this technique alone does not allow responses of the male ejaculatory apparatus.

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Fig. 2. Accelerometic records and frequency spectrum analysis graphs of pelvic movements in typical mounts displayed by intact male and female rabbits, and by ovariectomized (ovx) rabbits receiving estradiol benzoate (EB) or testosterone propionate (TP) treatments. Upper graphs: signals generated by the accelerometer during mounting. Lower graphs: frequency analysis (range 1–50 Hz) of the signals generated during an 8 s period in which mounting occurred. The frequency analysis of the male mount shows a single component with a peak frequency value (F) of 14.875 Hz, as indicated by the cursor. In contrast, that of the female mount does not show a dominant frequency but a series of ill defined components. Note sharp, single components in the spectra of the EB-treated, ovariectomized rabbits, showing also high thrusting frequencies (F = 21.00 and 17.625 Hz). Frequency analysis of TP-stimulated mounts reveals two patterns: one with a well defined component (F = 12.500), and the other showing both a dominant frequency (F = 16.00) and an ill defined band of higher frequencies. Modified from Soto et al. (1984).

DESCRIPTION OF THE MASCULINE COPULATORY periodic until penile insertion occurs, at which moment MOTOR PATTERN OF THE RABBIT, RAT, they are interrupted (Fig. 1). Effective mounts, that is, HAMSTER, GUINEA PIG, AND MOUSE those culminating in intromission and ejaculation, tend to be shorter than ineffective mounts and are more regular and Rabbit rhythmic than ineffective ones, as evidenced by frequency Copulation in rabbits involves the display of mounts with spectrum analysis. Similarly, effective mounts show slightly rhythmic, vigorous pelvic thrusts performed for several but signiﬁcantly higher thrusting frequencies than ineffective seconds against the female’s rump, and that may or may not ones (Table 1). This suggests that the adequate stimulus culminate in intravaginal penile insertion. At intromission, for inducing the lordosis posture in the doe is a rhythmic, ejaculation invariably occurs. The dynamic characteristics “high”-frequency pelvic thrusting. of pelvic thrusting have been described in detail by using During pelvic thrusting, no changes in the seminal vesicle the accelerometric technique (Contreras & Beyer, 1979). The pressure are observed in rabbits. However, shortly after pelvic thrusts (around 14 per second) are highly regular and penile insertion, a slow rise in pressure, outlasting copulation,

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Fig. 4. Polygraphic records of signals generated by the accelerometer in relation to the pelvic thrusting (PT) movements of male hamsters during mount, intromission, ejaculation, and long intromission behavioral patterns, and by the intromission detection circuit indicating the occurrence and duration of genital contacts (GC) associated with penile insertion during these responses. Penile insertion is related to intromission responses, to the interruption of rhythmic pelvic thrusting and, at ejaculations, to a deﬁned period of intravaginal thrusting. Long intromissions are characterized by prolonged periods of penile insertion during which the male displays slow intravaginal thrusting (2 thrusts/s). Modiﬁed from Arteaga & Moralí (1997).

