How Hot Are They? Neural Correlates of Genital Arousal: An Infrared Thermographic and Functional Magnetic Resonance Imaging Study of Sexual Arousal in Men and Women.

BACKGROUND: The few studies that have examined the neural correlates of genital arousal have focused on men and are methodologically hard to compare. AIM: To investigate the neural correlates of peripheral physiologic sexual arousal using identical methodology for men and women. METHODS: 2 groups (20 men, 20 women) viewed movie clips (erotic, humor) while genital temperature was continuously measured using infrared thermal imaging. Participants also continuously evaluated changes in their subjective arousal and answered discrete questions about liking the movies and wanting sexual stimulation. Brain activity, indicated by blood oxygen level-dependent (BOLD) response, was measured using functional magnetic resonance imaging. OUTCOMES: BOLD responses, genital temperature, and subjective sexual arousal. RESULTS: BOLD activity in a number of brain regions was correlated with changes in genital temperature in men and women; however, activation in women appeared to be more extensive than in men, including the anterior and posterior cingulate cortex, right cerebellum, insula, frontal operculum, and paracingulate gyrus. Examination of the strength of the correlation between BOLD response and genital temperature showed that women had a stronger brain-genital relation compared with men in a number of regions. There were no brain regions in men with stronger brain-genital correlations than in women. CLINICAL TRANSLATION: Our findings shed light on the neurophysiologic processes involved in genital arousal for men and women. Further research examining the specific brain regions that mediate our findings is necessary to pave the way for clinical application. STRENGTHS AND LIMITATIONS: A strength of the study is the use of thermography, which allows for a direct comparison of the neural correlates of genital arousal in men and women. This study has the common limitations of most laboratory-based sexual arousal research, including sampling bias, lack of ecologic validity, and equipment limitations, and those common to neuroimaging research, including BOLD signal interpretation and neuroimaging analysis issues. CONCLUSIONS: Our findings provide direct sex comparisons of the neural correlates of genital arousal in men and women and suggest that brain-genital correlations could be stronger in women. Parada M, Gérard M, Larcher K, et al. How Hot Are They? Neural Correlates of Genital Arousal: An Infrared Thermographic and Functional Magnetic Resonance Imaging Study of Sexual Arousal in Men and Women. J Sex Med 2018;15:217-229.

Neural Representation of Subjective Sexual Arousal in Men and Women.

INTRODUCTION: Studies investigating brain indices of sexual arousal have begun to elucidate the brain's role in processing subjective arousal; however, most research has focused on men, used discrete ratings of subjective arousal, and used stimuli too short to induce significant arousal in women. AIM: To examine brain regions modulated by changes in subjective sexual arousal (SSA) rating intensity in men and women. METHODS: Two groups (20 men, 20 women) viewed movie clips (erotic or humorous) while continuously evaluating changes in their SSA using a Likert-like scale (0 = not aroused, 10 = most aroused) and answering discrete questions about liking the movies and wanting sexual stimulation. Brain activity was measured using functional magnetic resonance imaging. MAIN OUTCOME MEASURES: Blood oxygen level-dependent responses and continuous and discrete measurements of sexual arousal. RESULTS: Erotic movies induced significant SSA in men and women. No sex difference in mean SSA was found in response to the erotic movies on continuous or discrete measurements. Several brain regions were correlated with changes in SSA. Parametric modulation with rating intensity showed a specific group of regions within the parietal lobe that showed significant differences in activity among low, medium, and high SSA. CONCLUSION: Multiple regions were concordant with changes in SSA; however, a subset of regions in men and women was modulated by SSA intensity, a subset previously linked to attentional processes, monitoring of internal body representation, and processing of sensory information from the genitals. This study highlights that similar brain regions are activated during subjective assessment of sexual arousal in men and women. The data further highlight the fact that SSA is a complex phenomenon made up of multiple interoceptive and attentional processes.

Vaginocervical stimulation attenuates the sensitization of appetitive sexual behaviors by estradiol benzoate in the ovariectomized rat.

