HORMONES
AND
Hormone
BEHAVIOR
8,
1-7 (1977)
Induced Lordosis and Its Relation Sexual Activity in Male Rata
to Masculine
N. E. VAN DE POLL and H. VAN DIS Netherlands Central Ins&&e for Brm’n Research, Ijdijk 28, Amsterdam- The Netherlands Intact and castrated male rats were injected with a single dose of estrogen (75 clp), followed by progesterone (1 mg) or by oil. Intact males showed higher lordosis quotients as compared to castrated males. Progesterone facilitated lordosis behavior in castrated as well as in intact males. An estrogen-progesterone treated group of sexually inactive male rats and of sexually exhausted males showed lower levels of lordosis as compared to the intact sexually active males.
Only in the last years have systematic reports on the induction of lordosis behavior in male rats begun to appear in the literature. The neural substrate mediating feminine behavior is generally assumed to be refractory to estrogens and ‘this fact is reflected by the difficulty in stimulating feminine responses in males when estrogens are administered (Young, 1961). Chronic administration of estradiol benzoate in various dosages to castrated males resulted in a gradual increase of the lordosis quotients (Davidson, 1969; Aren-Engelbrektson, Larsson, Sodersten and Wilhelmson, 1970). Pfaff (1970) and Whalen, Luttge and Gorzalka (1971) on the other hand failed to induce lordosis despite 10 days of treatment with estradiol benzoate. In studies at our laboratory frequent lordosis was induced in male Wistar rats by a single large dose of estradiol benzoate. These results and some factors that might be of importance on this subject are presented in this paper. The induction of sexual receptivity in the female rat can be facilitated when estrogen injections are followed by progesterone administration (Beach, 1942a; Powers, 1970). The possibility of facilitating lordosis behavior by progesterone is generally thought to be present in the female rat, but absent in the male (Davidson, 1969; Davidson and Levine, 1969; Aren-Engelbrektson et al., 1970). In the present experiment the facilitatory effect of progesterone on lordosis behavior in the male rat induced by a single high dosage of estrogen is investigated. Masculine and feminine sexual behavior in the male rat until now have usually been studied without considering the possibility of an interaction Copyright All rights
Q 1977 by Academic press, Inc. of reproduction in any form reserved.
ISSN 001&506X
2
VAN DE POLL AND VAN DIS
between these two behavior systems. Such an interaction might be found on different levels. The presence of endogenous testosterone could influence feminine behavior. Without specified theoretical arguments, earlier investigations have mostly utilized castrated males for the study of lordosis behavior. Experiments of Davidson (1969) however, suggest that the rate of increase in lordosis responses is less in animals studied 6 weeks after castration than in groups which were studied 1 week after castration. In considering an interaction between the masculine and feminine behavior systems, it is necessary for feminine behavior to be studied in male rats with comparable levels of masculine mating activity, or in groups of males with low levels of masculine sexual behavior that are not related to deficiencies in testosterone production. The persistent failure of some male rats to engage in masculine sexual behavior with an estrous female is a well known phenomenon, although the underlying physiological mechanisms are unknown (Whalen, 1964; Pottier and Baran, 1973). This deficiency is probably not caused by differences between copulating and noncopulating rats with respect to androgen production or androgen sensitivity (Whalen, Beach, and Kuehn, 1961; Whalen, 1964). To investigate whether the activity of the masculine sexual behavior system is of consequence for the levels of estrogen induced lordosis behavior, in this study normal active rats have been compared to sexually inactive males. The second way to investigate whether or not the activity of the masculine sexual behavior system influences estrogen induced feminine sexual behavior is by studying lordosis in male rats that are temporarily sexually inactive after sexual exhaustion. Although the underlying mechanisms of this decline in masculine sexual behavior are unknown it is unlikely that testosterone plays an essential role in this process (unpublished results from the authors’ laboratory).
