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

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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 © 2003 The Scandinavian Psychological Associations. Published by Blackwell Publishing Ltd., 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA. ISSN 0036-5564. 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
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