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Response of the internal reproductive organs to clitoral stimulation: The clitorouterine reflex

Abstract

We investigated hypothesis that uterine erection, elevation and enlargement during sexual response are reflex and result from penis buffeting the glans clitoris (GC). In 23 healthy women, two recording electrodes were applied to the uterine mucosa and one to cervix uteri (CU). GC was stimulated electrically and mechanically by pencil electrode. The uterine and CU pressures were measured. Tests were repeated after anesthetization of the uterus or GC. Uterine electrodes recorded slow waves, followed by random bursts of action potentials (APs). No waves registered from CU. Electrical or mechanical GC stimulation eliminated uterine electric waves, but anesthetized GC did not, nor did GC stimulation while the uterus anesthetized. Uterine pressure declined on electrical or mechanical stimulation. Results suggest presence of reproducible reflex relationship between GC and the uterus, we call ‘clitorouterine reflex’. GC buffeting seems to evoke reflex and initiate uterine responses. Reflex may prove of diagnostic significance in sexual disorders.

Introduction

The reactions of the female reproductive organs during the sexual response cycle have been studied by many investigators.1, 2, 3, 4, 5, 6 Sexual stimulation causes changes in the external and internal reproductive organs of the woman.2, 3, 7, 8 The labia majora straddle apart exposing the vaginal introitus. With continued excitation, the labia majora and minora become thickened due to venous congestion. Glans clitoris (GC) also swells and increases in both length and thickness. These changes in the external reproductive organs are suggested to be either brought about reflexly or to represent a psychogenic response.2, 9, 10, 11, 12

Likewise, the internal reproductive organs of the woman undergo changes during the sexual response cycle.2, 3, 4 These changes comprise vaginal transduction of a mucoid fluid as well as expansion and elongation of the vagina. The uterus rises in the pelvis from its anteverted and anteflexed position and the cervix moves away from the posterior vaginal wall. The uterus enlarges by as much as 50%. The cause of uterine erection and elevation is not exactly known;2 some theories have tried to explain these changes during sexual stimulation proposing that they could be due to vasocongestion in the true pelvis or to neuronally produced contraction of the smooth musculature in the ligaments that support the uterus.2

We hypothesized that the uterine changes happening during sexual stimulation are reflex in nature and occur as a result of penile buffeting of the GC. This hypothesis was investigated in the current communication.

Materials and methods

Subject

The study comprised 23 healthy female volunteers with a mean age of 36.7±6.3 standard deviation (s.d.) y (range 28–44). The women were recruited during the proliferative phase of the menstrual cycle. They were sexually active, had normal menses and no gynecologic complaint in the past or at the time of enrolment. A total of 10 were nulliparous and 13 multiparous with normal vaginal deliveries. Physical examination including gynecologic and neurologic assessment had normal findings. Sonograms showed normal genitourinary organs. Women with vaginal discharge, cervical erosions or sonographic lesions were excluded from the study. The subjects were fully informed about the nature of the study, the tests to be performed and their role in the study. The study was approved by the Review Board of the Cairo University Faculty of Medicine and its Ethics Committee.

Methods

The response of the uterus to electrical and mechanical stimulation of the GC was determined.

Electromyographic (EMG) studies

The procedure was carried out without sedation on an outpatient basis. However, some women, especially the nulliparous, were given intravenous diazepam (10 mg; Hoffman La Roche, Basle, Switzerland) for sedation during cervical dilatation. With the women in the lithotomy position, a self-retaining speculum was introduced into the vagina. Cervical dilation was performed with Hegar's dilators in the sizes from 2/5 to 3/6 mm. The uterine electric activity was recorded by means of a 4F catheter attached to the uterine wall by suction to a negative pressure of 20 cmH2O that was maintained during the test. The myoelectric activity was recorded by a monopolar silver–silver chloride electrode, 0.25 mm in diameter and situated 1 cm from the tip of the catheter (Smith Kline-Becham, Los Angeles, CA, USA). The protruding part of the electrode lay in contact with the endometrium, thus acting as a surface electrode.

Three electrodes were applied to the uterus: two to the uterine and one to the cervix uteri (CU) mucosa. The two uterine electrodes were introduced through the CU to be attached by suction to the mucosa of the uterine wall, one electrode above the other and 2 cm apart. The third electrode was applied to the cervical mucosa at about the middle of the cervical canal. The reference electrode was a metal disk applied to the skin of the abdomen. The signals detected by the electrodes were amplified using an AC amplifier with a frequency response within ±3 dB from 0.016 Hz to 1 kHz and were displayed on a recorder at a sensitivity of 1 mV/cm. A strain gauge respiration transducer was attached to the thoracic wall to exclude respiratory artifacts.