The acute administration of estradiol benzoate (EB) to the ovariectomized (OVX) rat induces low levels of lordosis while sexually appetitive behaviors (e.g., hops, darts, solicitations) are absent, yet the repeated administration of EB results in a behavioral sensitization in which lordosis is potentiated and sexually appetitive behaviors are induced. We have shown that repeated copulation attenuates the sensitization of appetitive sexual behaviors. Here, we assessed which component of male stimulation during copulation is involved in the attenuation. On 8 occasions, sexually experienced OVX Long-Evans rats were treated with 10µgEB and 48h later assigned to one of six groups that differed in their experience on intermediates tests (2-7). One was given repeated access to a male (EB/Male), and another was placed in the copulation chamber alone (EB/Alone) on intermediate tests. Three groups were given one of three somatosensory stimuli by the experimenter: manual flank stimulation (FLS), clitoral stimulation (CLS), or vaginocervical stimulation (VCS). Finally, the control group was left undisturbed in the animal care facility (ACF). Sexual behaviors were measured on Tests 1 and 8. VCS received from the experimenter (VCS) or from the male during copulation (EB/Male) attenuated the magnitude of the sensitization of appetitive sexual behaviors compared with those that were not brought to the testing rooms (ACF), and the effect was most pronounced on sexual solicitations. These results suggest that VCS received during penile intromission inhibits the sensitization of sexually appetitive behaviors by repeated administration of EB. As such, repeated administration of EB may oppose those mechanisms that induce estrous termination, perhaps by sensitizing inhibitory processes within the ventromedial hypothalamus that typically prevent the display of sexual behaviors (i.e., by facilitating disinhibition).

Clitorodynia: A Descriptive Study of Clitoral Pain.

INTRODUCTION: Clitorodynia is classified as a type of localized vulvodynia. Our knowledge of this problem is limited to case studies and one published report. AIMS: The objective of the present study was to describe quantitatively the clinical characteristics of clitoral pain, to assess interference with sexual function, and to investigate whether clitoral pain is a unitary category. METHODS: One hundred twenty-six women with clitoral pain completed an online questionnaire that assessed demographic information, descriptive pain characteristics, intensity and impact on daily activities, sexual function, and gynecological and medical histories. MAIN OUTCOME MEASURES: The main outcome measures used for the study are the following: clitoral pain characteristics (e.g., intensity, duration, quality, distress, etc.), short-form McGill pain questionnaire-2, and the female sexual function index. RESULTS: Clitoral pain is characterized by frequent and intense pain episodes that can either be provoked or unprovoked, and causes significant impairment in both daily and sexual function. The pain can be localized to the clitoris only or can occur with other genital pain. Comorbidity with other chronic pain disorders is common. A cluster analysis suggested two distinct patterns of clitoral pain, one localized and one generalized. CONCLUSION: Our findings indicate that women with clitoral pain suffer from significant, distressing, and often long-term pain, which interferes with sexual and daily activities. Two subtypes of clitoral pain may exist, each with distinct pain characteristics and subjective experiences.

The role of ovarian hormones in sexual reward states of the female rat.

To what extent does the reward value of sexual stimulation in females depend on ovarian hormones? The effects of estradiol benzoate (EB) and progesterone (P) were examined on the acquisition and expression of sexual reward induced by paced copulation and clitoral stimulation (CLS) in ovariectomized (OVX) rats. In experiment 1 we examined the expression of a pacing-induced conditioned place preference (CPP). Ovariectomized, hormone-primed rats were given experience with paced copulation associated with one side of a CPP apparatus. Changing hormonal status prior to the final CPP test did not alter pacing-induced CPP. However, subsequent partial extinction of CPP was observed only in rats primed with EB+P, a treatment previously shown to induce sexual desire and receptivity. In Experiment 2, significant CLS-induced CPP developed in ovariectomized rats regardless of hormone priming. Our results show that the expression of the sexual reward state induced by paced copulation, and CLS in particular, is independent of hormone priming. We propose that ovarian hormones sensitize sensory and motor pathways necessary for sexual behavior and stimulation to induce reward.

Who, what, where, when (and maybe even why)? How the experience of sexual reward connects sexual desire, preference, and performance.

