A comparative approach to the study of dopamine and male sexual behavior: What can Japanese quail teach us? A reply to Pfaus (2010).

One of the most robust findings about dopamine (DA) is that the stimulation of dopaminergic systems promotes the activation of male sexual behavior. The commentary by Pfaus (see record 2010-24688-009) included a thorough review of studies of DA and male sexual behavior. We agree with him that the release of DA in the preoptic region in male quail in response to females and in association with the exhibition of male sexual behavior appears to be highly conserved and that it seems to have evolved very early in the evolutionary history of the vertebrate brain. However, additional data have been collected indicating that there may be significant species differences in the dopaminergic regulation of male behavior in quail compared with rats. In this response, we take the opportunity to make a few broader points about DA and male sexual behavior in light of other studies that have been conducted in birds and introduce some interesting taxonomic variation that is still not well understood. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Dopamine release in the medial preoptic area is related to hormonal action and sexual motivation.

To help elucidate how general the role of dopamine (DA) release in the medial preoptic area (mPOA) is for the activation of male sexual behavior in vertebrates, we recently developed an in vivo microdialysis procedure in the mPOA of Japanese quail. Using these techniques in the present experiment, the temporal pattern of DA release in relation to the precopulatory exposure to a female and to the expression of both appetitive and consummatory aspects of male sexual behavior was investigated. Extracellular samples from the mPOA of adult sexually experienced male quail were collected every 6 min before, while viewing, while in physical contact with, and after exposure to a female. In the absence of a precopulatory rise in DA, males failed to copulate when the barrier separating them from the female was removed. In contrast, males that showed a substantial increase in mPOA DA during precopulatory interactions behind the barrier, copulated with females after its removal. However, there was no difference in DA during periods when the quail were copulating as compared to when the female was present but the males were not copulating. In addition, we show that precopulatory DA predicts future DA levels and copulatory behavior frequency. Furthermore, the size of the cloacal gland, an accurate indicator of testosterone action, is positively correlated with precopulatory DA. Taken together, these results provide further support for the hypothesis that DA action in the mPOA is specifically linked to sexual motivation as compared to copulatory behavior per se. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Electrical stimulation of dorsal and ventral striatum differentially alters the copulatory behavior of male rats.

Sexual behavior is a natural reward that activates striatal dopaminergic (DA) circuits, and dopamine exerts a facilitative influence on copulation. Electrical stimulation of the striatum has been shown to be rewarding, but its effect on male sexual behavior display has not been established. The objective of the present work was to assess the effects of low- and high-frequency electrical stimulation of the dorsal and ventral striatum on male rat sexual behavior expression. To this aim, copulatory activity of sexually experienced male rats was recorded during electrical stimulation of the nucleus accumbens (NAcc) or caudate-putamen (CP), at each stimulation frequency, before and after sexual exhaustion. Results showed that electrical stimulation of the NAcc at both frequencies increased the number of ejaculations that male rats were able to show in a 30-min period. By contrast, stimulation delivered to the CP inhibited sexual behavior by slowing its display. Each effect was more pronounced at low than at high stimulation frequencies. In the same rats, once sexually exhausted, electrical stimulation of these brain areas did not reverse the sexual behavior inhibition that characterizes the sexual exhaustion state. It is concluded that dorsal and ventral striatal DA brain regions exert opposite influences on copulatory behavior expression of sexually experienced male rats. Also, that the facilitative effect of NAcc electrical stimulation on sexual activity, with the stimulation parameters used, cannot surmount the sexual behavior inhibition resulting from copulation to satiation. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Dopamine release in the medial preoptic area of female rats in response to hormonal manipulation and sexual activity.

Dopamine (DA) is responsive to hormonal manipulations and has been implicated in the regulation of female rat sexual behavior. In the present studies, extracellular DA levels were assessed in the medial preoptic area (MPOA) of ovariectomized female rats in response to exogenous ovarian hormones and during sexual activity. In female rats primed with a low dose of estradiol benzoate (2 μg), but not with a higher dose (20 μg), a 500-μg progesterone injection increased extracellular DA and facilitated copulatory behavior. Extracellular DA levels in the MPOA were further augmented during sexual interactions with a male rat in a nonpacing copulatory chamber by either perineal or vaginal stimulation. However, in a pacing chamber, DA efflux did not increase, although the metabolites rose significantly during copulation. Together, these findings suggest that extracellular DA in the MPOA responds to the hormonal state of the female rat and may contribute to her expression of sexual behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Increased extracellular dopamine in the nucleus accumbens and striatum of the female rat during paced copulatory behavior.

