Psychoneuroendocrinology,Vol.15,No.3, pp. 207-216,1990

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THE ENDOCRINE EFFECTS OF VISUAL EROTIC STIMULI IN NORMAL MEN C. CARANI, I J. BANCROFT,2 G. DEL RIO,1 A . R . M . GRANATA,1 F. FACCHINETTI3 and P. MARRAMA1 1Depar~ent of Endocrinology and Physiology and 2MRC Reproductive Biology Unit, Edinburgh, Scotland; 3Department of Gynaecology, University of Modena, Modena, Italy (Received 12 March 1990; l.nfinal form 5 June 1990)

SUMMARY Endocrine responses to erotic stimulation in the laboratory were assessed in eight normal subjects. Each subject was tested on two occasions. On one occasion only neutral stimuli were involved. After 15 rain baseline, 30 rain of films were shown. For the erotic condition on the other occasion, two 10min erotic films were interspersed with 10 min of neutral film. Fifteen-minute blood samples were taken from the start of each test and continued for 5 hr after the films. Plasma was assayed for testosterone, LH, prolactin, cortisol, ACTH and ~-endorphin. Urine was collected for 4 hr before and 4 hr after the films; this was assayed for adrenaline, noradrenaline and dopamine. Sexual arousal occurred in response to the erotic films in all subjects, as shown by erectile and subjective responses. There were no significant changes in hormone or catecholamine levels following either the erotic or the neutral stimuli, except for a rise in cortisol during the neutral but not the erotic film. These results indicate that in the laboratory, substantial sexual response can occur without accompanying endocrine or biochemical changes.

INTRODUCTION

THE ROLE o f androgens in maintaining normal sexuality in men is now well established. Lack of androgen results in loss o f sexual desire and an impaired capacity for spontaneous erections, such as occur during sleep. These effects are dose-related (Bancroft, 1989). By contrast, erectile response to visual erotic stimuli appears to be relatively independent o f androgens. Although a weak association between erectile response to erotic stimuli and plasma testosterone has been reported in normal men (Rubin et al., 1979; Lange et al., 1980), studies o f hypogonadal men have shown erectile response to visual erotic stimuli to be apparently unaffected by androgen replacement, whereas spontaneous erections during sleep are clearly enhanced (Bancroft & Wu, 1983; Kwan et al., 1983; O'Carroll et al., 1985). What is less clear is whether sexual response or activity has any effect on a man's endocrine status. Studies o f endocrine changes after both sexual activity and exposure to erotic stimuli in the laboratory have produced inconsistent results. Fox et al. (1972) reported a rise in testosterone (T) in one man both before and following orgasm. In this study, sexual activity involved the panner and m a y have been associated with some anticipatory arousal. Purvis et al. (1976) found a rise in T, dihydrotestosterone (DHT) and androstenedione following masturbation (to produce a semen Correspondence to be addressed to: Dr. Cesare Carani, Institute of Endocrinology, University of Modena, School of Medicine, Via Campi 287, 1-41100 Modena, ITALY. 207

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sample), but there was no rise in LH to account for this response and no evidence of a rise in T during the anticipatory phase. This m a y have reflected the lack of erotic quality in masturbating in a hospital room to produce a semen sample. Steams et al. (1973) and Lee et al. (1974) failed to record any hormonal changes after either sexual intercourse or masturbation. Studies o f hormonal response to erotic stimuli in the laboratory also have been inconsistent. Lincoln (1974) found no effects, Pirke et al. (1974) found a somewhat delayed rise in plasma T, and LaFerla et al. (1978) reported a rapid, though transient, rise in LH. H e l l h a m m e r et al. (1985) found a transient increase in salivary T 15 min after the onset of erotic films. In a different type of study, Levi (1969) s h o w e d erotic films to groups o f young m e n and w o m e n , collecting urine before and after the films. He found an increase in urinary excretion of both adrenaline and nora d r e n a l i n e in his m a l e subjects. In none o f these studies was any direct m e a s u r e of genital response involved, and assessment of sexual arousal depended on self-report. Rowland et al. (1987) measured erectile response to erotic films as well as T, LH, cortisol and prolactin. T h e y used a complex design, involving two groups of eight men. One group saw an erotic film early in the testing session and a second erotic film later in the session, and the other group saw a neutral film early in the session and an erotic film later. The purpose of this design was to assess whether any hormonal response to the first film would influence the response to the second film. It was not clear what the subjects in this study were led to expect; for this and other reasons, including weaknesses in study design, interpretation o f their results is difficult. Rowland et al. (1987) did, however, find some increase in LH after the first erotic film in the first group. In the study reported here we have aimed to assess the effect o f visual erotic stimuli on genital and subjective sexual response, and on n e u r o e n d o c r i n e and s y m p a t h o - a d r e n a l parameters, in healthy young adult men. METHODS Subjects