male copulation, and appears to be similar to it. However, using the accelerometric technique, clear sexual differences in the vigor, frequency, and periodicity of pelvic thrusting displayed by mounting male and female rabbits have been found (Soto et al., 1984) (Fig. 2). Frequency spectrum analysis Fig. 3. Polygraphic recordings of changes in seminal vesicle pressure (SVP), of the signals generated by the accelerometer in relation to of the signals generated by the accelerometer typically pelvic thrusting movements (PT) of intact male rats during a typical show a single peak around the 14 Hz band, indicating the mount, intromission, and ejaculation behavioral patterns, and of the rhythmical nature of thrusting in the male rabbit. Mounts occurrence and duration of the genital contacts (GC) during these displayed by females are shorter than those of males, comprise behavioral responses. Note the fusiform organization of the acceler- isolated pelvic movements of variable duration, and generate ometric record of the mounting train and the similar appearance of the intromission and ejaculation thrusting trains until penile inser- weak, irregular signals of lower amplitude. As shown in tion is achieved, as indicated by the dotted line and by the plateau Fig. 2, frequency spectrum analysis of female pelvic thrusting signal generated by the intromission detection circuit and recorded failed to reveal clear rhythmicity in female mounts. in the polygraph. Note a small broad rise in SVP during the mount In spite of this sexual difference, female rabbits seem to and the sharp increase coinciding with penile insertion. Two types possess the neural circuitry involved in the display of of ejaculatory patterns can be recognized: short and long ejaculations, differing in the duration and dynamic organization of the rhythmic thrusting, but lack the adequate hormonal levels pelvic thrusting train, and in the duration of the period of intravag- to activate this system. Thus, as shown in Fig. 2, testosterone inal thrusting that precedes ejaculation, and that is revealed by this propionate (TP)-treated female rabbits not only display combined methodology. Note that the SVP rises during penile inser- vigorous pelvic thrusting in many cases but also clear tion and intravaginal thrusting in ejaculation responses, culminating rhythmicity, with frequencies similar to those of intact males. in a further steep rise associated with seminal emission and remain- ing above the baseline for several seconds. Modiﬁed from Beyer et Most interestingly, estrogen treatment (estradiol benzoate, al. (1982) and Moralí & Beyer (1992). EB) induced highly synchronic thrusting activity, of higher frequency than that of normal or androgen-treated males. is recorded and ejaculation occurs with a brief latency after intromission is achieved (Contreras & Beyer, 1979) (Fig. 1). Laboratory rat Male-like sexual behavior (pseudomale behavior) may be The polygraphic analysis of mounts, intromission responses, shown by female rabbits that includes all the components of and ejaculation responses of male rats reveals their ﬁne

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Fig. 5. Polygraphic records of the signals generated by the accelerometer in relation to the pelvic thrusting movements performed during typical mount, intromission, and ejaculation behavioral responses of a guinea pig and an ejaculation response of a mouse, and the plateau signals generated by the intromission detection circuit when genital contact occurred in relation to penile insertion during the behavioral responses of the guinea pig. In both species, fast pelvic thrusting occurring before penile insertion shifts during insertion to a slow pattern that lasts for 20 s or more in the mouse, and that is followed by a characteristic period of intravaginal fast thrusting associated with ejaculation. dynamic organization. As can be seen from the accelero- but it is followed by a steep rise coinciding with penile metric tracings of Fig. 3, mounts consist of a series of 6–12 insertion (Beyer et al., 1982). pelvic thrusts of similar duration but variable amplitude, Pelvic thrusting trains at the ejaculatory behavioral giving the mounting train a fusiform appearance (Beyer responses are longer than those of mounts and intromis- et al., 1981). When using the intromission detection circuit, sions. The accelerometric technique has shown that rats may it can be seen that, at mounts, no (or only occasional) brief exhibit two types of ejaculatory response, consisting of either contacts occur between the penis and the vagina of the a short (0.68 s as an average) or a long (1.04 s as an average) receptive female (Moralí et al., 1983; Moralí & Beyer, 1992). pelvic thrusting train (Beyer et al., 1981, 1982; Moralí & When seminal vesicle pressure (SVP) recordings are also Beyer, 1992) (Fig. 3). A period of intravaginal pelvic thrust- made, a slight rise in SVP may be found at mounts as a ing, which had not been previously demonstrated by other single wave in association with pelvic thrusting (Beyer et al., techniques, occurs at both ejaculatory responses. Besides 1982). their duration, long ejaculations differ from short ones in Pelvic thrusting trains at intromission consist of only 4–7 showing clearly identiﬁable extra- and intravaginal thrusting rhythmic thrusts, being shorter than at mounts (Fig. 3; trains; in short ejaculations, extra- and intravaginal thrust- Table 1). They are indistinguishable from mounts in their ing proceeds in immediate succession as a single phase of initial part, but differ in showing a ﬁnal period of irregular gradually increasing amplitude, which culminates in a series broad signals coinciding with penile insertion and withdrawal. of irregular pelvic movements associated with seminal Penile insertion results in the interruption of thrusting and emission and ejaculation. lasts for 410 ± 150 ms (mean ± SD) (Moralí et al., 1983; As in the case of mounting and intromission responses, a Moralí & Beyer, 1992). As in mounts, a slight rise in SVP smooth, gradual rise in SVP occurs during the initiation of occurs during pelvic thrusting at the intromission responses, mounting in the ejaculatory responses, followed by a change

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Table 1. Characteristics of the motor and genital copulatory responses displayed by male rabbits, rats, hamsters, mice, and guinea pigs (means ± SD).