Although sexual behavior is controlled by hormonal and neurochemical actions in the brain, sexual experience induces a degree of plasticity that allows animals to form instrumental and Pavlovian associations that predict sexual outcomes, thereby directing the strength of sexual responding. This review describes how experience with sexual reward strengthens the development of sexual behavior and induces sexually-conditioned place and partner preferences in rats. In both male and female rats, early sexual experience with partners scented with a neutral or even noxious odor induces a preference for scented partners in subsequent choice tests. Those preferences can also be induced by injections of morphine or oxytocin paired with a male rat's first exposure to scented females, indicating that pharmacological activation of opioid or oxytocin receptors can "stand in" for the sexual reward-related neurochemical processes normally activated by sexual stimulation. Conversely, conditioned place or partner preferences can be blocked by the opioid receptor antagonist naloxone. A somatosensory cue (a rodent jacket) paired with sexual reward comes to elicit sexual arousal in male rats, such that paired rats with the jacket off show dramatic copulatory deficits. We propose that endogenous opioid activation forms the basis of sexual reward, which also sensitizes hypothalamic and mesolimbic dopamine systems in the presence of cues that predict sexual reward. Those systems act to focus attention on, and activate goal-directed behavior toward, reward-related stimuli. Thus, a critical period exists during an individual's early sexual experience that creates a "love map" or Gestalt of features, movements, feelings, and interpersonal interactions associated with sexual reward.

Context alters the ability of clitoral stimulation to induce a sexually-conditioned partner preference in the rat.

We have shown previously that clitoral stimulation (CLS) of female rats induces significant conditioned place preference (CPP), indicating that it is rewarding. The present study asked whether CLS could induce a conditioned partner preference. In the first experiment, sexually naïve females received 10 alternating trials of CLS and No-CLS in the presence of a male rat behind a wire-mesh screen. For one group, CLS was made in the presence of the male scented with almond extract. On alternating trials, those females received sham CLS in the presence of an unscented male behind the screen. The order was reversed for the other group. After 5 trials in each condition, females were placed into an open field with two sexually vigorous males, one scented and the other unscented. Contrary to expectation, females displayed a preference for the male associated with sham CLS. The second experiment examined whether a partner preference could be conditioned by associating CLS with the almond odor alone. A new group of sexually naive females received the same CLS-odor, No-CLS-No Odor pairings as above, but with the odor presented on cotton gauze in the chamber. During the final open field test, those females selectively solicited the scented male. We conclude that CLS that induces CPP also induces conditioned partner preference. However, we propose that CLS in the presence of an inaccessible male created a sexual inhibitory state for female rats.

Clitoral stimulation induces conditioned place preference and Fos activation in the rat.

The present study examined the ability of clitoral stimulation (CLS) to induce conditioned place preference (CPP) and Fos protein in the brain. Ovariectomized, hormone-primed Long-Evans rats were randomly assigned to receive either distributed CLS (1 stimulation every 5 s for 1 min prior to being placed in one distinctive side of a nonbiased CPP box for 2 min, after which the cycle of stimulation and CPP exposure were repeated for 4 more cycles, totaling 60 stimulations) or continuous CLS (1 stimulation per second for 1 min with 2 min in one side of the CPP box, repeated for 4 more cycles, totaling 300 stimulations). Two days later, females were placed into the other side of the CPP box without prior stimulation. CPP was tested after 5 sequential exposures each of CLS and no stimulation. Females given distributed stimulation developed a significant CPP whereas females given continuous stimulation did not. CLS induced Fos in hypothalamic and limbic structures, including the nucleus accumbens, piriform cortex, arcuate nucleus, and dorsomedial portion of the ventromedial hypothalamus, compared to no stimulation. However, distributed CLS induced more Fos in the medial preoptic area than continuous CLS or no stimulation. In contrast, continuous CLS induced more Fos in the posteroventral medial amygdala compared to no stimulation. These data indicate that CLS induces a reward state in the rat and a pattern of Fos activation in regions of the brain that process genitosensory input, incentive salience, and reward.

The roles of accumbal dopamine D1 and D2 receptors in maternal memory in rats.

Female rats show enhanced maternal responsiveness toward their young if they have had maternal experiences before. This kind of maternal experience-based memory is critically dependent on the mesolimbic dopamine (DA) system, especially the nucleus accumbens (NA) shell. However, the relative contributions of the two main DA receptor systems (D1 and D2) within the shell have not been delineated. This study investigates the roles of dopamine D1 and D2 receptors in maternal memory by infusing a selective D1 antagonist, SCH-23390; a selective D2 antagonist, sulpiride; or a combination D-1/D-2 antagonist, cis-Z-flupenthixol, into the NA shell of postpartum female rats. Sulpiride-infused rats showed a significantly longer latency to exhibit full maternal behavior following a 10-day pup isolation period in comparison to the controls that received a vehicle. Cis-Z-flupenthixol disrupted maternal memory to a greater extent, as rats receiving this showed the longest latencies to express maternal behavior. SCH-23390 infusions had only marginal effects. These findings suggest that both the D1 and the D2 receptor subtypes play a role in the consolidation of maternal memory and they might do so by mediating the motivational salience of pup stimulation.

