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Patterns of motor and seminal vesicle activities during copulation in the male rat.

The interaction between behavioral and visceral events during copulation was studied in nine intact adult male Wistar rats. The motor copulatory pattern was analyzed by an accelerometric technique and the seminal vesicle pressure (SVP) was recorded through a catheter chronically inserted into the right seminal vesicle. Mounting was associated with a small broad rise in SVP that often preceded the initiation of pelvic thrusting. Penile insertion resulted in a second sharp rise in SVP superimposed on the primary wave related to mounting. A steep rise in SVP occurred during the performance of the motor ejaculatory pattern after a variable period of intravaginal thrusting. This final rise was associated with ejaculation. Analysis of the temporal relationships ships between the SVP changes and copulatory behavior revealed that each of the three rises of SVP was related to distinct patterns of stimulation, suggesting that they were mediated by separate reflex arcs.

Animals↗

Hypothalamic temperature and deep body temperature during copulation in the male rat.

The medial preoptic area (MPOA) of the hypothalamus is involved in both the expression of male sexual behavior and the regulation of physiological temperature. This duality of function led us to ask whether arousal, intromission, and ejaculation are accompanied by a distinctive temperature profile. Using telemetric thermosensors, we monitored MPOA temperature and deep body temperature during copulation in the male rat. Changes in MPOA temperature were highly uniform, more so than changes in body temperature. The MPOA heated prior to ejaculation, cooled rapidly following ejaculation and then began to heat again coincident with the termination of the post-ejaculatory refractory period. These changes could not be related to variations in general activity. The most striking change in MPOA temperature, rapid cooling following ejaculation, was explained in terms of certain behaviorally-induced hemodynamic events.

Animals↗

How the nose cools the brain during copulation in the male rat.

Copulation in the male rat is accompanied by a progressive increase in both body temperature and hypothalamic temperature and, soon after ejaculation, by a rapid and selective decrease in hypothalamic temperature. We hypothesized that two changes occur in tandem within the vasculature of the nasal mucosa that contribute, respectively, to hypothalamic heating and hypothalamic cooling. The first takes place prior to ejaculation and involves mucosal vasoconstriction and warm venous blood flowing from the nose to the base of the brain. We thought of such warm blood as retarding heat loss from the hypothalamus. The second takes place immediately following ejaculation and involves the same venous blood, but now cool owing to an abrupt dilation of nasal blood vessels. We hypothesized that such cool venous blood is largely responsible for the observed postejaculatory reduction in hypothalamic temperature. To test our hypothesis, we measured temperature at the surface of the nasal mucosa and in the hypothalamus during successive copulatory bouts. In accord with prediction, we found a reduction in mucosal-surface temperature prior to ejaculation (reflecting vasoconstriction and heat retention) and a substantial rise in mucosal-surface temperature following ejaculation (reflecting vasodilation and heat dissipation). Accompanying these changes in nasal vasomotor tone was a progressive preejaculatory rise in hypothalamic temperature and a rapid postejaculatory decrease. We conclude that nasal venous blood modulates the temperature of the ventral brain through conductive heat exchange and that such heat exchange is conspicuous during sexual behavior.

Animals↗

Dissociation of hypothalamic effects on ultrasound production and copulation.

Two studies were conducted to compare the brain mechanisms for copulation with those controlling other sexual behaviors, such as the ultrasonic calls that help hamsters and other rodents attract potential mates. Specifically, male and female golden hamsters were castrated and hormone-primed prior to being observed for rates of ultrasound production and levels of sex-typical copulatory behavior (mounts, intromissions and ejaculations in males; lordosis in females). Such tests were conducted before and after subjects received sham operations or bilateral lesions of the preoptic area (POA), anterior hypothalamus (AH) or ventromedial hypothalamus (VMN). The results confirmed previous work in showing the POA lesions decrease rates of intromission, ejaculation and ultrasound production, while VMH lesions decrease lordosis duration. More surprising was the tendency of VMN lesions to increase rates of ultrasonic calling by both males and females. For males, these effects identify differences between the neural circuits controlling copulatory and noncopulatory sexual behaviors. For females, they suggest a mechanism for the behavioral incompatibility of ultrasound production and lordosis. In particular, they raise the possibility that the suspension of ultrasonic calling that normally accompanies lordosis reflects an increase in VMN activity that simultaneously provokes lordosis and inhibits vocalization.