Five groups of ovariectomized rats were tested during in vivo microdialysis, and concentrations of dopamine (DA) and its metabolites were determined in dialysate. In striatum, DA increased more in hormone-primed ovariectomized female rats pacing copulation than in those engaging in sex that could not pace, those that were hormone primed but tested without a male present, or oil-treated groups. Administration of estrogen before microdialysis resulted in enhanced striatal DA in response to a male rat relative to the animals tested without a male. Female rats that were pacing sexual behavior also exhibited a greater increase in accumbens DA than did the no-male, estrogen-primed, or oil-treated groups. Nonpacing animals displayed a significant decrease in DA from accumbens 30 min after introduction of the male rat but otherwise were not different from pacing animals. Estrogen-treated animals also had an enhanced increase in accumbens DA compared with oil-treated rats. These data suggest that DA release in the striatum and accumbens is dependent on the context in which sexual behavior occurs and that estrogen may in part modulate these dopaminergic responses. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Activation of POMC neurons during general arousal but not sexual behavior in male rats.

Exogenous opioids influence male rat sexual behavior, suggesting that endogenous opioid peptides are released during mating. Supporting this hypothesis, the authors recently showed that mating induced activation of mu opioid receptors. However, it is unknown which ligand(s) is acting on these receptors during mating. The current set of experiments tested the hypothesis that beta-endorphin-producing neurons, that is, proopiomelanocortin (POMC) neurons, are activated during sexual behavior. Mating-induced activation of POMC neurons was investigated during either the dark phase or the light phase, following different components of male rat sexual behavior or following control manipulations that resulted in general arousal. Results show activation of POMC neurons in the mediobasal hypothalamus following general arousal but not specifically related to sexual behavior per se. In addition, mating did not activate the subpopulation of POMC neurons that project to the medial preoptic nucleus. These results suggest that it is unlikely that POMC neurons contribute to the action of endogenous opioids in the brain area during sexual behavior but instead may contribute to the change in arousal state essential for the expression of sexual behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sexual experience increases nitric oxide synthase in the medial preoptic area of male rats.

Nitric oxide in the medial preoptic area (MPOA) is important for the expression and sensitization of male sexual behavior. In this article, the authors report that repeated sexual experience (mating for 2 hr on each of 3 days) increased levels of nitric oxide synthase (NOS) in the MPOA of male rats, regardless of whether they mated on the day they were given an overdose of sodium phenobarbital. This effect resulted from the previous experience and not acute mating, as NOS was not increased 2 hr after the first mating in previously naive males. Experience-induced increases in NOS in the MPOA may be one mechanism through which sexual experience facilitates sexual behavior in male rats. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Mating activates NMDA receptors in the medial preoptic area of male rats.

Studies have emphasized the role of the medial preoptic area (MPOA) as an important site for the regulation of male sexual behavior. Indeed, ablations of the MPOA impair sexual behavior, whereas stimulation of the MPOA enhances behavior. Furthermore, neural activity in the MPOA increases with mating. The current study tested the hypothesis that activation of N-methyl-D-aspartate (NMDA) receptors occurs in MPOA neurons and is essential for the expression of male sexual behavior in rats. Results indicate that nearly all MPOA neurons that expressed Fos following mating also contained the NR1 subunit of NMDA receptors. Furthermore, mating increased phosphorylation, thus activation, of NR1 in the MPOA. Additionally, blocking NMDA receptors significantly decreased mating-induced Fos expression and mating-induced phosphorylation of NMDA receptors and impaired male sexual behavior. These results provide evidence that mating activates NMDA receptors in the MPOA and that this activation is important for the expression of male sexual behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Effects of ibotenic acid lesions of the nucleus accumbens on paced mating behavior in the female rat.

The present study investigated the role of the nucleus accumbens (NAcc) in paced mating behavior in female rats. A sexually receptive female rat will approach and withdraw from a sexually active male, thereby controlling the timing of the receipt of sexual stimulation (e.g., mounts, intromissions, ejaculations). In this study, ibotenic acid lesions in the NAcc core increased the likelihood that a female rat would withdraw from a male rat after a mount but did not affect contact return latency or sexual receptivity. lbotenic acid lesions in the NAcc shell did not affect paced mating behavior or sexual receptivity. The results suggest that the NAcc core plays a role in suppressing withdrawal behavior in response to less intense mating stimulation. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

An NMDA antagonist impairs copulation and the experience-induced enhancement of male sexual behavior in the rat.

Sexual experience facilitates subsequent male sexual behavior; activation of the N-methyl-D-aspartate (NMDA) glutamate receptor may play a role in this experience-induced enhancement. In this article, the authors report that systemic injections of MK-801, an NMDA receptor antagonist, impaired male sexual behavior in sexually naive and sexually experienced male rats. Furthermore, saline-treated rats that received 7 daily exposures to an inaccessible estrous female instead of sexual experience displayed enhancement of copulation on the following day. Injections of MK-801 before each of these exposures inhibited the experience-induced enhancement on the drug-free test on Day 8. These data suggest that stimulation of NMDA receptors enhances sexual performance immediately and mediates the experience-induced enhancement of subsequent copulatory behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Serotonin impairs copulation and attenuates ejaculation-induced glutamate activity in the medial preoptic area.