MATERIAL
AND METHODS
Subjects. Subjects for this experiment were 100 intact and 31 castrated male Wistar rats weighing approximately 350 g. They were kept in cages containing 8-10 animals and were maintained on an artificially reversed (12 hr/12 hr) dark-light cycle. The following seven groups were used for experimentation: intact males: estrogen t progesterone, N = 28; estrogen + oil, N= 16 and oil t progesterone, N = 16. Castrated males: estrogen + progesterone, N = 15 and estrogen t oil, N = 16. Furthermore nine sexually inactive and 31 sexually exhausted males were used for experimentation, both groups treated with estrogen + progesterone. All groups with the exception of the intact inactive animals were comparable with respect to male sexual activity: three to five ejaculations in a
LORDOSIS
IN MALE RATS
3
30 min pretest, which for the castrated males took place before castration. Castration was carried out under phentanyl (Hypnorm) anesthesia 2 months before experimentation. The sexually inactive male rats were selected on the basis of the absence of any sexual activity other than genital sniffing during six 1 hr tests with receptive females during 3 weeks. During the sexual exhaustion test the males were tested until they did not ejaculate during a period of 90 min. Every 30 min a new stimulus female was presented. Hormone administration. Hormone administration to provoke lordosis in the males consisted of intramuscular injections of 75 pg estradiol and 1 mg progesterone, or as a control equal amounts (0.2 ml) of oleum arachidis. The interval between estrogen and progesterone administration was 36 hr. Behavioral tests were carried out 8 hr after progesterone injection. The exhausted males were injected with estrogen on the day of the exhaustion test, 1 hr after exhaustion was reached. Pretests and sexual exhaustion tests took place with females artificially brought in behavioral estrus by treatment with estradiol benzoate (50 pg), followed by progesterone (1 mg). Procedure. The tests for feminine behavior were carried out during the last hours of the dark period in semicircular cages (diameter 50 cm) illuminated with dimmed red light. The tests were continued until 10 mounts had occurred. For a lordosis response to be scored, the experimental male had to assume an arched position in which both head and tail were noticeably raised. Feminine behavior was expressed as a lordosis quotient (L/M X 100). Stimulus males, intended to evoke feminine responses, were used during the period of augmented sexual activity following their first postejaculatory interval. These males came from the same stock as the experimental animals.
RESULTS The various groups were compared with the Fisher exact-probability test for the percentage of animals displaying lordosis, and the Mann-Whitney U test for the lordosis quotients (Siegel, 1956). All results of this experiment are presented in Table 1. In the intact males, lordosis behavior was exhibited following both estrogen + oil (56%) and estrogen + progesterone treatment (86%). Oil t progesterone treatment never induced lordosis in these animals. In castrated male rats, estrogen t oil and estrogen + progesterone caused lordosis in 25 and 67% of the animals. No qualitative differences in lordosis patterns in any of the experimental groups could be observed. No hopping or ear wiggling was seen in any of these animals. Castrated vs intact males. The comparison between intact and castrated males under the estrogen + progesterone condition reveals a slightly larger percentage of intact animals responding with lordosis, and higher lordosis quotients in the intact males. Differences between intact and castrated males
4
VAN DE POLL AND VAN DIS TABLE 1 Percentage of Responding Animals and the Median and Range of Lordosis Quotients of Intact, Castrated, Sexually Inactive and Sexually Exhausted Male Rats*, and Statistical Analysis of the Results (Siegel, 1956)
N Estrogen + Oil
Estrogen + Progesterone
% resp. median range N % resp. median range
Intact
Castrated
Inactive
Exhausted
16 56% 30 (20) 20-100 28 86% 70 (65) 10-100
16 25% 65 (0) 50-90 15 67% 35(30) lo-80
9 44% 20 (0) 10-40
31 71% 60 (40) 10-100
Percentage** Estrogen/oil vs estrogen/prog.: Intact vs castrated males: Inactive vs active males: Exhausted vs intact males:
intact males castrated males estrogen/oil estrogen/prog. estrogen/prog. estrogen/prog.