Animals↗

The effects of depo-medroxyprogesterone acetate (DMPA) on copulation-related and agonistic behaviors in an island colony of stumptail macaques (Macaca arctoides).

This study examined the effects on copulation-related and agonistic behaviors of repeated DMPA (depo-Provera) treatment of adult females in a heterosexual island colony of stumptail macaques (Macaca arctoides). Comparison of mean rates revealed a decrease in male approach to females and dominant male following of females after they were treated with DMPA. As treatment did not affect female genital present, female approach or follow of males, we conclude, consistent with earlier results, that DMPA primarily reduced female sexual attractiveness. DMPA treatment was also consistently associated with increased female agonistic behavior (i.e., low-level threat, bite, and fear grimace), with aggression directed primarily at subadults, juveniles, and infants. Treatment did not alter dominance relationships. These data suggest that DMPA treatment is associated with increased low-key contact aggression.

Aggression↗

Fetal uterine position affects copulation and scent marking by adult male gerbils.

Those male Mongolian gerbils (Meriones unguiculatus) that as fetuses resided in uterine locations adjacent to no females, when adult, scent marked more frequently, mounted estrous females with shorter latencies, and ejaculated after fewer intromissions than did those male gerbils that as fetuses resided in uterine locations adjacent to two females. Both the scent-marking frequencies and copulatory patterns of adult males were positively correlated with three indices of their circulating levels of testosterone: ventral gland size, anogenital distance, and relative testes weights. Also, those males that scent marked relatively frequently copulated more reliably than did those males that scent marked relatively infrequently.

Androgens↗

Electromyographic analysis of male rat perineal muscles during copulation and reflexive erections.

Anatomical examination of the ventral bulbospongiosus (BS) muscle suggested that its proximal and distal portions may act during penile erection as a two-stage pump governing the intensity of glans erections. The coordination between these portions of the BS, and of the proximal BS with the ischiocavernosus (IC) muscle, was studied using electromyographic (EMG) recordings taken during copulation and reflexive erections. Mounts without intromission were accompanied by either strong IC activity with little or no proximal BS activity, or strong proximal BS activity preceding the onset of IC activity. Activity in the proximal BS during mounts was variable in both duration and amplitude but uniform in frequency. During mounts with intromission, EMG activity of the proximal BS consisted of two characteristic phases, an early phase of low-amplitude activity which was similar to proximal BS activity during nonintromissive mounts, followed by an intromissive phase of high-amplitude, high-frequency activity. During intromission patterns, IC activity reliably preceded proximal BS activity. Ejaculations were accompanied by stronger proximal BS activity than were other copulatory events and were followed by a series of proximal BS and IC bursts lasting for 10-20 seconds. During reflexive erections, EMG activity in the proximal BS was always fusiform and varied with the intensity of erection only in frequency. In contrast to the proximal BS, activity in the distal BS was similar in frequency and amplitude across copulatory and reflexive events. These findings suggest that: a) different motoneuron pools serve the different portions of the BS muscle; b) the distal BS does not differentially affect glans erection but may serve primarily to promote rigidity of the portion of the bulb that it surrounds, while the proximal BS acts as the variable aspect of a hypothetical two-stage pump, and c) activity in the IC must precede activity in the proximal BS to achieve intromission.

Animals↗

p-Chlorophenylalanine alters pacing of copulation in female rats.

When tested in apparatus that allowed them to determine their contacts with conspecifics, including sexually active male rats, estrogen- and progesterone-treated female rats systemically treated with para-chlorophenylalanine (PCPA), a tryptophan hydroxylase inhibitor, showed reduced frequency of coital contacts and reduced duration of interactions with sexually active males. PCPA administration did not alter contacts with noncopulating males or other females nor did treated females differ from controls in ability to display lordosis or posing, both stereotyped behaviors characteristic of female rats in behavioral estrus. It is suggested that the alteration of temporal pacing of copulation in the PCPA-treated females is a result of drug-induced changes in the processing of exteroceptive stimuli.

