Unified definition of human orgasm is difficult: in spite of the intuitive individual recognition of the phenomenon, the research on orgasm has not converged on a broadly accepted definition. Rather, the definitions range from those focusing on the subjective sensation to the release of neural tension, or the bodily changes involved, such as muscular contractions (Mah and Binik 2001). This multitude of descriptions reveals the multifaceted, individually variable and thus highly subjective experience of human orgasm. For the purposes of this short description, we will delineate the orgasm here as a neuroendocrine event, alluding to the two main physiological signaling systems involved, i.e., the nervous and the hormonal, serving as the starting point. We will first focus on external description of male and female arousal and orgasm and its neurological and hormonal underpinnings, followed by its possible roles in the evolution. Finally we will briefly address some of the historical interpretations.

Physiology of Human Orgasm

In both males and females, orgasm is preceded by the arousal stage, characterized by a rush of blood into genitalia and triggered either by cognitive or tactile stimulation. In males, the rush of blood into penile corpus cavernosum, enabled by the relaxation of smooth muscles lining the blood vessel walls (see below), leads to penile erection. What is commonly addressed as ejaculation consists of two parts – the emission, during which the seminal fluid is collected in the prostatic part of the urethra, and the ejaculation from the penis. We equal here ejaculation with male orgasm, even though the field is not in complete agreement on this topic (Alexander et al. 1993).The fact that pathological disorders can affect each of these processes separately suggests that their regulation is at least to some extent distinct. Arousal, emission, and ejaculation are a complex coordinated interplay of several smooth muscles of the ducts connecting testes with urethra (epididymis and vas deferens), of the seminal vesicle, prostate, and several sphincters, which likely contribute to the pressure with which semen exits at ejaculation. Ejaculation also includes the involuntary action of striated pelvic muscle, anal sphincter, and perineal muscles. The trigger of ejaculation is likely not simply a matter of the degree of arousal; however, the actual mechanism is not understood so far. In females, the arousal and orgasm has traditionally been described in four stages: excitement, plateau, orgasm, and resolution (Masters et al. 1966). Plateau is the stage in which, similar to male arousal, blood flow into the genitalia is increased, leading to vaginal lubrication and vaginal dilation, as well as clitoral swelling. Clitoris is the female anatomical counterpart of penis and consists of external visible parts (glans and labia) and an appreciable internal portion (paired bulbs and crura with erectile corpora cavernosa; O’Connell et al. 2005; Puppo and Puppo 2015). Female orgasm similarly manifests itself as involuntary rhythmic muscle contractions of pelvis, uterus, and vagina as well as lower anus. As in males, also in females, it is not understood what underlies the transition from arousal to orgasm.

Some of the neurobiological mechanisms coordinating the above phenomena are known (reviewed in Komisaruk et al. 2006). Cranial and spinal nerves integrating parts of autonomous (involuntary) and somatic nervous systems innervate genitalia. Most generally, it is thought that both parts of autonomous neural system are involved in control of sexual activity: the parasympathetic slow-acting system in arousal and the sympathetic quick-acting system in orgasm. The parasympathetic innervation of genitalia stems from cranial vagus (Komisaruk et al. 2004) and the sacral pelvic neural fibers, the later associated with pudendal spinal nerve (but see recent suggestion that the pelvic fibers may in fact be part of the sympathetic system; Espinosa-Medina et al. 2016). The established sympathetic innervation stems from the hypogastric plexus of lower abdomen, associated with lower lumbar spinal nerves. Neuroimaging studies of the brain during stimulation have shown activation of several brain regions. The somatosensory innervation of genitalia in both sexes maps to parts of medial cortex (Komisaruk et al. 2011), whereas the human orgasm itself has been shown to activate numerous additional brain regions. Mapping female and male orgasm (ejaculation) showed activity in the hypothalamic nuclei, cerebellum, preoptic area, bed nucleus of stria terminalis, amygdala, hippocampus, lower brainstem, and frontal cortex (Whipple and Komisaruk 2006; Georgiadis et al. 2007; Komisaruk and Whipple 2008; Komisaruk et al. 2011; Huynh et al. 2013). Thus at least to a great extent, male and female orgasm-associated brain circuits overlap. Interestingly, many of the same circuits have been also associated with male ejaculation in rodents indicating parts of homologous process across animal species (Baum and Everitt 1992) although there are also differences when compared to primates (Michael et al. 1999).