Extravaginal train Intravaginal train

Species Mount Intromission/ejaculation* Slow Fast

Duration of the pelvic thrusting train (s) Rabbit1 3.08 ± 2.16 2.61 ± 1.50 – – Rat2 0.38 ± 0.08b 0.31 ± 0.07a Short: 0.37 ± 0.09ab – 0.31 ± 0.07a Long: 0.50 ± 0.06c – 0.54 ± 0.06c Hamster3 1.28 ± 0.15c 0.87 ± 0.10b 6 to 25 0.45 ± 0.03a Mouse4 0.60 to 3.60 up to 40 2.00 Guinea pig5 1.18 ± 0.07b 0.54 ± 0.05a 1.44 ± 0.12 1.14 ± 0.05b

Frequency of pelvic thrusting (movements/s) Rabbit1 12.08 ± 0.98a 13.54 ± 1.11b –– Rat2 20.95 ± 0.82 21.22 ± 1.33 – 22.00 Hamster3 14.78 ± 0.28a 15.20 ± 0.30ab 2.31 16.40 ± 0.41b Mouse4 22.00 to 25.00 2.24 22.00 Guinea pig5 11.27 ± 0.18a 11.88 ± 0.25ab 1.50 12.34 ± 0.23b

Ejaculation responses

Intromission responses To ejaculation Total contact Duration of the genital contact (s) Rabbit1 0.72 ± 0.27 0.72 ± 0.27 0.72 ± 0.27 Rat6 0.41 ± 0.15a Short: 0.306 ± 0.08a 1.136 ± 0.22c Long: 0.542 ± 0.08b 1.452 ± 0.33d Hamster4 2.21 ± 0.16b 1.25 ± 0.08a 3.15 ± 0.10b Guinea pig5 1.44 ± 0.12ª 2.54 ± 0.08b 3.82 ± 0.34c

* When no differences between intromission and ejaculation exist, data are pooled together. Data taken from: 1Contreras & Beyer (1979); 2Beyer et al. (1981, 1982); 3Arteaga & Moralí (1997); 4Wang et al. (1989) and Moralí & Sachs (unpublished results); 5Moralí, González-Vidal & Cervantes (submitted); 6Moralí & Beyer (1992) and Moralí, Contreras & Beyer (unpublished results). Different letters indicate significant differences ( p < 0.05) within a row, Tukey tests. in the slope of the curve associated with penile insertion. treatments (see Baum, 1979; Meisel & Sachs, 1994, for After a variable period of intravaginal thrusting, a further reviews), female rats can display the ejaculatory pattern. steep rise in SVP takes place and then declines just prior Great similarity has been found in the temporal organization to the end of the ejaculatory pattern. This last phasic rise and even in the vigor of the mounting and intromission associated with seminal emission lasts approximately 100 ms. motor patterns of female and male rats (Moralí et al., 1985). Thereafter, the SVP falls to its previous level, and remains Power spectrum analysis of the frequency of the signals above the baseline for several seconds (Fig. 3). generated during mount and intromission responses of From these recordings, it can be seen that a more abrupt intact female and male rats showed similar values (19–22 Hz) rise in SVP occurs during short than during long ejaculation in both sexes, as well as similar rhythmicity and periodicity. responses, leading to ejaculation after a significantly shorter The only significant difference between the sexes was a period of genital contact (0.31 vs. 0.54 s) (Table 1) (Moralí, longer duration of females’ mounts. The ejaculatory Contreras & Beyer, manuscript in preparation). The factors responses of neonatally androgenized females recorded at determining the occurrence of short and long ejaculatory adulthood, without any additional hormonal treatment, patterns have not been elucidated yet. However, hormonal were similar to the long ejaculatory pattern of male rats, with conditions, age, motivational state, and phenomena related the only difference being that the phase of low-amplitude to the sequential display of successive ejaculatory series seem thrusts, which normally coincides with penile insertion in to contribute to the occurrence of a short vs. a long ejaculatory males, was not evident in females. pattern (Moralí, Contreras & Beyer, unpublished results). Female rats display mount and intromission patterns similar to those of males (Beach, 1942). Moreover, under Golden hamster particular experimental circumstances, such as neonatal Male golden hamsters display four types of copulatory beha- androgenization, painful stimulation, or pharmacological vioral responses: mounts, intromissions, ejaculations, and