Eight men, ages 20 to 26 years, participated in the study after being shown to be in good health, drug-free, without any sexual dysfunction or other sexual problem, and with exclusive heterosexual orientation. Procedures

A cross-over design was used, involving two tests on consecutive days. On one day, erotic films were shown; on the other day only neutral films. The order of presentation was balanced, with four subjects seeing the erotic film on the first day, and four on the second. As the anticipation of seeing an erotic film might have influenced the baseline hormonal state, the following information was given to each subject: There were three groups of subjects; the first group would see an erotic film on both days, the second group would see an erotic film on only one of the two days, and the third group would not see an erotic film at all. In this way, each subject's expectations were such that he would not know whether to expect an erotic or a neutral film on each occasion. Each test started at 1145h with urine and blood sampling continuing for a further 5 hr, 45 rain. At the beginning of each test an intravenous eannula was insea'ted to be used for repeated blood sampling, and the subject was seated comfortably alone in a room, with a video screen in front of him. The experimenter, who was male, was situated in an adjoining room, except for blood sampling and obtaining self-ratings of sexual arousal after each stimulus presentation. After 15 rain of sitting quietly, three 10-rain video-recordings were shown to the subject. During the "erotic" condition, the first and third recordings were erotic, showing explicit heterosexual activity. The second recording involved a neutral, non-erotic subject. During the "non-erotic" condition, all three films were of neutral content. Measurements

Penile erecti0n This was measured by means of a Rigiscan. This commercially available device (Dacomed) provides independent measures of penile circumference and rigidity, sampled at 15-see intervals, The device consists of two rings, one applied around the base and one around the distal part of the penile shaft. Circumference is measured in mm. Rigidity is assessed by measuring the extent to which the ring can be reduced in diameter when a pulling force is