.05 .05 ns (.lO) ns ns (.lO) ns
Quotients***
.oia ns (.io)a nsb
.olb .olb ns (.lO)b
aone-tailed probabilities. btwo-tailed probabilities. The calculation of the Mann-Whitney U test is based upon the data of all animals per group. *Median and range are presented for the responding animals; medians of all animals per group are given in parentheses. **Fisher exact-p; ***Man-Whitney CI test.
in the estrogen+ oil condition did, however, not reach statistical significance, either for the percentage of responding animals, or for the lordosis quotients. The facilitatory effects of progesterone. Both in castrated and intact males progesterone significantly facilitated the estrogen effect on lordosis behavior. In the castrated males, the percentage of responding animals was increased, whereas in the intact males both the percentagesof responding animals and the lordosis quotients were higher. Sexually active vs inactive males. After estrogen+ progesterone treatment the sexually inactive males showed lower levels of lordosis behavior as compared to sexually active males. Sexual exhaustion and lordosis behavior. The male rats reached 6-17 ejaculations in the sexual exhaustion tests, showing a median of 11 ejaculations. Sexually exhausted, estrogen+ progesteronetreated males showed levels of lordosis behavior that tended to be somewhat lower than those of normal active males.
LORDOSIS
IN MALE RATS
5
The difference in percentagesof responding animals of these groups did not reach statistical significance. DISCUSSION The present,results show that treatment of intact male rats with a single dose of estrogen may result in substantial levels of lordosis behavior. Moreover, the results suggestthat the feminine mating pattern might be more successfully induced in intact than in castratedmales.Progesteronefacilitated the occurrence of lordosis in castratedas well as in intact male rats. Compared to sexually active males, the rats that persistently fail to copulate or rats that are sexually inactive following sexual exhaustion responded with lower levels of lordosis behavior after treatment with estrogenand progesterone. The low levels of lordosis behavior following estrogen treatment in male rats reported in literature may be due to severalfactors. Firstly, most authors worked with castrated animals, perhaps with the underlying implicit assumption that androgens from the testes, or the activity of the masculine mating system, inhibits the occurrence of feminine sexual behavior. Apparently the opposite is true. That endogenousor exogenousandrogensmay play a role in the display of feminine sexual behavior in the male was earlier suggestedby Beach (1941, 1945). Some evidence has been obtained suggestingthat the stimulatory effect of androgens upon lordosis behavior would have to be ascribed to an enzymatic conversion of androgens into estrogen (Beyer and Komisaruk, 1971; Naftolin, Ryan, and Petro, 1972; Whalen, Battie, and Luttge, 1972). These processesmight explain the differences between the intact and castrated malesbut are less likely to be involved in the lower levels of lordosis behavior in the other groups. A second factor contributing to the rather high levels of lordosis behavior might be found in the selection of the samplesof animals. In the present study all experimental males were selected for showing high levels of masculine sexual activity. A positive correlation of the activity of the masculine and feminine sexual behavior system is suggestedby some earlier studies. Male rats spontaneouslyshowing feminine copulatory behavior proved to be exceptionally vigorous copulators when placed with receptive females (Stone, 1924; Beach, 1938, 1945). Moreover, the present study indicates that males not showing any masculine sexual activity also exhibit less feminine copulatory behavior. Comparing the number of ejaculations in an exhaustion test and the spontaneous levels of lordosis in Danish male Wistar rats, Sodersten, De Jong, Vreeburg and Baum (1974) recently failed to fmd any correlation. In this experiment Danish males showing unusual high levels of lordosis behavior were comparedwith a Danish no-lordosis group and a Dutch (Wistar) no-lordosis group. Although a comparison of masculine sexual be-