Scand J Psychol 44 (2003) Male copulatory motor pattern in mammals 285 long intromissions. These responses have been described in occurs (Fig. 5) (Table 1). This fast pelvic thrusting period is detail by Bunnell et al. (1976), who also assessed the dura- associated with ejaculation and usually occurs at a precise tion of the genital contacts at these responses. The poly- moment (2.5 s) after the onset of penile insertion. Thus, as graphic analysis of the copulatory responses of the male in hamsters and rats, the tactile stimulus required to trigger golden hamster has provided a precise quantitative estima- ejaculation is a period of intravaginal fast thrusting, whose tion of the duration of the thrusting trains, and of the characteristics seem to be highly predictable in this species. frequency, rhythmicity and vigor of pelvic thrusting, in tem- On the other hand, the duration of the genital contact after poral correlation with the genital contacts at copulation ejaculation may vary widely. (Arteaga & Moralí, 1997) (Fig. 4). As in rabbits and hamsters, effective mounts of guinea Series of rhythmic, synchronic extravaginal pelvic thrusts, pigs (those in which males achieve intromission) are shorter with frequencies between 14 and 15.5 thrusts/s are displayed than ineffective mounts and show higher thrusting fre- during the four types of copulatory responses. As in rabbits, quencies than ineffective ones. mounting trains are usually longer and have lower thrusting frequencies than those at intromission and ejaculation responses. The thrusting train at the intromission behavioral House mouse responses ends when penile insertion occurs. Penile insertion Similar to rats and hamsters, house mice display several at the intromission responses lasts for 2.2 s, on average. The mounts and intromissions preceding ejaculation and, depend- pelvic thrusting train at ejaculation ceases in relation to ing on the strain, may show multiple ejaculations or only penile insertion; however, after a brief period (50–100 ms), a one on a mating session (for a review, see Dewsbury, 1979). short train of intravaginal pelvic thrusting, generating signals Data on their motor copulatory pattern have been of lower amplitude, and higher frequency (16 thrusts/s) than obtained from a small number of animals (Wang et al., 1989). those of the extravaginal train, is resumed. This intravaginal Although these data do not yet allow a complete quantita- fast thrusting train, like that of rats, seems to be associated tive description of all parameters, clear accelerometric images with ejaculation. The duration of this period (0.45 s), varies have been obtained and pelvic thrusting frequencies have very little both between and within the individuals, and been determined (Fig. 5, Table 1). Mounts, characterized occurs at a precise moment after the onset of penile insertion. by the display of fast (22–25 thrusts/s) rhythmic thrusting After several ejaculatory series, when a male is approaching trains, may last for variable periods. If the male achieves sexual satiety, it presents “long” intromissions, in which penile insertion, fast thrusting shifts to a slow thrusting penile insertion is held for 30 s or more, while displaying pattern (2/s), as occurs in guinea pigs and in long intromis- intravaginal pelvic thrusting of slow frequency (around sions of hamsters. If the mouse loses penile insertion, fast 2 thrusts/s) (Bunnell et al., 1976). Extravaginal fast pelvic thrusting is resumed until insertion is achieved again. After thrusting trains at long intromissions are of similar fre- variable periods of intravaginal thrusting, lasting for several quency, rhythmicity and vigor as those of intromissions and seconds, males may either dismount or proceed to ejaculation. ejaculations, and, in response to penile insertion, shifts to At ejaculation responses, as in guinea pigs, after a preinser- slow intravaginal thrusting generating low-amplitude signals tion fast thrusting train and an intravaginal slow thrusting (Arteaga & Moralí, 1997) (Fig. 4). period, which in mice may last for 20 s or more, a remarkably characteristic, new period of fast thrusting of similar frequency to that of extravaginal thrusting, and presumably Guinea pig associated with ejaculation, is recorded (Fig. 5). After this The copulatory activity of the male guinea pig may involve period, the male may remain inserted for several seconds a variable number of mounts and intromission responses and then withdraw (Moralí & Sachs, unpublished results). preceding ejaculation, but, as with rabbits, guinea pigs are capable of ejaculating on a single insertion on at least some occasions (Dewsbury, 1979). The polygraphic analysis of Interspecies comparisons copulation of adult, Hartley albino male guinea pigs has Comparisons of the motor copulatory patterns of the species shown that, before penile insertion, intact animals show studied show that the duration and frequency of pelvic rhythmic pelvic thrusting trains with frequencies of 11–12 thrusting trains, as well as their dynamic organization, are thrusts/s (Moralí, González-Vidal and Cervantes, submitted). particular to each species. In rabbits, ejaculation occurs If penile insertion is achieved, fast pelvic thrusting ceases with a brief latency after the onset of intromission, in the and shifts to a slow pattern of about 1.5 thrusts may last absence of pelvic thrusting. In the other species, whether for several seconds. At the ejaculation behavioral responses, they display intravaginal slow thrusting (guinea pigs and after a brief period of slow thrusting performed during mice) or not (rats and hamsters), a remarkable period of insertion, a well deﬁned train of intravaginal fast pelvic intravaginal fast pelvic thrusting, of similar frequency to thrusting, generating signals of lower amplitude and slightly that of extravaginal thrusting, is performed in association higher frequency than those of preinsertion thrusting, with ejaculation.