GC stimulation

GC was stimulated both electrically and mechanically. Electric stimulation was performed with a surface electrode (Vickers Medical, Medelec, Woking, UK) applied to the GC and fixed by electrode gel. Mechanical stimulation was carried out with a pencil electrode consisting of a solid steel rod, 15 cm long and 5 mm in diameter. To avoid injury to the GC, the distal end of the electrode was covered for about 2 cm by a polyvinyl sponge which was fashioned like a cone to simulate the shape of the glans penis. The response of uterus and CU to gentle stroking of the GC by the pencil electrode was recorded. The GC stroking by the pencil electrode intended to simulate GC buffeting by the erect penis during coitus. It was performed by one investigator in all of the examined women. In all, 20 gentle GC strokes were made for each subject. The test was repeated at least twice in the individual subject.

Manometric studies

The uterine and CU pressures were measured by a manometric tube of a 0.5 mm inner and a 1 mm outer diameter, with two side ports, perfused with normal saline at a rate of 1.6 ml/min by a pneumohydraulic perfusion system (Arndorfer, Medical Specialities, Greendale, WI, USA), A vaginal speculum was inserted into the vagina to expose the CU. One lubricated tube was introduced 4–5 cm into the uterine cavity and another one into the CU. They were connected to a strain gauge pressure transducer (Statham 230B, Oxnard, CA, USA). We started recording the uterine electric activity and pressure 30 min after the electrodes and the manometric tubes had been applied to the uterus and CU. During this half-hour the uterus would have adapted to these devices. At least two recording sessions of 60 min each were performed for every woman.

Clitoral and uterine anesthetization

To study whether the uterine response to clitoral stimulation was a direct or a reflex action, GC stimulation was performed after individual anesthetization of the uterus and GC. GC was anesthetized by means of xylocaine gel (Astra, Södertälje, Sweden). At 20 min following gel application, the response of the uterus to GC electrical and mechanical stimulation was recorded. After 3 h later when the anesthetic response had disappeared, the uterine response to GC stimulation was registered. The test was repeated using bland gel instead of xylocaine gel. On another day, the uterus was anesthetized by instilling 10 ml of 2% xylocaine, added to 10 ml of normal saline, into the uterine cavity through the CU. The uterine response to GC stimulation after 20 min and after 3 h was recorded. The test was repeated using normal saline instead of xylocaine.

The results were analyzed statistically using the Student's t-test. Values were given as the mean±s.d. Differences assumed significance at P<0.05.

Results

All the women finished the tests without complications during or after the test performance and were evaluated.

The suction electrodes were atraumatic to the uterine or cervical wall. They were easy to apply, were stable and not dislodged as long as the already mentioned suction pressure was maintained. Dislodgment of an electrode would have been recognizable from loosening of the catheter.

Electromyographic recording

Slow waves (SWs) were recorded from the two electrodes applied to the uterus. They were monophasic and negatively deflected (Figure 1). The waves had a regular rhythm and exhibited the same frequency, amplitude and velocity of conduction from the two electrodes of the individual women. The mean frequency was 3.2±0.9 cycle/min, (cpm, range 2–5), the amplitude 0.5±0.1 mV (range 0.3–0.8), and the conduction velocity 4.1±1.6 cm/s (range 3.2–5.6, Figure 1). The SWs variables were constant in the two electrodes when the test was repeated in the same woman.

Figure 1
figure1

Electrohysterogram at rest showing the electric activity recorded by the two electrodes applied to the uterus (U) in the form of slow waves followed or superimposed by the action potentials (arrow). No waves were recorded from the cervix uteri. C=cervical EMG.

The SWs were followed, or superimposed, by bursts of fast activity spikes or action potentials (APs), represented by negative deflections (Figure 1). They did not accompany each SW and their number varied from one test to the other.

While the uterus exhibited resting electric waves, the CU did not. No waves were registered from the CU during the two recording sessions (Figure 1). Electrical stimulation of the GC was induced by a train of five square pulses of 1 ms duration and 1 ms apart, with the threshold varying from 35 to 75 mA (mean 50.7±10.9). At threshold, no electric waves were recorded from the three electrodes applied to the uterus and CU (Figure 2). However, in some women, we recorded occasional SWs from the uterus which were not associated with APs (Figure 3). The uterus responded to GC stimulation as long as the stimulation was maintained. Upon cessation of electrical GC stimulation, the uterine SWs reappeared with variables similar to those before electrical GC stimulation. The latency which is the period from the stimulus to the start of the response recorded a mean of 19.4±2.1 ms (range 17–23).