Animals↗

D2 receptors in the paraventricular nucleus regulate genital responses and copulation in male rats.

The D2 dopamine receptor agonist quinelorane (LY-163502), microinjected into the paraventricular nucleus (PVN), affected genital response of restrained supine male rats in a biphasic dose-dependent fashion. A moderate dose (1 microgram) facilitated penile responses (intense erections and penile movements), and decreased the latency to the first response. A high dose of quinelorane (10 micrograms) facilitated seminal emission while inhibiting penile responses. The addition of the D1 antagonist SCH-23390 to the 1 microgram dose of quinelorane potentiated quinelorane's increase in seminal emission. We suggest that D1 receptors in the PVN may be antagonistic to D2 receptor-mediated seminal emission, and possibly also penile responses. In copulation tests 1 microgram quinelorane decreased mount latency, whereas 10 micrograms quinelorane increased mount and intromission latencies and slowed copulatory rate. Both 1 and 10 micrograms quinelorane, and also 1 and 10 micrograms of the mixed D1 and D2 agonist apomorphine, decreased the number of intromissions preceding ejaculation.

Animals↗

Sexual attraction and copulation in male rats: effects of the dopamine agonist SND 919.

Behavioral differences towards receptive females, involving latency to the first contact, amicable behavior, genital exploration, and copulatory pattern, were seen in sexually active (A), sluggish (S), and inactive (I) male rats classified on the basis of 11 consecutive mating tests. The D2 dopamine agonist SND 919 (1 mg/kg) was intraperitoneally administered to the three groups 25 min before a 12th test; the drug stimulated the copulatory behavior of A and S but not of I rats in which it diminished genital exploration and amicable behavior. In a 13th test, conducted 1 week later, 31% of I initiated mating, 16% of them reaching ejaculation. The stimulant effect of SND 919 on copulation in A rats was confirmed in further experiments where it was injected at 0.1 mg/kg, a dose selective for the D2 autoreceptors.

Animals↗

Electromyographic activity of rat ischiocavernosus muscles during copulation after treatment with a GABA-transaminase inhibitor.

The administration of GABA-transaminase inhibitors (GABA-TIs) to male rats reduces the proportion of mounts that result in intromissions. Copulatory pelvic thrusting remains normal, despite the fact that animals treated with GABA-TIs show gross deficiencies in other motor acts. In order to determine whether altered sexual behavior produced by GABA-TI could be due to deficiencies in activity of striated penile muscles, we recorded the electromyographic (EMG) activity of the ischiocavernosus (IC) muscle during copulation in male rats treated with sodium valproate. The duration of IC EMG bursts was reduced by sodium valproate in separate tests that allowed or prevented intromission. There was no effect on EMG amplitude or frequency. It is suggested that insufficient activity of the IC muscles reduces the likelihood of vaginal penetration. The actions of GABA may be localized to hypothalamic or brain stem nuclei with GABAergic projections to the spinal motoneurons controlling the IC muscles, or GABA may act directly on these neurons.

4-Aminobutyrate Transaminase↗

Increased dopamine release in the nucleus accumbens of copulating male rats as evidenced by in vivo voltammetry.

This report describes the changes in extracellular levels of dopamine (DA) and dihydroxyphenylacetic acid (DOPAC) detected in the nucleus accumbens of male rats engaged in copulatory activity. They were monitored by using differential normal pulse voltammetry (DNPV) with electrochemically pretreated carbon fiber microelectrodes and numerical analysis of the catechol signal. The copulatory pattern displayed during the voltammetric recordings was similar to those recorded prior to surgery. Copulating animals showed a conspicuous increase in the DA and DOPAC electrochemical signals up to, respectively, 170% and 150% of baseline levels. This response was much attenuated when the experimental animals were exposed to either non-receptive castrated females or intact males. These data are consistent with the permissive role currently ascribed to the dopaminergic innervation of the n. accumbens in the selection and the initiation of behavioral adaptive sequences.

