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Try out PMC Labs and tell us what you think. Learn More. 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.

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. Both male and female rats display behavioral patterns consistent with OLRs. 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.

Orgasms are among the most wonderous and pleasurable events we experience as human beings. Kinsey, Pomeroy, and Martin and Kinsey, Pomeroy, Martin, and Gebhard noted that orgasms come largely from penile stimulation in men and clitoral stimulation CLS in women, although stimulation of other erogenous zones on the body could also sum up to, or in some cases generate, orgasms. Despite a plethora of poetry and songs devoted to orgasms and their repercussions, the phenomenology of orgasm in humans is fraught with a multitude of definitions and interpretations, different subjective experiences across individuals, and even different experiences in the same individual across the lifespan.

That said, people's experiences with orgasms, especially first experiences, can be profound and life-changing. Stimulation of the glans and shaft of the erect penis also give rise to pelvic floor muscle contractions as orgasm nears. The glans penis and external clitoris are homologous structures, and tactile stimulation activates similar sensory nerves e. The pudendal nerve is a mixed sensory and motor nerve that serves the entire sacral plexus. In addition to the clitoris and penis, the pudendal nerve receives sensory inputs from labia, scrotum, and anus.

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Its motor division controls contractions of the external urethral and anal sphincters along with the rest of the pelvic floor muscles. The pelvic nerve controls contractions of the internal urethral and anal sphincters and is responsible for erection of the clitoris and penis. Stimulation of the hypogastric nerve activates the sympathetic outflow responsible for orgasm. In turn, the pelvic nerve carries sensory information from the cervix and pelvic floor muscle contractions during orgasm.

These nerves thus subserve the genitosensory input to the spinal cord and brain that are processed ultimately as genital swelling, sexual stimulation, and orgasm Fig. In male rats, a set of spinothalamic neurons in the lower lumbar spinal cord LSt neurons has been identified that act as an ejaculation generator, coordinating inhibitory and excitatory outflow from brainstem and hypothalamic nuclei notably nucleus paragigantocellularis, paraventricular PVN nucleus, and medial preoptic area mPOA to control sympathetic, parasympathetic, and motor actions Coolen et al.

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It is not known to what extent these neurons play a role in orgasm relative to the control of ejaculation, as ejaculation can occur without corresponding orgasm in men McKenna, b. Nerves pudendal, pelvic, hypogastric, and vagus that subserve sexual arousal and orgasm in women and men. B: bladder.

C: cervix. CB: corpora spongiosum of the bulbocavernosus. E: epididymis. NTS: nucleus of the solitary tract brainstem. P: prostate. SV: seminal vesicle. T: testis. U: uterus. V: vagina. Adapted from Georgiadis, et al. Schematic diagram of the spinal and supraspinal regulation of tumescence T and detumescence D of the clitoris and penis. Dashed lines are excitatory and solid lines inhibitory for genital blood flow.

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After De Groat and Steers LSt neurons that comprise the ejaculation generator in males are located in the lower lumbar cord see Coolen et al. Using positron emission tomography to analyze regional cerebral blood flow, Huynh, Willemsen, Holstege et al. Multiple neurotransmitter systems, including endogenous opioids, serotonin, and endocannabinoids, are involved in the subjective feelings of pleasure, satiety, and sedation common to orgasms and their aftermath Pfaus, Accordingly, administration of the opioid receptor antagonist naloxone to men blunts the pleasure of orgasm and eliminates the oxytocin release associated with it Murphy et al.

In addition to the opioid contribution, orgasm depends critically on sympathetic activation, and there appear to be individually defined optimality curves for orgasm across increasing levels of arousal. Furthermore, drugs or situations that reduce sympathetic tone can delay or abolish orgasm, whereas drugs or situations that increase sympathetic tone can either increase the magnitude or of orgasms, although such increases must be specific to, or associated with, sexual interaction Pfaus et al.

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Accordingly, these models are used widely in sexual and reproductive medicine Chianese et al. Mechanisms of erection, ejaculation, and the post-ejaculatory refractory period have been studied in detail in rodents and other species e. This begs a question: Can we assume that a male rat or rhesus macaque experiences the pleasure of ejaculation as we experience an orgasm? During this time, some female macaques also open their mouths and tense their facial muscles in what Slob et al.

Do female macaques or females of other species experience OLRs in response to sufficient copulatory stimulation? And if so, how could we know? One advantage of studying orgasms in humans is that people can provide a subjective verbal assessment of their feelings that can be contrasted with physiological correlates. However, this comes with a caution: at best, humans do not have a common way to scale orgasm quality or intensity despite available validated rating scales, like that of Mah and Binikwhich researchers doing objective assessments have not utilized ; at worst, they lie. Moreover, it is virtually impossible to study human orgasms in any kind of natural environment without necessarily altering the context.

And of course, we cannot study first experiences of orgasm except as Kinsey and colleagues did in the subjective retrospective of their participants.

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Obviously, we do not know what it feels like to be another animal Nagel, In fact, our empathy and intuition take us only so far in inferring the feelings of other people. For example, to someone who is sexually active but has never experienced an orgasm, the tales of those that have multiple orgasms must seem outlandish if not also depressing. However, consistent with Dennettif an orgasm could be distilled into observable and testable components, it would be easier to make quantitative determinations of differences in expression that might reflect lawful differences in qualitative experience.

What might those components be? A hint is given from the work of Mah and Binik In developing their adjective-based rating scale, Mah and Binik examined factor loadings and structure among a large set of words used by women and men to describe their subjective experience of orgasm from masturbation and copulation.

These terms were then rated by several hundred university-age women and men, and then organized by principal components analysis into 12 factors. The sensory dimension consisted of terms that described sensations of building, flooding, flushing, shooting, throbbing, and muscle spasms.