ENDOCRINERESPONSESTOEROTICSTIMULI

209

applied to it. An incompressible penile shaft would allow no reduction and this would represent a rigidity of 100%. Rigidity is expressed in percentage terms. The Rigiscan was fitted at the beginning of the session and remained in place throughout the testing session. Erectile parameters used in the analysis were: maximum circumference increase during each 10-min stimulus, Mean circumference increase (i.e. the average of the 15-see samples), maximum rigidity recorded (as a percentage), mean rigidity (i.e. average of 15-sec samples). Sobiective sexual arousal At the end of each 10-min stimulus the subject was given a visual analogue rating scale (100 mm line) with the following instruction: "After each stimulus I will ask you to give me a score from 0 to 100 to indicate how sexually excited you felt during the film; not how much erection you experienced, but how excited you felt inside yourself. 0 would mean 'not excited at all', 100 'very strongly excited for me'." Urine collection All subjects emptied their bladders at 0800h on each test day and collected all urine passed for the next 4 hr, i.e. until just before the first stimulus presentation. They re-emptied their bladders at the beginning of the testing session, and urine was collected for the next 4 hr. This resulted in two 4-hr urine samples per test, one pre-stimulus, the other post-stimulus. The urine was immediately acidified with 6NHC1 and stored at -4" C until assayed. Concentrations of noradrenaline (NA), adrenaline (A) and dopamine (DA) were measured in the 4-hr specimens by reverse-phase, highpressure liquid chromatography with electrochemical detection (Del Rio et al., 1989). Results are reported as nmol per 4 hr. The inwaassay coefficients of variation of NA, A and DA were 5%, 5% and 3% respectively. All four samples for each subject were analysed in the same assay. Blood samtflin~, Sixteen milliliters of blood was collected at 15-rain intervals throughout each test. Plasma was separated and stored at -20" C until assayed for the following hormones; testosterone, LH, prolactin, cortisol, ACTH and 13endorphin. All samples from one individual were measured in the same assay. Plasma testosterone was measured by radioimmunoassay (RIA) after ether extraction. All samples were measured in duplicate. Tritiated steroids were obtained from New England Nuclear (Boston, MA); standards were purchased from Vister (Milan). Antisera were obtained from Radim (Rome). The inter- and intra-assay coefficients of variation were 10.7% and 5.9%, respectively. Plasma LH was measured by a double antibody RIA with a kit obtained from Pacific Biotech (San Diego, CA). Samples were measured in duplicate and at two different dilutions. The inter- and intra-assay coefficients of variation were 8% and 6%, respectively. Plasma prolactin was measured by two-site fluoroimmunometric assay based on the directed sandwich technique (DELFIA) with a kit from LKB (Wallac, Turku, Finland). The inter- and intra-assay coefficients of variation were 5% and 2.5%, respectively. Plasma cortisol and ACTH were measured with kits commercially available from Techno Genetics (S. Mauro Torinese, Italy). For cortisol the inter- and intra-assay coefficients of variation were 10% and 6.8%, and for ACTH, 9.5% and 6%, respectively. Plasma 13-endorphin (13-EP) was measured by RIA (Facchinetti et al., 1987). The inter- and intra-assay coefficients of variation were 9.9% and 6.1%, respectively. Statistical analysis Comparison of hormone levels at different times of the test and during the two test occasions were carried out using repeated measures analysis of variance and Duncan's multiple comparison analysis technique (Winer, 1971) RESULTS Genital response Erectile r e s p o n s e to the erotic videos, in terms o f c i r c u m f e r e n c e change and rigidity, is shown in Table I as m e a n values for the eight subjects. Erectile ~esponse to the n e u t r a l videos during the " n o n - e r o t i c c o n d i t i o n " were n e g l i g i b l e , a n d the results are n o t s h o w n . S u b s t a n t i a l erections in terms of c i r c u m f e r e n c e a n d rigidity were s h o w n b y all eight subjects while w a t c h i n g the erotic recordings. T h e responses to the first 10-rain erotic s t i m u l u s were significantly greater, in both respects, t h a n the response to the second 1 0 - m i n erotic stimulus.

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Subjective arousal Mean subjective ratings for the two 10-min erotic recordings and the intervening neutral recording are also shown in Table I. The ratings for the two erotic stimuli were not significantly different.

Catecholamine responses Urinary excretion of adrenaline, noradrenaline and dopamine in the 4 hr preceding the films and the 4 hr during and following them is given in Table II, Comparison of the erotic and neutral conditions at both baseline and after stimulation, and comparison of pre-post change scores in the two conditions, showed no significant effects. Exposure to erotic films in this study was not associated with any alteration in catecholamine excretion in the urine.

TABLE I. ERECTILE RESPONSE AND S U ~ C T I V E AROUSAL TO EROTIC FILMS Erotic Film Scores Erotic I

Penile circumference change (mm) Maximum

Neutral

37.6 (2.8) 32.2 (2.2)

Mean Penile Rigidity (%) Maximum

67.5 (8.8) Mean 58.2 (8.2) Subjective Arousal 76.5 (100 mm line) (11.1) Numbers in parentheses are standard deviations

TABLE II. URINARY CATECHOLAMINEE X C ~ N

Erotic 2

Erotic I vs. 2

9.5 (3.2) -

31.6 (3.5) 25.0 (4.4)

p = 0.02

13.1 (5.8)

55.4 (9.7) 42.9 (9.7) 68.5 (16.7)

p = 0.04

3.5 (1.4)

p = 0.01

p = 0.02 N.S.