3,4-Dihydroxyphenylacetic Acid↗

Experimental manipulation of male behaviour during copulation in Stenomacra marginella (Heteroptera: Largidae): effect on copula duration, female remating and oviposition.

Apparently stimulatory male copulatory behaviour (MCB) is widespread among arthropods and it could help males to increase their fitness by inducing favourable behavioural and physiological changes in females. The empirical study of female responses to MCB is hindered because its experimental manipulation is difficult. We have developed a technique for reducing, with minimal disturbance, the frequency of MCB in the true bug Stenomacra marginella. Here, we test the idea that, in a polygamous species like S. marginella, sexual selection favours males whose MCB induces females to increase copula duration (thereby increasing the amount of sperm and accessory substances transferred), reduce their sexual receptivity to additional males and increase their rate of oviposition. Males prevented from performing MCB increased their rate of attempts to perform MCB. Copulations with previously mated females were of longer duration than those with virgin females, probably as a male adaptation for sperm competition, and MCB could have played a role in inducing this effect. Partial or total experimental reduction of MCB frequency had no effect on remating rates, because most females accepted remating at the first opportunity (1 day after their first copula). The probability of egg laying was reduced in females whose first mate was partially prevented from performing copulatory courtship, but not in females whose first mate was completely prevented from performing copulatory courtship. This is an intriguing result and further experiments are needed to understand its causes. We hypothesize that MCB evolved as a result of sexual selection.

Animals↗

Effects of testosterone on the development of neuromuscular systems and their target tissues involved in courtship and copulation in green anoles (Anolis carolinensis).

Male green anole lizards court females using a red throat fan (dewlap) and copulate by intromitting one of two penises (hemipenes). These structures begin sexually monomorphic, but by adulthood males have larger dewlaps, only males have hemipenes, and many of the neuromuscular components of both systems show male-biased dimorphisms. We hypothesized that testosterone (T), which increases in juvenile males but not females about a month after hatching, facilitates masculinization. To test this idea, on post-hatching day 30, gonadally intact females received either a blank or T implant, and males were either castrated or sham-castrated. At day 90, juveniles were euthanized and the length of the cartilage and cross-sectional areas of the muscle fibers and motoneurons required for dewlap extension were examined. We also measured the cross-sectional areas of the hemipenes and associated muscle fibers and motoneurons, and counted the motoneurons. T-treated females had longer cartilages and larger dewlap muscle fibers compared to those with blank implants. No effects on motoneurons were detected, and no females possessed hemipenes or associated musculature. In males, castration produced shorter dewlap cartilages and smaller hemipenes; other measures were not affected by treatment. These data indicate that components of the dewlap system differentiate relatively late in development, that T likely mediates the process, and that although components of the copulatory system are plastic in juvenile males, sexual differentiation of peripheral features is complete before day 30. The data also suggest that target structures (dewlap cartilage and hemipenes), compared to their neuromuscular effectors, are particularly sensitive to developmental T exposure.

Androgens↗

The development of rabbit ovarian follicles following copulation.

The morphologic development of rabbit ovarian follicles was studied by means of light and electron microscopy 0, 2, 4, 6, 8, and 10 hours after copulation. The progressive changes at the apex of the follicle included extensive edema, hyperemia, and rupture of blood vessels, and then rupture of the follicular wall. Ovulation occurred when the cohesive forces in the cellular layers of the follicular apex became less than the physical forces within the follicle. Most of the morphologic changes in the follicle as it approached ovulation could be related to the effects of locally produced estrogens.

Animals↗

Disparate effects of small medial amygdala lesions on noncontact erection, copulation, and partner preference.