What we know about the neurotransmitters involved in signaling during arousal and orgasm is derived mainly from targeting of specific neurotransmitters to treat nervous conditions in other disease contexts, such as depression. Several drug classes have been shown to affect arousal and/or orgasm in humans. These include drugs that act directly on transmitter receptors, such as agonists of serotonin receptors or antagonists of inhibitory noradrenalin receptors, both of which enhance aspects of sexual behavior. Further, the use of drugs that inhibit degradation of transmitter in the synapse, or inhibit its reuptake (e.g., SSRI), has indicated that serotonin and dopamine modifications significantly modulate sexual reaction and orgasm (Montejo-Gonzalez et al. 1997; Balon 2006; Higgins et al. 2010).

In addition to neural circuits in other brain regions, orgasmic activation of the hypothalamus also triggers a hormonal response of the pituitary. The pituitary is an endocrine gland, which functionally connects two signaling systems, the neural and the hormonal system. Its function is triggered by the neural signal to the brain, conveyed to pituitary either by direct neural connections (posterior pituitary) or by the signals secreted from the neurons to the hypothalamic vessel plexus, and transferred into pituitary by the blood (anterior pituitary). Orgasm triggers a surge of pituitary hormone secretion in humans, which is particularly pronounced in females (Exton et al. 1999, 2001). The strongest hormonal surge is that of prolactin; however, also a minor surge of oxytocin has been reported (Carmichael et al. 1987). The physiological significance of these surges is unknown. Because the long-term elevation of prolactin inhibits libido, the prolactin surge has been suggested to inhibit the promiscuous behavior in females (Kruger et al. 2002) after coitus. However, the fact that women (in contrast to men) lack refractory period after orgasm suggests that this explanation of the brief prolactin surge is unlikely (Bianchi-Demicheli and Ortigue 2007). An alternative suggestion is that the PRL peak is a remnant of evolutionarily older process that induces ovulation and therefore has had a reproductive function in the evolutionary past (see below). Indeed, prolactin peak is associated with normal ovulation in women (Vekemans et al. 1977; Braund et al. 1984). This will be discussed further in the section on evolution of orgasm. Mechanistically, the prolactin peak is likely a consequence of brief interruption of dopamine signaling in the hypothalamus, where dopamine constitutively inhibits prolactin secretion; thus, dopamine inhibition (e.g., due to transient increase in serotonin signaling) can account for the prolactin surge (Bianchi-Demicheli and Ortigue 2007). The existence of orgasm-associated surge of the second pituitary hormone, oxytocin, has been variably reported (Kruger et al. 2003) and is likely rather due to projections of the separate neuronal signals from genitals and breast to the same brain region in hypothalamus (Cross and Wakerley 1977). The reproductive functional significance of oxytocin is likely found in causing the contraction of the myoepithelial cells in breast milk glands as well as in the reproductive tract, involved in milk ejection in the breast, and propagation of the egg cell (and, in labor, the fetus) through the reproductive tract. The social function that is often attributed to oxytocin is that of enhancing partner bonding, in analogy to what is observed in rodents (Carter 1992; Witt et al. 1992; Cho et al. 1999; Razzoli et al. 2003). However, the putative orgasm-associated surge reported for humans is not only variably detected, but very small (~1.3-fold change in female orgasm; Carmichael et al. 1987) compared to the experimental dosages in rodents (up to tenfold change in experimental settings showing effect on social behavior in rats; Witt et al. 1992). Given that oxytocin is suggested to reinforce future trust and sexual behavior also in humans, it is not clear whether orgasm (sex) contributes to this effect or whether it rather stems from other aspects of intimacy or relationship.