6
VAN DE POLL AND VAN DIS
havior of these three groups indicated that Dutch males achieved ejaculation in significantly more tests than the other groups no further differences in masculine sexual activity were indicated. Apparently further investigation is required to define and specify possible relations between the masculine and feminine mating systems. Finally, a third factor might add to the results of this experiment. Little is known about the factors causing one male to mount another male. Testing male rats for lordosis behavior requires a stock of highly active stimulus males, which mount the experimental males with sufficient vigor. This factor is difficult to standardize, especially when the experimental males are intact. Therefore, this might significantly add to the rather contradictory results on this subject. In the present seriesof experiments progesteronesignificantly facilitated the display of lordosis in male rats. This is in contrast with earlier reports on this subject (Davidson, 1969; Davidson and Levine, 1969; Aren-Engelbrektson et al., 1970; Clemens,Shryne, and Gorski, 1970). Perhapsthe most significant difference between the procedure used in our experiment and those reporting conflicting results might be found in the number of days of estrogen treatment preceding progesterone administration. When high dosages of estrogen are given for a considerabletime, the level of feminine responsiveness is possibly determined to a high degree by estrogen, whereas the facilitator-y effect of progesterone can only be demonstrated when estrogenis given for a short time. The present results, therefore, corroborate the suggestion of Eriksson and Sodersten (1973) that males respond to progesteroneif estrogen and progesteroneare administrated in an adequatetime schedule.
REFERENCES Aren-Engelbrektson, B., Larsson, K., Sodersten, P., and Wilhelmson, M. (1970). The female lordosis pattern induced in male rats by estrogen. Horm. Behnu. 1, 181-188. Beach, F. A. (1938). Sex reversals in the mating pattern of the rat. J. Genet. Psychol. 52, 329-334. Beach, F. A. (1941). Female mating behavior shown by male rats after administration of testosterone propionate. Endocrinology 29, 409-412. Beach, F. A. (1942). Importance of progesterone to induction of sexual receptivity in spayed female rats. Proc. Biol. Med. 5 1, 369-37 1. Beach, F. A. (1945). Bisexual mating behavior in the male rat: Effects of castration and hormone administration. Physiol. Zool. 18, 390-402. Beyer, C., and Komisaruk, B. (1971). Effects of diverse androgens on estrous behavior, lordosis reflex; and genital trait morphology in the rat. Horm. Behav. 2, 217-225. Clemens, L. G., Shryne, J., and Go&i, A. (1970). Androgen and development of progesterone responsiveness in male and female rats. Physiol. Behav. 5, 673-678. Davidson, J. M. (1969). Effects of estrogen on the sexual behavior of male rats. Endocrinology 84, 1365-1372.
LORDOSIS IN MALE RATS
7
Davidson, J. M., Levine, S. (1969). Progesterone and heterotypical sexual behavior in male rats. J. Endocrinol. 44, 129-130. Eriksson, H., and Sodersten, P, (1973). A failure to facilitate lordosis behavior in adrenalectomized and gonadectomized estrogen-primed rats with monoaminesynthesis inhibitors. Horm. Behav. 4, 89-97. Naftolin, F., Ryan, K. J., and Petro, Z. (1972). Aromatization of androstenedione by the anterior hypothalamus of adult male and female rats. Endocrinology 90, 295-298. Pfaff, D. W. (1970). Nature of sex hormone effects on rat sex behavior: Specificity of effects and individual patterns of response. J. Comp. PhysioZ. Psychol. 