The whole versus the sum of some of the parts: toward resolving the apparent controversy of clitoral versus vaginal orgasms.

BACKGROUND: The nature of a woman's orgasm has been a source of scientific, political, and cultural debate for over a century. Since the Victorian era, the pendulum has swung from the vagina to the clitoris, and to some extent back again, with the current debate stuck over whether internal sensory structures exist in the vagina that could account for orgasms based largely on their stimulation, or whether stimulation of the external glans clitoris is always necessary for orgasm. METHOD: We review the history of the clitoral versus vaginal orgasm debate as it has evolved with conflicting ideas and data from psychiatry and psychoanalysis, epidemiology, evolutionary theory, feminist political theory, physiology, and finally neuroscience. RESULTS: A new synthesis is presented that acknowledges the enormous potential women have to experience orgasms from one or more sources of sensory input, including the external clitoral glans, internal region around the "G-spot" that corresponds to the internal clitoral bulbs, the cervix, as well as sensory stimulation of non-genital areas such as the nipples. CONCLUSIONS: With experience, stimulation of one or all of these triggering zones are integrated into a "whole" set of sensory inputs, movements, body positions, autonomic arousal, and partner- and contextual-related cues, that reliably induces pleasure and orgasm during masturbation and copulation. The process of integration is iterative and can change across the lifespan with new experiences of orgasm.

Do rats have orgasms?

BACKGROUND: Although humans experience orgasms with a degree of statistical regularity, they remain among the most enigmatic of sexual responses; difficult to define and even more difficult to study empirically. The question of whether animals experience orgasms is hampered by similar lack of definition and the additional necessity of making inferences from behavioral responses. METHOD: Here we define three behavioral criteria, based on dimensions of the subjective experience of human orgasms described by Mah and Binik, to infer orgasm-like responses (OLRs) in other species: 1) physiological criteria that include pelvic floor and anal muscle contractions that stimulate seminal emission and/or ejaculation in the male, or that stimulate uterine and cervical contractions in the female; 2) short-term behavioral changes that reflect immediate awareness of a pleasurable hedonic reward state during copulation; and 3) long-term behavioral changes that depend on the reward state induced by the OLR, including sexual satiety, the strengthening of patterns of sexual arousal and desire in subsequent copulations, and the generation of conditioned place and partner preferences for contextual and partner-related cues associated with the reward state. We then examine whether physiological and behavioral data from observations of male and female rats during copulation, and in sexually-conditioned place- and partner-preference paradigms, are consistent with these criteria. RESULTS: Both male and female rats display behavioral patterns consistent with OLRs. CONCLUSIONS: The ability to infer OLRs in rats offers new possibilities to study the phenomenon in neurobiological and molecular detail, and to provide both comparative and translational perspectives that would be useful for both basic and clinical research.

Tactile stimulation during artificial rearing influences adult function and morphology in a sexually dimorphic neuromuscular system.

Maternal licking of rat pups affects the development of the spinal nucleus of the bulbocavernosus (SNB), a sexually dimorphic motor nucleus that controls penile reflexes involved with copulation. Maternal licking influences SNB motoneurons, with reductions in licking producing decreased SNB number, size, and dendritic length in adulthood. Reduced maternal licking also produces deficits in adult male copulatory behavior. In this experiment, we used an artificial rearing paradigm to assess the potential role of tactile stimulation in mediating the effects of maternal licking on the SNB neuromuscular system. During artificial rearing, pups were stroked with a paintbrush to mimic maternal licking, receiving low, medium, or high levels of daily stimulation. In adulthood, ex copula penile reflex behavior was tested and the morphology of SNB motoneurons assessed. SNB motoneurons were retrogradely labeled with cholera toxin-conjugated HRP and dendritic arbor was reconstructed in three dimensions. Animals that received low levels of stimulation showed deficits in penile reflexes relative to maternally reared controls, including a longer latency to erection, fewer cup erections, and fewer erection clusters. SNB dendritic morphology was also shaped by stimulation condition, with animals that received low or medium levels of stimulation showing an average 27% reduction in dendritic length. In addition, several reflex behaviors were significantly correlated with dendritic length, including latency to first erection, percent of cup erections, and number of erection clusters. These results suggest that tactile stimulation provided by maternal licking mediates some of the effects of maternal care on the development of male copulatory behavior.