Lordotic Behavior Research Articles

Effects of ultrasonic vocalizations and male's urine on female rat readiness to mate.

Journal of Comparative and Physiological Psychology 1978, Vol. 92, No. 3, 457^62 Effects of Ultrasonic Vocalizations and Male's Urine on Female Rat Readiness to Mate Lynette A. Geyer, Tracy K. Mclntosh, and Ronald J. Barfield Department of Biology Livingston College, Rutgers—The State University Solitary estrous female rats were presented with ultrasonic vocalizations and/ or urine of males to determine their effects on the females' subsequent copula- tory behavior. Following exposure to ultrasounds, females exhibited a shorter latency to dart and a higher rate of darting when a male was presented. The vocalization effect was enhanced when male urine was present, but urine alone had no effect. The rate of copulation was also increased by the vocalization priming of the female. For a few individual females, ultrasounds elicited darting in the absence of a male. These results indicate that auditory cues, particularly in association with appropriate olfactory cues, prime estrous fe- males for preceptive behavior. This increases both the likelihood and the rate of sexual performance and, therefore, the probability of successful mating. During copulation, the female rat (Rattus norvegicus) exhibits hopping and darting movements. Typically, these movements immediately precede mounting sequences by the male rat (McClintock, 1974). When sexually naive males are tested with females exhibiting darting, there is a higher probability of copulation occurring than when females showing only the lordotic response are used (Hlinak & Madlafousek, 1972). Thus, hopping and darting may be a form of solicitation that facilitates copu- lation. This article is based on a dissertation submitted by the first author to Rutgers University in partial fulfill- ment of the requirements for the PhD degree. This research was supported by National Institute of Child Health and Human Development Research Grant HD-04484 to the third author and by U.S. Public Health Service Predoctoral Fellowship 27-3887 to the first author. Hormones used in the study were generously donated by R. Neri, Schering Corporation, Bloomfield, New Jersey. We are grateful to D. R. Griffin of Rock- efeller University for technical advice and for loan of essential equipment used in this study. It is also a pleasure to thank G. K. Beauchamp and R. L. Doty of the Monell Chemical Senses Center for many useful comments on the manuscript. L. A. Geyer is now at the Monell Chemical Senses Center, University of Pennsylvania. Requests for reprints should be sent to R. J. Barfield, Department of Biology, Livingston College, Rutgers— The State University, New Brunswick, New Jersey Darting has been characterized as pre- lordotic behavior by Pfaff and Lewis (1974). At the end of a darting sequence, the female comes to an abrupt halt and assumes a crouching posture, a forward extension of the front legs, a bilaterally symmetric posture, and a skeletal musculature tension that fa- cilitates lordosis (Pfaff, Lewis, Diakow, & Keiner, 1972). Solicitation patterns such as hopping and darting appear to be affected by experience as well as hormones. Gerall and Dunlap (1973) described the enhancement of solici- tation behavior by experience in several mating tests. At later ages sexually experi- enced females had longer intervals between solicitation bouts and markedly delayed ejaculation by preventing mounting. They achieved greater reproductive success than virgins of similar ages that did not show the control of intromission pacing (Dunlap & Gerall, Note 1). Immediately before and during mounting sequences, rats produce ultrasonic vocali- zations, with the main energy around 50 kHz (Sales, 1972). Both males and females emit pulses in mating situations (Geyer, 1976). High pulse production is associated with the hormonal and behavioral readiness of both the male and the female to copulate. Specific sensory cues eliciting solicitation have not been identified. The presence of Copyright 1978 by the American Psychological Association, Inc. 0021-9940/78/9203-0467$00.75

Masculinization and defeminization induced in female hamsters by neonatal treatment with estradiol benzoate and RU-2858

To test the hypothesis that masculinization may be androgen dependent and defeminization, estrogen dependent, newborn female hamsters were administered 50–2000 ng of estradiol benzoate (EB), 0.05–50 ng of the synthetic estrogen RU-2858, or 1000 ng of testosterone propionate (TP). All three agents facilitated the display of male-type mounting responses in adulthood. A dose of 500 ng of EB was most potent in this regard, although significant masculinization was induced by 50 ng of EB and 0.05 ng of RU-2858 as well as by TP. TP did not inhibit adult lordotic behavior. Lordosis durations were reduced in a dose-dependent manner by EB, whereas the dose-response curve for RU-2858-induced defeminization was found to be nonlinear. The observation that picogram to nanogram amounts of estrogen can masculinize is consistent with the aromatization hypothesis of sexual differentiation.