73, 349-358. Pottier, J. J. G., and Baran, D. (1973). A general behavioral syndrome associated with persistent failure to mate in the male laboratory rat. J. Comp. Physiol. Psychol. 83, 3, 499-509. Powers, J. B. (1970). Hormonal control of sexual receptivity during the estrous cycle of the rat. Physiol. Behav. 5, 831-835. Siegel, S. (1956). Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York. Sodersten, P. (1974). Lordosis behavior in intact male rats: Absence of correlation with mounting behavior or testicular secretion of estradiol-170 and testosterone. Physiol. Behav. 13, 803-808. Stone, C. P. (1924). A note on ‘feminine’ behavior in adult male rats. Amer. J. Physiol. 68, 39-41. Whalen, R. E. (1964). Hormone-induced changes in the organization of sexual behavior in the male rat. J. Comp. Physiol. Psychol. 57, 175-182. Whalen, R. E., Beach, F. A., and Kuehn, R. E. (1961). Effects of exogenous androgen on sexually responsive and unresponsive rats. Endocrinology 69, 373-380. Whalen, R. E., Battie, C., and Luttge, W. G. (1972). Anti-estrogen inhibition of androgen induced sexual receptivity in rats. Behav. BioZ. 7, 31 l-320. Whalen, R. E., Luttge, W. G., and Gorzalka, B. B. (1971). Neonatal androgenization and the development of estrogen responsivity in male and female rats. Horm. Behav. 2, 83-90. Young, W. C. (1961). The hormones and mating behavior. In W. C. Young (Ed.), Sex and InternationaZ Secretions, Vol. 11, pp. 1173-1239. Williams & Wilkins, Baltimore.
AND
Hormone
BEHAVIOR
8,
1-7 (1977)
Induced Lordosis and Its Relation Sexual Activity in Male Rata
to Masculine
N. E. VAN DE POLL and H. VAN DIS Netherlands Central Ins&&e for Brm’n Research, Ijdijk 28, Amsterdam- The Netherlands Intact and castrated male rats were injected with a single dose of estrogen (75 clp), followed by progesterone (1 mg) or by oil. Intact males showed higher lordosis quotients as compared to castrated males. Progesterone facilitated lordosis behavior in castrated as well as in intact males. An estrogen-progesterone treated group of sexually inactive male rats and of sexually exhausted males showed lower levels of lordosis as compared to the intact sexually active males.
Only in the last years have systematic reports on the induction of lordosis behavior in male rats begun to appear in the literature. The neural substrate mediating feminine behavior is generally assumed to be refractory to estrogens and ‘this fact is reflected by the difficulty in stimulating feminine responses in males when estrogens are administered (Young, 1961). Chronic administration of estradiol benzoate in various dosages to castrated males resulted in a gradual increase of the lordosis quotients (Davidson, 1969; Aren-Engelbrektson, Larsson, Sodersten and Wilhelmson, 1970). Pfaff (1970) and Whalen, Luttge and Gorzalka (1971) on the other hand failed to induce lordosis despite 10 days of treatment with estradiol benzoate. In studies at our laboratory frequent lordosis was induced in male Wistar rats by a single large dose of estradiol benzoate. These results and some factors that might be of importance on this subject are presented in this paper. The induction of sexual receptivity in the female rat can be facilitated when estrogen injections are followed by progesterone administration (Beach, 1942a; Powers, 1970). The possibility of facilitating lordosis behavior by progesterone is generally thought to be present in the female rat, but absent in the male (Davidson, 1969; Davidson and Levine, 1969; Aren-Engelbrektson et al., 1970). In the present experiment the facilitatory effect of progesterone on lordosis behavior in the male rat induced by a single high dosage of estrogen is investigated. Masculine and feminine sexual behavior in the male rat until now have usually been studied without considering the possibility of an interaction Copyright All rights
Q 1977 by Academic press, Inc. of reproduction in any form reserved.