The medial preoptic area (MPOA) is critical for male sexual behavior. Glutamate is released in the MPOA of male rats during copulation, and increasing glutamate levels by reverse dialysis of glutamate uptake inhibitors facilitates mating. Conversely, increased release of serotonin (5-HT) inhibits sexual behavior. In both rats and men, selective serotonin reuptake inhibitors (SSRIs) impair erection, ejaculation, and libido. Here we reverse-dialyzed 5-HT through concentric microdialysis probes in the MPOA of male rats; concurrently we collected 2-min samples for analysis of glutamate and measured sexual behavior. Sexual activity, and especially ejaculation, increased levels of glutamate in the MPOA. However, reverse dialysis of 5-HT into the MPOA impaired ejaculatory ability and attenuated glutamate release. Implications of these results for impairment of sexual behavior that results from administration of SSRIs are discussed. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Is sexual motivational state linked to dopamine release in the medial preoptic area?

The medial preoptic area (mPOA) is a key site for the dopaminergic enhancement of male sexual behavior. Dopamine release increases in the rat mPOA with mating, supporting the critical stimulatory role played by preoptic dopamine on male sexual behavior. However, it has been questioned whether dopamine is specifically related to the occurrence of male sexual behavior and not simply involved in general arousal. To address this question, we asked whether dopamine release in the mPOA is linked to the production of male sexual behavior in Japanese quail (Coturnix japonica), a species that exhibits a much shorter temporal pattern of copulation than rats and does not have an intromittent organ, resulting in a very different topography of their sexual response. Extracellular samples from the mPOA of adult sexually experienced male quail were collected every 6 min before, during, and after exposure to a female using in vivo microdialysis and analyzed using high-performance liquid chromatography with electrochemical detection. Extracellular dopamine significantly increased in the presence of a female and returned to baseline after removal of the female. However, quail that failed to copulate did not display this increased release. These findings indicate that it is not solely the presence of a female that drives dopamine release in males, but how a male responds to her. Furthermore, in quail that copulated, dopamine release did not change in samples collected during periods of no copulation. Together, these findings support the hypothesis that dopamine action in the mPOA is specifically linked to sexual motivation and not only to copulatory behavior or physical arousal. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sex-related alcohol expectancies predict sexual risk behavior among severely and persistently mentally ill adults.

Three hundred three adults (57% male, average age 42 years) with severe and persistent mental illness receiving treatment at community mental health clinics completed a survey, which included B. C. Leigh's (1990) sex-related alcohol expectancy scale and measures of alcohol use and sexual risk behavior. Hierarchical logistic regression analyses, controlling for drinking behavior, revealed that participants with stronger expectancies that drinking would lead to enhanced sexual experience were more likely to have drank prior to intercourse and that, among participants who drank prior to intercourse, those with stronger expectancies that alcohol would lead to riskier sexual behavior were more likely to have engaged in sexual risk behavior. Implications for preventing HIV infection among people with severe mental illness are discussed. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Aggression in male mice lacking functional estrogen receptor α.

Estrogen receptor alpha knockout (ERαKO) male mice fail to display sexual behavior. The authors hypothesized that ERαKOs require higher testosterone (T) concentrations than wild-type (WT) males to exhibit copulatory behavior. Increasing T stimulated sexual behavior and preference for females in WT males but failed to do so in ERαKOs. However, T did induce female-directed aggression in ERαKOs. In aggression tests, WT residents selectively attacked T-treated male intruders. ERαKO residents attacked female, T-treated male, and estrogen-treated male intruders equally. Increased access to olfactory cues prior to direct contact reduced overall aggression in ERαKO versus WT males but did not cause ERαKOs to differentially attack male and female opponents. Results suggest that ERα is essential for normal social behavior, perhaps via processing of chemoinvestigatory cues, which are required to discriminate males from females. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

"Maternal Stress and Pituitary-Adrenal Manipulations During Pregnancy in Rats: Effects on Morphology and Sexual Behavior of Male Offspring"; Corrections to Chapman and Stern.