Types of Female Orgasm

Whereas males perceive orgasm relatively uniformly, women report different types of orgasm associated with stimulation of different parts of genitalia (“vaginal,” “cervical,” vs. “clitoral” orgasm, Grafenberg spot). The innervation of genitalia mentioned above includes separate branches supplying parts of genitalia, and these all likely respond to stimulation. There is, in addition to spinal nerves, evidence for innervation independent of the spinal cord, which has been suggested to account for cervical orgasm (Sansone et al. 2002; Komisaruk and Sansone 2003; Komisaruk et al. 2004). Moreover, it is important to realize that the clitoris is an organ much larger than glans clitoris that is externally visible and extends internally dorsolateral, parallel to the urethra and also to the ventral vaginal wall (O’Connell et al. 2005; Puppo and Puppo 2015). It is thus likely that vaginal penetration can achieve indirect stimulation of internal clitoral parts, leading to perception of the ventral vaginal side as “G-spot,” so-called after German physician Graefenberg (1950), who studied the role of urethra in female orgasm.

Evolutionary Origin of Orgasm

To identify the evolutionary origin of any trait requires recognizing the corresponding trait in different species and then identifying the last common ancestor of the lineages in which the trait is present. Finding a corresponding trait of human orgasm is difficult, in part because research on orgasm has been primarily conducted in humans and primates, and therefore orgasm has been very narrowly characterized to capture human-specific characteristics, difficult to detect in other animals (Pfaus et al. 2016). For this reason, little is known about the presence, or the role, of corresponding traits across mammals. It is very unlikely that the physiological basis of orgasm has arisen only in human or primate lineage. However, it is likely that the trait has acquired human-specific modifications in human lineage.

It is useful here to focus separately on male and female orgasm for a moment. The orgasm in males is associated with ejaculation and sperm transfer and therefore crucial for reproduction. Prompt ejaculation of relatively large amount of sperm thus is generally assumed to be a sufficient explanation for the existence of orgasm-like impulse in species with internal fertilization. Indeed, erection and ejaculation are widely spread across animal kingdom, in particular in amniotes, that is, the reptiles and mammals.

In contrast to male orgasm, the human female orgasm is not required for reproduction, and in fact a high percentage of women do not experience orgasm during reproductive (penetrative) sex (Hite 1976; Lloyd 2005). To nevertheless explain its existence, various reproductive roles were suggested, by which the presence of female orgasm would still positively affect the number of offspring; ranging from mate choice (Alcock 1980; Puts et al. 2012), to bonding, to enhancement of sperm transfer (Levin 2011a), to name a few. So far no evidence could be found for such effects of orgasm on reproductive fitness (Levin 2011b; Zietsch and Santtila 2013). However, whether the female orgasm presently has a (reproductive) function or not reveals little definitive about why it originated, as the function of a trait often changes during the trait’s evolution. An important critical review of existing theories of origination and maintenance, specifically of female orgasm, was published in 2005 by Elizabeth Lloyd (2005). Lloyd pointed out the difference between sexes in how closely reproductive sex is related to orgasm: whereas reproductive sex is effective in achieving orgasm in men, it is highly ineffective in women. This makes the explanations based on direct reproductive effect implausible. Lloyd systematically evaluated 21 theories based on the evidence their authors provided and rejected all but the by-product hypothesis (Symons 1979). This hypothesis states that the female orgasm is a side effect of male orgasm, meaning that it originated and is maintained (in spite of having no function), because the male counterpart is required for reproduction. To understand why female trait would be so dependent on male trait, it is useful to remember that the female clitoris is homologous to the male penis and therefore shares the very similar genetic basis. As this basis is passed sometimes to male and other times to female progeny, it becomes partially modified in the developmental context of particular sex to build either clitoris or penis. Whereas the adult morphology in males and females is different, not all the features of male and female physiology can be genetically decoupled, and physiology of orgasm could be one such feature. The necessity of orgasm in males is thus suggested to drive the origin and maintenance of the female orgasm.