ISSN 001&506X
2
VAN DE POLL AND VAN DIS
between these two behavior systems. Such an interaction might be found on different levels. The presence of endogenous testosterone could influence feminine behavior. Without specified theoretical arguments, earlier investigations have mostly utilized castrated males for the study of lordosis behavior. Experiments of Davidson (1969) however, suggest that the rate of increase in lordosis responses is less in animals studied 6 weeks after castration than in groups which were studied 1 week after castration. In considering an interaction between the masculine and feminine behavior systems, it is necessary for feminine behavior to be studied in male rats with comparable levels of masculine mating activity, or in groups of males with low levels of masculine sexual behavior that are not related to deficiencies in testosterone production. The persistent failure of some male rats to engage in masculine sexual behavior with an estrous female is a well known phenomenon, although the underlying physiological mechanisms are unknown (Whalen, 1964; Pottier and Baran, 1973). This deficiency is probably not caused by differences between copulating and noncopulating rats with respect to androgen production or androgen sensitivity (Whalen, Beach, and Kuehn, 1961; Whalen, 1964). To investigate whether the activity of the masculine sexual behavior system is of consequence for the levels of estrogen induced lordosis behavior, in this study normal active rats have been compared to sexually inactive males. The second way to investigate whether or not the activity of the masculine sexual behavior system influences estrogen induced feminine sexual behavior is by studying lordosis in male rats that are temporarily sexually inactive after sexual exhaustion. Although the underlying mechanisms of this decline in masculine sexual behavior are unknown it is unlikely that testosterone plays an essential role in this process (unpublished results from the authors’ laboratory).
MATERIAL
AND METHODS
Subjects. Subjects for this experiment were 100 intact and 31 castrated male Wistar rats weighing approximately 350 g. They were kept in cages containing 8-10 animals and were maintained on an artificially reversed (12 hr/12 hr) dark-light cycle. The following seven groups were used for experimentation: intact males: estrogen t progesterone, N = 28; estrogen + oil, N= 16 and oil t progesterone, N = 16. Castrated males: estrogen + progesterone, N = 15 and estrogen t oil, N = 16. Furthermore nine sexually inactive and 31 sexually exhausted males were used for experimentation, both groups treated with estrogen + progesterone. All groups with the exception of the intact inactive animals were comparable with respect to male sexual activity: three to five ejaculations in a
LORDOSIS
IN MALE RATS
3
30 min pretest, which for the castrated males took place before castration. Castration was carried out under phentanyl (Hypnorm) anesthesia 2 months before experimentation. The sexually inactive male rats were selected on the basis of the absence of any sexual activity other than genital sniffing during six 1 hr tests with receptive females during 3 weeks. During the sexual exhaustion test the males were tested until they did not ejaculate during a period of 90 min. Every 30 min a new stimulus female was presented. Hormone administration. Hormone administration to provoke lordosis in the males consisted of intramuscular injections of 75 pg estradiol and 1 mg progesterone, or as a control equal amounts (0.2 ml) of oleum arachidis. The interval between estrogen and progesterone administration was 36 hr. Behavioral tests were carried out 8 hr after progesterone injection. The exhausted males were injected with estrogen on the day of the exhaustion test, 1 hr after exhaustion was reached. Pretests and sexual exhaustion tests took place with females artificially brought in behavioral estrus by treatment with estradiol benzoate (50 pg), followed by progesterone (1 mg). Procedure. The tests for feminine behavior were carried out during the last hours of the dark period in semicircular cages (diameter 50 cm) illuminated with dimmed red light. The tests were continued until 10 mounts had occurred. For a lordosis response to be scored, the experimental male had to assume an arched position in which both head and tail were noticeably raised. Feminine behavior was expressed as a lordosis quotient (L/M X 100). Stimulus males, intended to evoke feminine responses, were used during the period of augmented sexual activity following their first postejaculatory interval. These males came from the same stock as the experimental animals.