Role of hypothalamic serotonergic receptors in the control of lordosis behavior in the female rat

The role of serotonin in mediating hypothalamic control of sexual behavior in estrone-primed ovariectomized (OVX) rats was studied by comparing the lordotic patterns following medial preoptic (MPOA) and arcuate-ventromedial (ARC-VM) infusions of serotonin (5-HT), methysergide (MS), and vehicle. In the initial experiments, low receptivity (preinfusion receptivity: mean lordosis/mount ratio = 0.164) was maintained by priming each animal with a low dose of estrone 48 hr prior to mating. The infusion of MS in either the MPOA or ARC-VM area resulted in a significant enhancement of lordotic behavior from initial low receptivity, 5-HT infusions were found to have no statistically significant effect upon lordotic behavior. In order to corroborate the findings observed in the low preinfusion receptivity protocol, OVX rats were primed with higher doses of estrone to maintain a high level of receptivity (preinfusion receptivity: mean lordosis/mount ratio = 0.787). Using this protocol, significant depressions in lordotic behavior were observed following MPOA or ARC-VM infusions of 5-HT, It was thus proposed that serotonergic receptors within the MPOA or ARC-VM areas have inhibitory effects upon lordotic behavior. In addition to the effects of 5-HT upon estrogen-induced sexual receptivity, serotonergic influences upon luteinizing hormone-releasing hormone (LRH)-facilitated mating behavior were also evaluated. Comparisons were made between the lordotic responses following MPOA or ARC-VM infusions of vehicle, LRH, or LRH with 5-HT in OVX rats primed with low doses of estrone. The infusion of LRH into the MPOA or ARC-VM significantly enhanced lordotic behavior above vehicle levels. However, the addition of 5-HT to the LRH infusate abolished this behavioral enhancement. These findings indicated that LRH and 5-HT have opposing effects within forebrain areas known to be important for the control of lordotic behavior.

Effects of perinatal androstenedione on sexual differentiation in female rats.

Androstenedione was administered prenatally, postnatally, postnatally, or both pre-and postnatally to female rats. The extent to which reproductive morphology, ovarian functioning, and adult sexual behavior were masculinized and defeminized depended on the dosage, timing, and duration of the hormone treatment. The combined pre-plus postnatal treatment resulted in the greatest degree of modification in that such females were anatomically masculinized and did not ovulate. When tested in adulthood, they showed a high potential for the male copulatory pattern and little lordotic behavior. It is concluded that androstenedione, while not as potent an androgen as testosterone propionate, nevertheless has the potential to participate in the process of sexual differentiation.

Central progesterone induces female sexual behavior in estrogen-primed intact male rats.

Progesterone induced high levels of female lordotic behavior in 10 of 17 intact, estrogen-primed male rats when it was applied directly to the medial preoptic-anterior hypothalamic area. All 17 males previously had shown lordosis when the serotonergic antagonist methysergide was applied to the same central sites. Few males responded to systemic progesterone and none to intracralial cholesterol. Intradiencephalic Metycaine, a local anesthetic, induced lordosis in eight male that previously had responded to central progesterone. These data indicate that estrogen and progesterone act synergistically to induce lordosis in male rats when progesterone is administered directly to sensitive brain sites.

Effects of septal lesions on the lordotic behavior of weanling male and female rats

Twenty-four-day-old weanling male and female rats were either lesioned in the septal area, gonadectomized, lesioned and gonadectomized, or not treated. Tests for lordotic behavior were carried out at 27 and 28 days of age after priming with estradiol alone and with estradiol plus progesterone. A second set of tests for lordotic behavior was carried out at 47 and 48 days of age. In the interim period, some of the animals were given chronic estrogen treatment. In tests given at 27 days of age, septal lesions facilitated lordotic responding after estrogen priming; no differences were observed between male and female animals. At 47 and 48 days of age, however, unless male rats had been exposed to chronic estrogens following septal lesioning, no facilitation of estrogen-induced lordotic behavior occurred. In addition, it was found that female rats gonadectomized at 24 days of age and given no exposure to estrogens between the tests at 27 and 28 days and those at 47 and 48 days of age showed reduced sensitivity to estrogens, as compared to normal or estrogen-treated females, whether lesioned or not.