Reports an error in the original article by Robert H. Chapman and Judith Stern (Journal of Comparative and Physiological Psychology, 1978, Vol. 92[6], pp. 1074-1083). On p. 1081, paragraph 2, line 27, "handling" should read "group housing." Reference Note 3 should be a Reference entry: Dunlap, J. L., Zadina, J. E., & Gougis, G. Prenatal stress interacts with prepubertal social isolation to reduce male copulatory behavior. (The following abstract of this article originally appeared in record 1980-08973-001.) Investigated whether the demasculinizing and feminizing effects of prenatal stress (i.e., stress applied to the mother during pregnancy) in rats reported previously by I. L. Ward (1972) are mediated by activation of the maternal pituitary-adrenal axis. Neither whole-body restraint, with or without hyperthermia, nor ACTH treatment during the last third of gestation had any reliable effect on masculine or feminine sexual behavior in male Sprague-Dawley offspring, although these treatments produced maternal pathology and evidence of maternal adrenocorticoid release. Significant littermate similarity was found for almost every morphological and behavioral measure. Failure to control for the litter variable may account for many previously reported effects of prenatal stress on sexual behavior in rats. The discrepancy between the present and earlier findings is discussed in terms of methodological and theoretical considerations. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sexual behavior in young adulthood: A population-based twin study.

Objective: With behavior genetic analyses of data from young adult twins, we evaluated theoretical perspectives that differentially emphasize biological dispositions, social/cultural factors, or universal pathways to explain individual differences in sexual behaviors. Design: We fit biometric sex limitation models to three aspects of sexual behavior reported by 4,925 Finnish twins ages 23-27. Main Outcome Measure: From a postal questionnaire, we obtained self-report information on initiation/abstinence of sexual intercourse, onset age, and number of sexual partners. Results: Genetic and non-shared environmental influences were significant for all three measures. There were trends for common environmental influences on initiation and, in females, age at first intercourse. Some differential effects in males and females were found. Results comparing onset age and number of partners among experienced twins from pairs concordant and discordant for initiation found genetic and environmental influences on initiation/abstinence overlapped those found for the other aspects of sexual behavior. Conclusions: These results document genetic variation in individual differences in sexual behavior of young adults. Incorporating genetic dispositions into integrated models of sexual behavior will facilitate more effective health promotion and risk taking intervention. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Comparative effects of the N-methyl-D-aspartate antagonist MK-801 and the calcium channel blocker KB-2796 on neurologic and metabolic recovery after spinal cord ischemia

The effects of maternal exposure to picrotoxin (PT) during the prenatal and postnatal periods of sexual brain differentiation were studied. Behavioral (sexual behavior), physical (sexual maturation, body, and organ weights) and neurochemical (striatal and hypothalamic monoamine and respective metabolite levels) data were assessed in the offspring of PT-treated dams. The following results were obtained: 1) sexual maturation as measured by the day of testis descent and testis weight comparison was unchanged; 2) a decrease in male sexual behavior occurred, as well as a decrease in body, ductus deferens, and seminal vesicle weights and in plasma testosterone levels of adult male offspring; 3) striatal dopamine (DA) and homovanillic acid (HVA) levels were decreased and hypothalamic norepinephrine (NE) levels were increased. These results indicate that perinatal exposure to PT during the critical periods of male brain sexual differentiation has long-term effects on the reproductive physiology and behavior of male rats.     

Differential behavioral response to dopamine D? agonists by sexually naive, sexually active, and sexually inactive male rats.

This study was performed with male rats categorized as sexually active (SN), sexually active (SA). or sexually inactive (SI). In a first experiment the effects of the dopamine (DA) D? agonist SND 919 (0.05, 1, and 10 mg/kg) on the copulatory behavior of SN, SA. and SI rats were assessed. In a second experiment the DA D? agonist B-HT 920 (0.2 mg/kg) was used, and examination was limited to SN and SA rats. The effects exerted on stretching-yawning, penile erection, and sedation by the same compounds at the same doses in these three rat categories were also investigated. The main findings were that SND 919 and B-HT 920 facilitated ejaculation in SA rats, and that the rats that were different as regards level of sexual activity exhibited different behavioral responses to the two DA agonists. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Opioids and sexual behavior of male rats: Involvement of the medial preoptic area.

Local infusion of β-endorphin (β-END) into the medial preoptic area (MPOA) dose-dependently impaired the gating of the copulatory response and the execution of the sexual performance of sexually experienced, intact male rats. Local naloxone treatment prevented the impairment of the sexual response by β-END, but failed to facilitate unimpaired copulation. Local infusion into the MPOA of equimolar doses of α-endorphin, dynorphin-A-(1-17) or met-enkephalin were less effective than β-END. It is suggested that endogenous opioid systems in the MPOA are normally quiescent, and increased activity may be related to disrupted or inhibited male sexual behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Naloxone blocks place preference conditioning after paced mating in female rats.

Sexual behavior in male rats induces a positive affect as evaluated by conditioned place preference (CPP). In addition, when females control or "pace" the rate of sexual interaction, a clear CPP is also observed. The reward state induced by mating in male rats is blocked by the injection of the opioid antagonist naloxone. In the present experiment, a dose of 4 mg/kg of naloxone completely blocked the CPP induced in females by paced mating. It appears that a common opioid system is involved in the positive affect induced by sexual behavior in both male and female rats. (PsycINFO Database Record (c) 2010 APA, all rights reserved)