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EFFECT OF HORMONES ON THE MASCULINE COPULATORY MOTOR PATTERN OF THE RABBIT, Rat RAT, HAMSTER AND GUINEA PIG Neither the thrusting frequency nor the amplitude or rhythmicity of pelvic thrusts in the copulatory responses Rabbit shown by male rats several weeks after surgery are significantly Rabbits may display mounts for several months after affected by castration (Beyer et al., 1981). Only the duration castration, but only a low proportion of these mounts of the mounting trains is somewhat longer in castrated rats culminate in ejaculation, mainly because of a decrease in (mean ± SD: 536 ± 20 ms vs. 380 ± 80 ms in intact rats). This the effectiveness of the mount to stimulate lordosis in the effect may result from some failure either of penile erection female (Stone, 1932; Beyer et al., 1980). The accelerometric or in the orientation of the penis to the vaginal region, as recordings of these mounts show periods of low-amplitude has also been described in cats, along with a lengthening of movements, and interthrust intervals that cause a decrease mounts, after castration (Rosenblatt & Aronson, 1958). in thrusting frequency and break the rhythm of thrusting Administration of TP reestablishes full copulatory beha- (Beyer et al., 1980) (Fig. 6). At a later stage in the disorgan- vior in castrated rats, with identical motor characteristics ization of the mounting pattern, pelvic thrusts disappear to those of intact rats (Beyer et al., 1981). Administration and the mounts are characterized by weak, tremor-like of estrogen (EB) to castrated rats stimulates the display of pelvic movements. These mounts never stimulate lordosis mount and intromission responses, and only few ejaculations in the receptive females. The changes in the copulatory corresponding to the short pattern (Fig. 7). Pelvic thrusting motor pattern following castration occurred earlier than was highly rhythmic in estrogen-treated male rats, and they the decrease in the number of mounts per test, suggesting showed intromission responses with thrusting frequencies that the motor parameters (thrusting frequency and significantly higher (mean ± SD: 22.15 ± 1.29 thrusts/s) than rhythm) are more sensitive to androgen deprivation than those of intact rats (19.43 ± 1.57 thrusts/s). is sexual motivation. Androgen administration (TP, 10 mg/ The lack of effects of castration on the frequency, rhyth- day for 15 days) to castrated rabbits gradually restores the micity and vigor of pelvic thrusting in male rats could indic- incidence of mounting but not of intromission to the ate that sex steroids do not modulate the copulatory motor intact level. Androgen administration also significantly pattern of the rat. However, it is also possible that rats stop increases thrusting frequency and strength of pelvic move- copulating before alterations in the copulatory motor pattern ments until the normal morphology of pelvic thrusting is are detected. The hormonal stimulation of the initiation of restored. male sexual behavior in the rat seems to be exerted in the medial preoptic area (mPOA) and anterior hypothalamic area. The copulatory motor pattern of long-term castrated rats whose sexual behavior was restored by local implants of TP in the mPOA was compared with that shown by the same individuals when intact (Moralí et al., 1985). The vigor, frequency, and temporal organization of the copulatory pelvic thrusting shown by the castrated, TP-implanted rats were similar to those previously shown by the rats when intact, even when, as revealed by the atrophy of the sexual accessory organs, it could be inferred that the spinal circuits involved in pelvic thrusting were also not exposed to significant amounts of circulating androgen. These data may indicate that the spinal neurons related to the organization of pelvic thrusting during copulation in the male rat can function without direct androgenic stimulation. Fig. 6. Accelerometric records of the first four mounts performed To investigate the possible role of early postnatal androgen by a New Zealand white rabbit when intact (I), and mounts performed in the organization of the copulatory motor pattern of the 30 days after castration (C), and 15 days after the initiation of rat, the copulatory responses of neonatally androgenized testosterone propionate administration (T). Upper tracings in each record carry a time mark (1 s) and a signal operated by the observer female rats and neonatally castrated male rats were compared when detecting intromission. Note the rhythmic characteristics of with those of control male and female rats before and after mounts of intact rabbits, of which the first three ended in intromis- treatment with either TP or EB (Moralí et al., 1985). The sion. Castration resulted in a diminution of the amplitude of the copulatory motor patterns of control and neonatally andro- signals and in the appearance of trains of small signals interspersed genized females, as well as those of neonatally castrated with periods of more vigorous activity. Note that testosterone administration tended to restore the normal mounting pattern in at male rats, were indistinguishable from those of control least some mounts (C and D). From Beyer et al. (1980), reproduced male rats (Moralí et al., 1985) (Fig. 7). Neonatally castrated with permission. rats treated with EB when adults never showed ejaculatory