Effects of subcutaneous injection and intrahypothalamic infusion of releasing hormones upon lordotic response to repetitive coital stimulation

The effects of luteinizing hormone-releasing hormone (LRH) and thyrotropin-releasing hormone (TRH) upon the lordotic response to repetitive coital stimlation were studied using ovariectomized (OVX) and ovariectomized-adrenalectomized (OVX-ADX) female rats. Both OVX and OVX-ADX rats, pretreated with estrone alone, exhibited a dual behavioral response to repeated coital stimulation. The initial response to short-term stimulation was facilitatory with peak sexual receptivity occurring approximately 120 min following the initial male contact. This initial phase was followed by a depression of sexual receptivity associated with continued coital stimulation. Subcutaneous injection of 500 ng of LRH prior to mating was found to significantly potentiate the initial increases in sexual receptivity and to delay the onset of behavioral depression. The injection of 500 ng of TRH was observed to significantly depress behavioral enhancement due to repetitive coital stimulation. The repetitive coital stimulation model was utilized to localize forebrain areas behaviorally responsive to LRH and TRH. Stainless steel cannulas were implanted into either the medial preoptic area (MPOA), arcuate area (ARC), lateral hypothalamic area (LHA), or cerebral cortex (CC). Cannulated animals, primed with estrone, were tested for sexual receptivity immediately prior to experimental treatment, i.e., the infusion of 0.5 μl of 50 ng of LRH or TRH in 0.9% saline, 0.5 μl of 0.9% saline, or sham infusion. A second mating (postinfusion) test was performed 1.75 hr following infusion. When infused into the MPOA or ARC, LRH significantly enhanced lordotic behavior as compared to values obtained for saline or sham infusions. The infusion of LRH into LHA or CC showed no enhancement beyond the levels observed in control infusions (saline and sham infusions). The infusion of TRH into the MPOA or ARC depressed lordotic enhancement to repeated mating, however, this depression was significant only in ARC. These findings were consistent with previously demonstrated actions of releasing hormones upon neural activity within the MPOA and ARC.

Effects of hypothalamic and preoptic lesions on reproductive behavior in male rats

Adult male rats, which were selected on the basis of showing complete patterns of male copulatory behavior on two prior tests, were castrated six weeks prior to brain surgery. Animals were divided into three groups and given small bilateral lesions in the dorsomedial preoptic area (POA), ventromedial hypothalamus (VMH), or sham operations. Starting 10 days postsurgery, all animals were injected with estrogen alone and estrogen plus progesterone, and tested twice for lordosis behavior. Ten days following the female behavior tests, animals were injected daily with testosterone propionate for 13 days and tested for masculine sexual behavior on injection days 5, 9 and 13. Low levels of lordotic behavior were observed for POA and VMH animals on both tests for female sex behavior and were comparable to sham operated animals. However, in terms of all dependent measures of male copulatory behavior, animals with VMH lesions showed significantly higher levels of male sex behavior with shorter latencies than sham animals across all three behavior tests. In contrast, POA lesioned rats showed little or no male sex behavior on any test and were significantly inferior to sham operated animals. Thus, the POA and VMH appear to exert excitatory and inhibitory control, respectively, over male copulatory behavior in male rats.

Exogenous androgen activates female behavior in noncopulating, prenatally stressed male rats.

Male copulatory behavior was severely impaired in the male offspring of female rats stressed during pregnancy. This deficiency persisted even after castration and prolonged treatment with testosterone propionate and after exposure to electric skin shock. However, androgen treatment effectively activated female lordotic behavior in a large percentage of prenatally stressed males but not in any control animals and in only a negligible number of postnatally stressed males. Although prenatal stress demasculinizes and feminizes behavior, no modifications of reproductive morphology were detectable. It is postulated that prenatal stress alters normal sexual behavior differentiation by attenuating testosterone secretion from the fetal testes.

Monoaminergic mediation of masculine and feminine copulatory behavior in female rats

Ovariectomized rats treated with testosterone propionate (TP; 100 μg/kg × 6 days) and para-chlorophenylalanine (pCPA; 100 mg/kg × 3 days), a serotonin synthesis inhibitor, showed more masculine copulatory behavior (including the ejaculatory pattern) than did females receiving either TP or pCPA alone. The facilitatory effect of pCPA on the masculine copulatory behavior in females was not potentiated by pargyline (50 or 100 mg/kg), a monoamine oxidase inhibitor; instead, pargyline antagonized the effect of pCPA. Apomorphine (100 μg/kg), a dopamine receptor stimulant, did not increase masculine copulatory behavior in TP treated females. A dopaminergic facilitatory effect was therefore not demonstrated. These results suggest a serotonin-mediated inhibition of masculine copulatory behavior in female rats. When feminine copulatory behavior was tested, females receiving TP plus pCPA plus pargyline, TP plus pargyline, or TP plus apomorphine displayed lordosis in response to mounting by male rats. Lordosis did not occur after administration of TP, pCPA, or pargyline, individually or in any other combination. The responses in pargyline groups are consistent with the hypothesis of a noradrenergic facilitatory system for lordotic behavior. The responses in the apomorphine group are discussed in terms of a possible role for low level dopaminergic stimulation in facilitating lordosis.