RESULTS The various groups were compared with the Fisher exact-probability test for the percentage of animals displaying lordosis, and the Mann-Whitney U test for the lordosis quotients (Siegel, 1956). All results of this experiment are presented in Table 1. In the intact males, lordosis behavior was exhibited following both estrogen + oil (56%) and estrogen + progesterone treatment (86%). Oil t progesterone treatment never induced lordosis in these animals. In castrated male rats, estrogen t oil and estrogen + progesterone caused lordosis in 25 and 67% of the animals. No qualitative differences in lordosis patterns in any of the experimental groups could be observed. No hopping or ear wiggling was seen in any of these animals. Castrated vs intact males. The comparison between intact and castrated males under the estrogen + progesterone condition reveals a slightly larger percentage of intact animals responding with lordosis, and higher lordosis quotients in the intact males. Differences between intact and castrated males
4
VAN DE POLL AND VAN DIS TABLE 1 Percentage of Responding Animals and the Median and Range of Lordosis Quotients of Intact, Castrated, Sexually Inactive and Sexually Exhausted Male Rats*, and Statistical Analysis of the Results (Siegel, 1956)
N Estrogen + Oil
Estrogen + Progesterone
% resp. median range N % resp. median range
Intact
Castrated
Inactive
Exhausted
16 56% 30 (20) 20-100 28 86% 70 (65) 10-100
16 25% 65 (0) 50-90 15 67% 35(30) lo-80
9 44% 20 (0) 10-40
31 71% 60 (40) 10-100
Percentage** Estrogen/oil vs estrogen/prog.: Intact vs castrated males: Inactive vs active males: Exhausted vs intact males:
intact males castrated males estrogen/oil estrogen/prog. estrogen/prog. estrogen/prog.
.05 .05 ns (.lO) ns ns (.lO) ns
Quotients***
.oia ns (.io)a nsb
.olb .olb ns (.lO)b
aone-tailed probabilities. btwo-tailed probabilities. The calculation of the Mann-Whitney U test is based upon the data of all animals per group. *Median and range are presented for the responding animals; medians of all animals per group are given in parentheses. **Fisher exact-p; ***Man-Whitney CI test.
in the estrogen+ oil condition did, however, not reach statistical significance, either for the percentage of responding animals, or for the lordosis quotients. The facilitatory effects of progesterone. Both in castrated and intact males progesterone significantly facilitated the estrogen effect on lordosis behavior. In the castrated males, the percentage of responding animals was increased, whereas in the intact males both the percentagesof responding animals and the lordosis quotients were higher. Sexually active vs inactive males. After estrogen+ progesterone treatment the sexually inactive males showed lower levels of lordosis behavior as compared to sexually active males. Sexual exhaustion and lordosis behavior. The male rats reached 6-17 ejaculations in the sexual exhaustion tests, showing a median of 11 ejaculations. Sexually exhausted, estrogen+ progesteronetreated males showed levels of lordosis behavior that tended to be somewhat lower than those of normal active males.
LORDOSIS
IN MALE RATS
5
The difference in percentagesof responding animals of these groups did not reach statistical significance. DISCUSSION The present,results show that treatment of intact male rats with a single dose of estrogen may result in substantial levels of lordosis behavior. Moreover, the results suggestthat the feminine mating pattern might be more successfully induced in intact than in castratedmales.Progesteronefacilitated the occurrence of lordosis in castratedas well as in intact male rats. Compared to sexually active males, the rats that persistently fail to copulate or rats that are sexually inactive following sexual exhaustion responded with lower levels of lordosis behavior after treatment with estrogenand progesterone. The low levels of lordosis behavior following estrogen treatment in male rats reported in literature may be due to severalfactors. Firstly, most authors worked with castrated animals, perhaps with the underlying implicit assumption that androgens from the testes, or the activity of the masculine mating system, inhibits the occurrence of feminine sexual behavior. Apparently the opposite is true. That endogenousor exogenousandrogensmay play a role in the display of feminine sexual behavior in the male was earlier suggestedby Beach (1941, 1945). Some evidence has been obtained suggestingthat the stimulatory effect of androgens