Figure 2
figure2

Electrohysterogram showing disappearance of the uterine electric waves (U) on electrical stimulation of the glans clitoris. ↑=stimulation; C=cervical waves.

Figure 3
figure3

Electrohysterogram showing appearance of occasional uterine slow waves (U) on electrical stimulation of the glans clitoris. ↑=stimulation; C=cervical waves.

Mechanical stimulation of the GC with pencil electrode caused disappearance of the uterine resting electric waves (Figure 4). The response was momentary; it occurred synchronously with the stroking of the GC by the pencil electrode and then the electric waves reappeared. Repeated buffeting of the GC with the pencil electrode was coupled with dis- and reappearance of the electric waves. The latency recorded a mean of 20.6±2.2 ms (range 18–25). No electric waves were recorded from the CU on mechanical GC buffeting.

Figure 4
figure4

Electrohysterogram showing disappearance of the uterine electric waves (U) on mechanical stimulation of the glans clitoris. ↑=stimulation; C=cervical waves.

We did not find a significant difference in the resting electric activity of the uterus or in the response to GP stimulation between nulli- and multiparous women and between the young and elderly women.

Response of the uterus to clitoral anesthetization

Electrical and mechanical stimulation of the GC 20 min after its anesthetization effected no disappearance of the uterine electric waves (Figure 5), whereas the waves disappeared with stimulation following bland gel application to the GC. Furthermore, the anesthetized uterus did not respond to GC stimulation, while it did when normal saline was instilled into it. The response of the uterus to GC stimulation returned when 3 h after anesthetic application its effect had disappeared.

Figure 5
figure5

Electrohysterogram 20 min after GC anesthetization. GC electric stimulation did not cause disappearance of the uterine electric waves (U). ↑=stimulation; C=cervical waves.

Pressure measurements

The uterine and CU resting pressure recorded a mean of 11.6±2.1 cmH2O (range 9–14). Electrical stimulation of the GC using the aforementioned variables led to a significant reduction of the uterine pressure to a mean of 2.7±0.7 cmH2O (range 1.6–3.4; P<0.05). The pressure reduction was maintained on continued GC stimulation. Mechanical GC stimulation also effected a significant uterine pressure reduction to a mean of 3.2±0.8 cmH2O (range 2–4.2; P<0.05). The pressure reduction was intermittent and coupled with GC buffeting with the pencil electrode. It did not differ significantly from that induced by electrical stimulation. During the aforementioned pressure measurements we did not find significant changes in the CU pressure (P>0.05).

The current results were reproducible with no significant difference when we repeated the tests in the individual subject.

Discussion

The external and internal reproductive organs undergo changes during the sexual act.1, 2, 3, 4, 5, 6, 7, 8 These changes reflect the functional adaptability of the reproductive organs to serve the sexual performance and notably the process of reproductivity. The current study may shed some light on the mechanism of the uterocervical changes that occur during the sexual act.

Upon GC stimulation, the uterus seems to adapt to the reproductive process. The rise of the uterus in the pelvis from its anteverted and anteflexed position with a subsequent movement of the CU away from the posterior vaginal wall as reported by investigators2, 3, 4 is a mechanism which is suggested to serve a twofold function: (a) it enables proper CU buffeting by the glans penis and (b) it brings the os of the CU in apposition with the glans penis to allow for direct passage of the deposited semen through the cervical os to the uterine cavity. In a previous study, we have demonstrated that, during sexual intercourse, the levator ani muscle undergoes reflex contractions mediated through the vaginolevator reflex.13 Levator muscle contraction pulls up the vaginal wall at the vaginal fornices (Figure 6) leading to their ballooning and formation of a receptacle for semen collection during the sexual act.13, 14 It may also lead to elevation of the CU and consequently of the uterus.

Figure 6
figure6

Diagram illustrating the effect of levator ani and puborectalis muscles contraction on the vagina and uterus. Antero-posterior view. (a) At rest (b) Upon levator contraction, the muscle becomes elevated and laterally retracted, with a resulting elevation of the uterus as well as dilatation of the upper vagina and vaginal fornices. Puborectalis muscle contraction compresses the lower vagina (from Shafik14).