Effect of CNS depressants and stimulants on latency for the appearance of copulatory response in the female rat

Diethyl ether anesthesia, sodium hexobarbital (20 mg/kg), diphenylhydantoin (50 mg/kg), strychnine (1 mg/kg) and picrotoxin (1-0.25 mg/kg) effectively induced the copulatory response (lordotic behavior) in estradiol benzoate treated ovariectomized rats although no progesterone was given. As none of the tested compounds were effective in replacing progesterone in adrenalectomized animals, adrenal secretion is likely to be implicated in the lordosis activating effect of these compounds. The lordosis response appeared faster after the CNS stimulants than after treatment with the CNS depressants. The influence of diethylether anesthesia, strychnine (0.5 mg/kg) or picrotoxin (0.25 mg/kg) on the latency for the appearance of the lordosis response after IV injection of isopregnenone was studied in estradiol benzoate treated ovariectomized females. A 10 min ether anesthesia delayed the onset of the lordosis response in adrenal intact as well as adrenalectomized animals. Anesthesia given after receptivity had been fully established suppressed the responses for a short period (10–30 min) after the narcosiis. The delay of the appearance of the first lordosis response after IV injection of isopregnone exceeded this period. Strychnine but not picrotoxin significantly shortened the latency to the onset of the female copulatory response. It is concluded that the lordotic activating action of progesterone or steroids with progesteronelike ability released from an endogenous source or given IV is influenced by compounds which exert a depressant or stimulant effect on neuronal activity. The total response obtained is not changed but the appearance of the response is prolonged by CNS depressants and shortened by certain CNS stimulants.

Sex differences in sensitivity of food intake, body weight, and running-wheel activity to ovarian steroids in rats.

The effects of sex and experimental androgenization on the responsiveness of food intake and running-wheel activity to exogenously administered ovarian hormones were investigated in adult, gonadectomized rats. Food intake was found to be analogous to lordotic behavior in that males and neonatally androgenized females were relatively insensitive to the influences of either estradiol benzoate (EB) or progesterone (P). Running-wheel activity, however, could be differentiated from food intake in that males responded the same as females to the effects of EB and P. Androgenized females (500-mug testosterone propionate on the third day of life) showed a response to EB quantitatively equivalent to that of nonandrogenized females, but they had a longer latency to respond. The estrogen-antagonistic effects of P were confirmed for both of these behaviors, and there was a positive correlation between the magnitude of the responses to EB and P.

Facilitation of female sexual behavior in male rats by septal lesions: An interaction with estrogen

Although destruction of the septal region markedly facilitates the lordosis behavior of female rats in response to estrogen priming, comparable lesions were found to be ineffective in facilitating the lordotic behavior of estrogen primed male rats. Neither the age at the time of septal destruction nor castration influenced the lordosis behavior of males. However, if prepubertal castrated males were given subcutaneous ovarian grafts or injected daily with 2 μgm estradiol benzoate (EB) during the 30 day period following septal destruction, a prolonged facilitation of the activational effects of EB on lordosis behavior was observed. Male rats subjected to septal destruction alone, chronic exposure to EB alone, exposure to ovarian grafts for 30 days prior to septal destruction, or chronic treatment with EB started 6 mo after septal lesioning, failed to show an increase in behavioral responsiveness to estrogen. Thus, in order for septal lesions to facilitate lordosis behavior of male rats, exposure to EB or ovarian tissue must occur within an apparent critical period following septal destruction. Adult male rats were found to be more responsive to this interaction of septal lesions and EB exposure than pubertal animals. It is suggested that the prolonged facilitation of lordosis behavior which follows septal destruction and estrogen exposure in the male rat may be due to hormonal modifications of the recovery process following brain damage.

Monoaminergic mediation of female sexual behavior.

Lordotic behavior was facilitated in estrogen-primed female rats by direct application of progesterone or serotonergic or beta-adrenergic receptor blockers to specific telencephalic, anterior hypothalamic-medial preoptic, or posterior hypothalamic sites. Blockade of the alpha-adrenergic system was ineffective in facilitating lordosis, as was the application of the active drugs to control sites in the thalamus or basal ganglia. Female soliciting behavior was not evoked by any of the treatments. It is concluded that the lordotic behavior component of the female rat's estrous behavior pattern is inhibited by a specific central monoaminergic system that also responds to progesterone. Soliciting behavior appears to be mediated by systems that are anatomically, and possibly neurochemically, separable from those regulating lordosis.