Male rats with radiofrequency lesions in the anterior medial amygdala (MeAa) or the posterior medial amygdala (MeAp), respectively, were tested for copulation and for noncontact erection (NCE; evoked by inaccessible estrous females) in a chamber in which the male was located between estrous and anestrous females. Barriers allowed only olfactory and auditory interaction between animals. With conscious females as stimuli, MeAp lesions virtually eliminated NCEs, and MeAa lesions moderately impaired them, without affecting the normal preference for estrous over anestrous females. When tested with anesthetized females to remove auditory stimulation, few males with lesions had NCEs. Only the males with MeAp lesions had a significant reduction in preference for estrous over anestrous anesthetized females. Neither MeAa nor MeAp lesions had an effect on copulatory behavior. MeAp lesions may have caused a reduced sensitivity to--or impaired processing of--estrous odors, thereby preventing NCE without disrupting copulatory behavior.

Amygdala↗

Diversity in cell specific co-expression of four neuropeptide genes involved in control of male copulation behaviour in Lymnaea stagnalis.

We report here the neuron-specific co-expression of four genes coding for neuropeptides involved in the control of male behaviour. These neurons are located in the anterior lobe of the right cerebral ganglion in the central nervous system of Lymnaea stagnalis and project via the penis nerve to the penial complex. In order to accomplish optimal assurance we applied in situ hybridization, immunocytochemistry and matrix-assisted laser desorption ionization mass spectrometry. The anterior lobe neurons express the gene encoding the amidated tetrapeptide APGWamide. Subsets of these cells are now shown to co-express the APGWamide gene exclusively with one of three other neuropeptide genes, encoding Lymnaea neuropeptide Y, conopressin or pedal peptide, respectively. All four genes are also expressed in other neurons in other centres projecting to the penial complex, but in these cells co-expression was not observed. The neuropeptides encoded by the genes could be identified in the anterior lobe cell bodies on the basis of immunocytochemistry and mass spectrometrical analysis. The neuropeptides APGWamide and Lymnaea neuropeptide Y, which are co-localized in the anterior lobe cells as well as in axons innervating the penis retractor muscle, do not induce muscle contraction but have a modulatory action by affecting the relaxation rate and amplitude of the contraction. APGWamide and conopressin had earlier been suggested to modulate peristalsis of the vas deferens. Thus, it seems that the neurons co-expressing the various combinations of neuropeptide genes in the anterior lobe represent functional units, each acting in the fine tuning of different muscles involved in specific aspects of male copulation behaviour.

Animals↗

Angiotensin I-converting enzyme (ACE) activity of the tomato moth, Lacanobia oleracea: changes in levels of activity during development and after copulation suggest roles during metamorphosis and reproduction.

Angiotensin I-converting enzyme (ACE) is a dipeptidyl carboxypeptidase that removes C-terminal dipeptides from relatively short oligopeptides, usually smaller than 15 amino acids. In mammals, the enzyme has several important roles in the metabolism of vasoactive peptides, but its physiological role in insects is not fully understood. We now report the properties of an ACE in a lepidopteran species (the tomato moth, Lacanobia oleracea) and suggest new physiological roles for the enzyme in this insect. ACE activity increases four-fold during the last stadium and in early pupae, a rise which, in its timing, is similar to what has been observed previously in the transition of larva to pupa in Drosophila melanogaster. This suggests that the increase in ACE activity might be of general importance for peptide metabolism during metamorphosis in holometabolous insects. High levels of ACE activity were found in the haemolymph of sixth stadium larvae and adult insects, and in the reproductive tissues of both male and female adults. Almost all of the ACE activity in the reproductive tissues was found in the accessory glands of the male and the spermatheca and bursa copulatrix of the female. The decline in accessory gland ACE in mated males and the concomitant rise in ACE activity in the spermatheca and bursa copulatrix of the female suggested the transfer of ACE from the male to the female during copulation. Using several convenient peptides as substrates, we have shown that the spermatophore/bursa copulatrix taken from mated female insects possess an aminopeptidase, a carboxypeptidase and a dipeptidase, in addition to high levels of ACE. These peptidases might be involved in the breakdown of proteins to peptides and eventually to amino acids in the spermatophore. Evidence for such a proteolytic pathway and its role in providing substrates for the TCA cycle has been obtained previously in a study of reproduction in Bombyx mori.

Amino Acid Sequence↗