upon lordosis behavior would have to be ascribed to an enzymatic conversion of androgens into estrogen (Beyer and Komisaruk, 1971; Naftolin, Ryan, and Petro, 1972; Whalen, Battie, and Luttge, 1972). These processesmight explain the differences between the intact and castrated malesbut are less likely to be involved in the lower levels of lordosis behavior in the other groups. A second factor contributing to the rather high levels of lordosis behavior might be found in the selection of the samplesof animals. In the present study all experimental males were selected for showing high levels of masculine sexual activity. A positive correlation of the activity of the masculine and feminine sexual behavior system is suggestedby some earlier studies. Male rats spontaneouslyshowing feminine copulatory behavior proved to be exceptionally vigorous copulators when placed with receptive females (Stone, 1924; Beach, 1938, 1945). Moreover, the present study indicates that males not showing any masculine sexual activity also exhibit less feminine copulatory behavior. Comparing the number of ejaculations in an exhaustion test and the spontaneous levels of lordosis in Danish male Wistar rats, Sodersten, De Jong, Vreeburg and Baum (1974) recently failed to fmd any correlation. In this experiment Danish males showing unusual high levels of lordosis behavior were comparedwith a Danish no-lordosis group and a Dutch (Wistar) no-lordosis group. Although a comparison of masculine sexual be-
6
VAN DE POLL AND VAN DIS
havior of these three groups indicated that Dutch males achieved ejaculation in significantly more tests than the other groups no further differences in masculine sexual activity were indicated. Apparently further investigation is required to define and specify possible relations between the masculine and feminine mating systems. Finally, a third factor might add to the results of this experiment. Little is known about the factors causing one male to mount another male. Testing male rats for lordosis behavior requires a stock of highly active stimulus males, which mount the experimental males with sufficient vigor. This factor is difficult to standardize, especially when the experimental males are intact. Therefore, this might significantly add to the rather contradictory results on this subject. In the present seriesof experiments progesteronesignificantly facilitated the display of lordosis in male rats. This is in contrast with earlier reports on this subject (Davidson, 1969; Davidson and Levine, 1969; Aren-Engelbrektson et al., 1970; Clemens,Shryne, and Gorski, 1970). Perhapsthe most significant difference between the procedure used in our experiment and those reporting conflicting results might be found in the number of days of estrogen treatment preceding progesterone administration. When high dosages of estrogen are given for a considerabletime, the level of feminine responsiveness is possibly determined to a high degree by estrogen, whereas the facilitator-y effect of progesterone can only be demonstrated when estrogenis given for a short time. The present results, therefore, corroborate the suggestion of Eriksson and Sodersten (1973) that males respond to progesteroneif estrogen and progesteroneare administrated in an adequatetime schedule.
REFERENCES Aren-Engelbrektson, B., Larsson, K., Sodersten, P., and Wilhelmson, M. (1970). The female lordosis pattern induced in male rats by estrogen. Horm. Behnu. 1, 181-188. Beach, F. A. (1938). Sex reversals in the mating pattern of the rat. J. Genet. Psychol. 52, 329-334. Beach, F. A. (1941). Female mating behavior shown by male rats after administration of testosterone propionate. Endocrinology 29, 409-412. Beach, F. A. (1942). Importance of progesterone to induction of sexual receptivity in spayed female rats. Proc. Biol. Med. 5 1, 369-37 1. Beach, F. A. (1945). Bisexual mating behavior in the male rat: Effects of castration and hormone administration. Physiol. Zool. 18, 390-402. Beyer, C., and Komisaruk, B. (1971). Effects of diverse androgens on estrous behavior, lordosis reflex; and genital trait morphology in the rat. Horm. Behav. 2, 217-225. Clemens, L. G., Shryne, J., and Go&i, A. (1970). Androgen and development of progesterone responsiveness in male and female rats. Physiol. Behav. 5, 673-678. Davidson, J. M. (1969). Effects of estrogen on the sexual behavior of male rats. Endocrinology 84, 1365-1372.
LORDOSIS IN MALE RATS
7
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