Female lordotic behavior mediated by monoamines in male rat.

Direct application of serotonergic of beta-adrenergic receptor blockers to anterior or posterior areas of the hypothalamus induced lordosis in intact estrogen-primed male rats. Such treatment with an alpha-adrenergic blocker or systemic administration of progesterone failed to increase lordosis. Centrally elicited lordosis did not occur without estrogen priming. Anatomical and neurochemical similarity may exist in the brain mechanism mediating lordotic behavior in male and female adult rats.

The ovulatory surge of gonadotropin and sexual receptivity in the female golden hamster

The present experiments were undertaken to study the nature of the relationship between ovulatory gonadotropin (GTH) release and subsequent sexual behavior in the hamster. GTH antiserum (GTH A/S) injected just prior to the release of the GTH surge prevented both ovulation and lordotic behavior. Both behavior and ovulation could be restored by injecting LH. FSH was effective in restoring ovulation but appeared to have less effect on behavior as compared to LH. Progesterone restored behavior but not ovulation. Large doses of estradiol had no effect on either parameter. The results suggest that ovulatory GTH release (especially LH) is a central event leading to the onset of a sexual receptivity. GTH probably acts by stimulating ovarian progesterone. This steroid acts to induce receptivity and also appears to induce a subsequent period during which the female is behaviorally refractory to sex steroids.

Olfactory bulb removal facilitates the hormonal induction of sexual receptivity in the female rat

Malateral aspiration of the olfactory bulbs facilitates the hormonally induced display of sexual receptivity (lordosis) in spayed female rats. The facilitating effect of bulbectomy is apparent under conditions of estrogen stimulation alone, or after estrogen-progesterone treatment. Moreover, facilitation occurs even when bulb removal is subtotal. Peripherally induced anosmia does not affect the hormonally induced display of lordotic behavior in female rats, indicating that the effect of bulbectomy is not due to the production of anosmia per se. Apparently the olfactory bulbs constitute a source of tonic inhibition upon other neural systems, such that bulb removal enhances the hormonally induced expression of lordotic behavior.

Latency between intravenous injection of progestins and the appearance of estrous behavior in estrogen-treated ovariectomized rats

The latency of the lordosis response after different progestins and progesterone metabolites given by the intravenous route was studied in spayed rats pretreated with estradiol benzoate (10 μg/kg sc). Progestins with anesthetic capacity (progesterone, medroxyprogesterone) had a longer latency at high doses than at low. It is suggested that the true latency for these progestins is masked by the anesthetic property even at dose levels which did not give an overt sedative effect. In analogous experiments with isopregnenone, which lacks an anesthetic effect, a median latency of 10–30 min was obtained regardless of doses given (0.5, 5.0 mg). The isopregnenone data suggest that a certain time is required between the treatment and the appearance of lordotic behavior which is longer than could be expected to be due only to transport from the circulation to the brain tissue.

Neonatal androgenization and estrogenization and the hormonal induction of sexual receptivity in rats

Administration of male sex hormone to neonatal female rats has been shown to inhibit the development of the capacity of the female to respond to female sex hormones in adulthood with the display of sexual receptivity (lordosis). Since the hormonal induction of sexual receptivity in the ovariectomized female typically involves the administration of both estrogen and progesterone, the failure of virilized females to show lordosis following treatment with these two hormones could be due to a diminished sensitivity to estrogen, a diminished sensitivity to progesterone, or both. One purpose of the present study was to determine which of these alternatives obtains. A second purpose of the study was to compare neonatally estrogenized females with neonatally androgenized females, in an attempt to determine to what extent neonatal estrogenization exactly mimics neonatal androgenization. Female rats were given either an injection of testosterone propionate, estradiol benzoate, or oil on the day of birth. Male rats were given a control injection of oil on the day of birth. As adults all rats were gonadectomized and tested for sexual receptivity following either estrogen administration or administration of both estrogen and progesterone. Females given oil at birth showed moderate levels of sexual receptivity when administered estrogen alone. Levels increased as estrogen dose was increased. At each dose level, females given oil at birth and estrogen and progesterone in adulthood showed higher levels of receptivity than did females given only estrogen. Male rats, androgenized females, and estrogenized females failed to show significant receptivity at any dose level of estrogen stimulation, regardless of whether or not progesterone was also administered. It was concluded that a major effect of neonatal androgen stimulation, exogenous or endogenous, is an inhibition of the development of estrogen sensitive systems for lordotic behavior. In this regard, neonatal estrogenization appears to mimic the effects of neonatal androgenization.