In 2016, Pavlicev and Wagner proposed a new hypothesis for female orgasm (Pavlicev and Wagner 2016). The authors provided evidence that female orgasm may be a remnant of the neuroendocrine signal, which induces ovulation in some species. Ovarian cycles are spontaneous in women, meaning ovulation does not depend on environmental signals or the pheromones or copulatory stimulation by a male, releasing a single egg cell periodically every ~28 days (ovulation). However, in many mammals, ovulation is not spontaneous but rather dependent on an external trigger, which is often tactile genital stimulation during copulation. These species are called induced ovulators and include many carnivores (cats, ferrets, etc.), camels, rabbits, etc. Pavlicev and Wagner suggested that the orgasmic neuroendocrine signal that triggers pituitary hormones in human female orgasm still carries a signature of the signal that triggers ovulation (via pituitary) in induced ovulators. Moreover, induced ovulation is phylogenetically older and thus may have been a predecessor of spontaneous ovulation. Many traits lose functions during evolution, but traces still stay around. Additional evidence is seen in female genital morphology: coincident with evolution of spontaneous ovulation, also the position of strongly orgasm-triggering glans clitoris has changed. In species, which require induction by copulation, the clitoris is positioned within copulatory canal where it gets directly stimulated, whereas in the species that ovulate spontaneously, the clitoris is removed from the copulatory canal. The latter at the same time may explain the rarity of female orgasm during reproductive (i.e., penetrative) sex.

Historical Cornerstones of Research on Human Orgasm

The irregularity of female orgasm in particular has intrigued thinkers since the ancient times. Aristotle already has reflected on the question whether or not female orgasm is important for reproduction (reported in Leroi 2014). Early on, the female sexuality, including the lack of orgasm, has been strongly associated with psychological state, and the sexual massages were used as treatment for hysteria, hysteria standing for a very general description of female mental and behavioral disorders (psychosexual connotation is still reflected in hysterectomy for uterine removal). Particularly influential in this context up to the present day were the writings of Sigmund Freud, the Viennese founder of psychoanalysis. Freud in his work on mental disorders laid great emphasis on the experiences during early development, as well as specifically on sexuality. With respect to female orgasm, he proposed a natural developmental succession from infantile clitoral to mature vaginal orgasm (Freud 1905). The grave consequence of this influential conceptualization was that the absence of vaginal orgasm during reproductive sex has become interpreted as a signature of mental immaturity, of women stuck in a childlike sexual state- quite overlooking that this is rather the norm than a deviation. One of the early remarkable woman sexologists was Marie Bonaparte (Bonaparte 1933). Herself a psychoanalyst, she opposed Freud’s concept, proposing that glans clitoris remains the main source of mature female orgasm and that the lack of orgasm during reproductive sex is due to the lack of clitoral stimulation during penetrative sex, deriving from displacement of clitoris from the vagina, typical of human anatomy. In 1930s she collected over 200 individual measurements of the distance between vagina and clitoris and found a correlation between that distance and a decreased rate of copulatory orgasm (a dataset more recently re-evaluated by Wallen and Lloyd 2011). Best known empirical research on human sexuality and orgasm from the twentieth century is undoubtedly that by the zoologist Alfred Kinsey from Indiana University (Kinsey et al. 1948, 1953), followed by the rich work of William Masters and Virginia Johnson, at Washington University in St. Louis (Masters and Johnson 1960; Masters et al. 1966, 1974, 1993; Kolodny et al. 1979). An important contribution in particular in female sexuality came from Shere Hite. In a comprehensive review of female sexual experience, she first documented the high percentage of women that rarely or never experience orgasm in penetrative sex – thus considered dysfunctional in Freud’s theory – however are perfectly able to do so in masturbation (Hite 1976). From the 1970s to 1990s, evolutionary theories of female orgasm were discussed by a wide variety of authors from the ethologist Desmond Morris (1967) to the behavioral biologist John Alcock (1980), to the paleontologist Steven J. Gould (1991). With the exception of the work of Symons, Gould, and Lloyd, all attempts to explain the evolution of orgasm, discussed above, have been adaptationist, meaning that they attempt to explain the origin of female orgasm by its assumed current utility in humans (Wagner and Pavlicev 2016). This debate was synthesized in the influential book by Elisabeth Lloyd (2005). Finally, major contributions to the current knowledge of the physiology of female orgasm were made starting in the 1990s by Barry Komisaruk and collaborators.

Cross-References