Fig. 7. Accelerometric records of mount (M), intromission (I), and ejaculation (E) behavioral responses performed by control (postpubertally castrated), and neonatally castrated male rats, and by ovariectomized control, and neonatally androgenized female rats, under estradiol benzoate (EB) or testosterone propionate (TP) treatment. Note the similarity in the organization, frequency, and rhythmicity of pelvic thrusting trains in the four groups of rats under either treatment. Neonatally castrated rats did not ejaculate when treated with EB. Those receiving TP generally performed the short ejaculatory pattern, with similar characteristics to those of short ejaculations of control males. Control females did not show ejaculatory behavior. Neonatally androgenized females under EB treatment often showed the short-type ejaculatory pattern, whereas those under TP treatment generally displayed the long ejaculatory pattern. Modified from Moralí et al. (1985). behavior. Surprisingly, EB, which in castrated males signi- animals with androgen gradually restored the occurrence of ficantly increased thrusting frequencies, lacked this effect in copulatory responses, with similar motor characteristics to ovariectomized rats. those of intact animals. These data suggest that the neural The results show that the organization of the movements mechanisms responsible for the presentation of the copulat- involved in the masculine sexual behavior in rats are ident- ory behaviors (motivation), as well as those involved in the ical in both sexes, thus suggesting that the neural circuits execution of genital responses during both intromissive and controlling these behaviors could be identical. Neonatal or ejaculatory behaviors, require androgen for their functioning. postpubertal androgen in the rat influences the incidence In contrast, the neuronal circuits involved in the expression of male-like responses, but not their temporal or dynamic of the motor components of the copulatory behavior of the characteristics. hamster seem to be independent of androgen action. Similarly, mounts recorded in guinea pigs up to nine weeks after castration show pelvic thrusting trains with Golden hamster and guinea pig similar frequency and rhythmicity to those of intact animals Castration of hamsters results in a progressive decline of (Moralí, González-Vidal & Cervantes, submitted). Under their sexual activity, so that, two weeks after castration, TP treatment, castrated guinea pigs showed copulatory ejaculatory responses are no longer displayed and the responses with similar motor and genital characteristics to duration of penile insertions is significantly reduced those of intact animals. (Arteaga & Moralí, unpublished results). As described for rat mounting trains, the duration of the extravaginal pelvic thrusting trains of castrated hamsters was longer in all Interspecies comparisons copulatory responses in relation to that of intact animals. Overall, the effects of castration and hormone treatment The frequency, vigor and periodicity of thrusting were upon the masculine copulatory motor pattern differs between similar to those of intact subjects. Treatment of castrated rabbits, rats, hamsters, and guinea pigs. Two mechanisms

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