The cognitive—affective dimension described ecstasy, pleasurable and satisfying sensations, relaxation, and emotional intimacy. If we distill these components further into what might be observed in humans or other animals, we can derive at least three phenomena that could characterize an OLR:. Short-term behavioral changes that reflect immediate awareness of a pleasurable hedonic reward state. Long-term behavioral changes that depend on the reward state induced by the OLR. These include an identifiable state of 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.

To understand the potential expression of OLRs in a rat model, it is necessary to consider the form and patterning of rat copulatory behavior. Sexually receptive females actively solicit sexual interaction with males by making a headwise orientation to the male followed by an abrupt runaway. This often entices the male to chase them, after which the female holds a pre-lordosis crouch. Males mount with flank palpation, further increasing the lordosis posture of the female, allowing vaginal penetration as the male intromits with brief pelvic thrusts that typically last less than a second.

If vaginal penetration has occurred, the male dismounts abruptly and grooms his erect penis into detumescence. The female typically runs away a short distance, and either hops and darts around the male or makes another full solicitation. Hopping and darting typically entices the male to mount again and is used as a proximal solicitation, especially if the male is not chasing or if the female does not have enough room in a testing environment to make a full solicitation with a longer runaway.

Finally, stimulation of the cervix in an inhibitory state. This fighting behavior enforces longer and longer intervals between intromissions.

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Similarly, in large open fields with attached burrow systems, females typically take themselves out of the copulations after a smaller of ejaculations compared with small chambers McClintock, Ejaculation by males in a post-ejaculatory refractory period, after which males copulating with the female toward another ejaculation. In response to female solicitations, male rats mount, intromit, and ejaculate, and males have relatively stable individual patterns of these behaviors Pattij et al.

However, these disruptions of copulatory behavior do not occur if male rats have sufficient sexual experience Pfaus et al. Males are also aware of their sexual state during copulation. Immediately after ejaculation, males emit a long 22 kHz vocalization which corresponds to their period of behavioral quiescence Burgdorf et al. Sensory stimulation of female red and male blue rats during sexual interaction. OFS: olfactory stimulation. FLS: flank tactile stimulation. VCS: vaginocervical stimulation. CLS: clitoral stimulation. PNS: penile stimulation. Pacing is facilitated for females in large open fields, bilevel chambers where she can run from level to levelor in unilevel chambers bisected by a Plexiglas partition with holes at the bottom that allow the female — but not the male — to cross from side to side.

Females show regular patterns of pacing in these three testing environments. These observations bolstered the notion that females enforce an optimal timing between intromissions that le to optimal timing for the induction of a progestational state Adler, If females are tested in small chambers that do not allow efficient pacing, they are more likely to display defensive responses such as rearing or boxing to enforce intervals between mounts, intromissions, and ejaculations. During copulation, females receive olfactory stimulation from male odors and pheromones, somatosensory stimulation from the flanks FLS where males palpate, CLS from pelvic thrusts, and VCS from penile intromissions, which in the seminal plug after ejaculation Fig.

In contrast, chronic anesthesia of the external gland of the clitoris alone had the opposite effect in which females had a greater of exits from and entrances to the male compartment but spent less time with the male Parada et al. Together, these data suggest that genitosensory stimulation of the penis or clitoris induce a pleasurable state that males and females are aware of in terms of appetitive calls, and which they attempt to compensate for behaviorally if the stimulation is reduced by pharmacological agents or lesions to specific nerves. Copulation in both male and female rats also induces a reward state that can be associated by Pavlovian processes with contextual- or partner-related cues to form long-term conditioned place preferences CPPs or conditioned partner preferences.

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CPP is often demonstrated in an apparatus with two distinctive compartments that are connected to either side of a third neutral compartment. During training, the compartments are paired sequentially with different unconditional stimuli, e. In the final test, the animal is placed into the neutral compartment between the two distinctive compartments, with the two doors on either side opened to allow free access to either compartment. CPP is said to have developed if the rat spends ificantly more time in the reward-paired compartment than the other compartment. We have mimicked the CLS females receive from males by applying it to the clitoris directly with a 4 camelhair paintbrush Parada et al.

CLS applied in intervals to mimic its distribution during paced copulation induces a strong CPP relative to continuous CLS or a control condition in which the female's tail is raised but no CLS is applied. CLS induces immediate 50 kHz vocalizations that follow individual trill-flat patterns Fig. These patterns are emitted in response to distributed but not continuous stimulation and are maximal in females that are fully sexually motivated and receptive. Thus, like male 50 kHz vocalizations, females appear to be aware of timed CLS and respond to it in a way consistent with the induction of a reward state.

Ultrasonic vocalizations made by female rats in response to distributed CLS. Left side depicts raw calls. Middle depicts the proportion of total calling during CLS taken by flats, trills, flat-trills, step-ups, and compound calls. Right side depicts median calls in females that receive full hormone priming with estradiol benzoate and progesterone versus no hormone oil vehicle. In another group of studies, we have shown that placement of a neutral odor, such as almond or lemon, on a vigorous and receptive sex partner can be paired with the reward state induced by first experiences of ejaculation in males or paced copulation in females.

Typically, these preferences are formed by paired copulation in bilevel or unilevel pacing chambers and then tested in a large open field with two potential sex partners, one scented and the other unscented. Unpaired controls who received repeated pairing with an unscented partner show a slightly weaker conditioned preference for the unscented partner on the final open-field test, and random-paired controls do not show any conditioning.

Strain cues from pigmented versus non-pigmented partners also induce ificant partner preferences in both females Coria-Avila et al. Interestingly, a female rat given her first paced copulatory experience with one particular male displays conditioned mate-guarding behavior in the presence of that male and a competitor female Holley et al.

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