The current study as well as previous15 studies have shown that the uterus exhibits electric waves which are presumably responsible for the motor activity of the organ.16, 17, 18, 19, 20, 21 Thus it seems that the uterine electric activity is responsible for inducing the uterine resting tone which is assumed to assist in keeping the uterus in its resting position and shape. The source of these electric waves is controversial. They could be discharged from the uterine smooth muscle fibers or the interstitial cells of Cajal (ICC).22, 23, 24, 25 The ICC exist in the gut,23, 24, 25 yet we do not know if they also exist in the uterus. As previously demonstrated,15 the CU did not exhibit electric waves; this may be related to the fact that the CU contains but a few smooth muscle fibers. Presumably, the motor activity of the electric waves is produced by the APs.16, 17, 18, 19, 20, 21 Earlier studies have revealed that the APs were coupled with a rise of the intrauterine pressure, while the SWs were not.15 As the APs followed or were superimposed on the SWs, we postulated that probably the SWs pace the APs in terms of direction and amplitude.20

On GC stimulation, electrical or mechanical, the uterine electric waves disappeared. Disappearance of the APs seems to be associated with absence of uterine motor activity. The uterine resting tone apparently disappears on GC stimulation. We propose that disappearance of the uterine tone during GC stimulation is accountable for uterine enlargement as well as for the rise of the uterus in the pelvis from its anteverted and anteflexed position. Furthermore, the disappearance of the uterine motor tone which results in uterine wall relaxation, uterine cavity dilatation, and uterine pressure reduction, appears to create a condition of relatively negative uterine pressure and suction action that sucks the semen collected in the vaginal fornices into the uterine cavity.

The clitorouterine reflex

The current findings postulate a hitherto unrecognized relationship between GC stimulation and the uterine electric activity. The disappearance of the uterine electric waves on GC stimulation hypothesized the possible involvement of a reflex which we term ‘clitorouterine reflex’. The constancy of this reflex relationship is evidenced by reproducibility and by its absence on individual anesthetization of the assumed two arms of the reflex arc, namely the GC and the uterus. Anesthetization with xylocaine (lidocaine) blocks C and Aα- fibers which are responsible for pain and reflex activity.26

We suggest that the clitorouterine reflex is evoked during penile buffeting of the GC in the sexual act. The resulting disappearance of the uterine electric activity and the possible consequent uterine muscle relaxation and uterine dilatation appear to explain the changes in the uterus and CU during coitus. These changes, assumed to be preparatory for receiving the semen deposited in the vaginal fornices, comprise uterine enlargement as well as the rising of the uterus in the pelvis from its anteverted and anteflexed position with a resulting movement of the CU away from the posterior vaginal wall.2, 3

The afferent limb of reflex arc seemingly comprises the sensory nerve endings in the GC which are stimulated by penile buffeting of the GC. Afferent impulses appear to be transmitted to the sacral segment by the pudendal nerve (S2, 3, 4), while the efferent limb probably passes via the autonomic supply to the uterus.

Recordings of the electric waves of the uterus are limited by artifacts. It may be argued that these waves represent artifacts. However, the consistency and reproducibility of the waves are against this argument. The uterine electric waves could be easily differentiated from the electrocardiographic waves by the characteristic shape of the latter waves. The possibility of respiratory artifacts was excluded by recording the respiratory electric activity via a transducer attached to the chest wall (Figure 7).

Figure 7
figure7

Respiratory artifacts recorded from a transducer attached to the chest wall.

Diagnostic role of the clitorouterine reflex

The investigative tools for the diagnosis of female sexual disorders are few.27 Episodic vaginal blood flow during sleep is measured in an attempt to assess the neurophysiological substrate of the sexual desire in women.28, 29 The diagnostic significance of vaginal responses to erotic stimuli in the waking state is not yet clear.30

The clitorouterine reflex may be considered as an investigative tool in the diagnosis of female sexual disorders. Changes in the reflex latency or the wave variables or the response to clitoral stimulation may indicate a defect in the reflex pathway. However, further investigations need to be performed to confirm the current results.

In conclusion, the findings of our study suggest the presence of a reproducible reflex relationship between the GC and the uterus which we call the ‘clitorouterine reflex’. During the sexual act and penile buffeting of the GC, the clitorouterine reflex seems to be evoked and initiates the uterine response that comprises erection, elevation and enlargement of the uterus. Owing to paucity of the currently available investigative tools for the diagnosis of sexual disorders, the clitorouterine reflex may be incorporated, after further studies, as an investigative tool in the diagnosis of such disorders.

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Acknowledgements

Margot Yehia assisted in preparing the manuscript.

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Shafik, A., El-Sibai, O., Mostafa, R. et al. Response of the internal reproductive organs to clitoral stimulation: The clitorouterine reflex. Int J Impot Res 17, 121–126 (2005). https://doi.org/10.1038/sj.ijir.3901278

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Keywords

  • cervix uteri
  • uterus
  • clitoris
  • slow waves
  • action potentials
  • sexual disorders

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