RESPONSE TO NELrI'RALAND EROTIC FILMS

Neutral Film Pre-film Post-film

Erotic Film Pre-film Post-tilm

0800-1200h

1200-I600h

0800-1200h

1200 -1600h

Adrenaline (nmol/4 hr)

18.8 (18.2)

21.5 (15.0)

24.4 (20.4)

18.9 (21.9)

Noradrenaline (nmol/4 hr)

61.1 (35.2)

61.1 (34.3)

58.1 (31.0)

62.2 (27.4)

419.8 ~ (212.3)

473.0 (190.3)

539.5 (331.0)

499.5 (164.2)

Dopamine (nmol/4 hr)

Numbers 'in parentheses are standard deviations

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211

Hormonal response Mean testosterone and LH levels at 15-min intervals throughout the experiment are shown for the erotic and neutral film conditions in Figs. 1 and 2. There were no significant differences between any two time points in either condition, and there was a non-significant trend for testosterone to be higher in the erotic condition (F-- 3.03; df= 1,362; p = 0.083). Thus, in this experiment no effects of exposure to an erotic film on testosterone or LH were observed either during the film or for a period of 5 hr after it. For the other endocrine parameters in this study, it was decided to reduce the number of samples assayed. All samples for only two subjects were assayed for prolactin, cortisol ACTH and 13-endorphin. For the other subjects, a reduced number of timepoints (i.e. 15-min intervals) were chosen to represent the trends of the complete curves. For prolactin, these were 1 to 6, 8 and 12. For the other hormones they were 1 to 3, 5, 10 and 14. The means and standard errors for these hormones and time points are shown in Figs. 3-6. For ACTH, cortisol and 13-endorphin there was a rise in levels during the film presentation, but this occurred in response to both erotic and neutral films and was somewhat greater with the latter. The only within-session change to reach significance was for cortisol during the neutral condition: levels at timepoints 3 and 5 were each significantly higher than at point 14. The difference between erotic and neutral conditions approached significance for cortisol (p =0.071) With prolactin, none of the within-session change reached significance at the .05 level, but overall, prolactin was significantly higher during the neutral condition than the erotic condition (F = 4.98; df= 1,39; p = 0.031). Correlations between erectile response and plasma testosterone Correlations between penile circumference change and rigidity and testosterone levels are shown in Table m-I, separately for the erectile response to each of the two 10-min erotic films during the erotic condition. There is a strikingdifference between the first arid second films, with correlations with testosterone being negative for the first and positive for the second, and correlations being more substantial in both directions when the overall mean testosterone level is used. Correlations between testosterone and subjective ratings did not show this pattern and were all nonsignificant.

TABLE Ill. ACROSS-SUBJECTS CORRELATIONSBETWEEN PLASMATESTOSTERONE {T) AND ERECTILE RESPONSE

Baseline T

Circumference "AMaximum A Mean First Second First Second Film Film Film Film

Rigidity Maximum Mean First Second First Second Film Film Film Film

0.04

Overall -0.46 Mean T *p< 0.05; tp< 0.10.

0.30

0.08

0.39

0.05

0.11

0.05

0.06

0.73*

-0.37

0.67 t

-0.48

0.22

-0.48

0.48

212

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LH

12

9

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Hours I~G. 1 (top pane~: P l a s m a testosterone levels at 15-mln Intervals before, during, a n d for 5 h r after p r e s e n t a t i o n of a n erotic a n d a n e u t r a l film in eight n o r m a l m e n . FIG. 2 (bottom pane]): P l a s m a LH levels at l S , m l n intervals before, d u r i n g , a n d for 5 h r after p r e s e n t a t l o n of a n erotic a n d a n e u t r a l film in eight n o r m a l m e n .

E ~ D O C ~ RESPONSESTOEROnC STIMULI

213

Cortisol

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80-

ACTH

60" 40-

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Hours FIG. 3 (top panel): Pla.~na corttsol levels before, during, a n d at selected t l m e p o i n t s after p r e s e n t a t i o n of a n erotic a n d a n e u t r a l film in eight n o r m a l m e n . T h e post-film t l m e p o l n t s were selected, on the b a s t s of a s s a y of all 15-min s a m p l e s in two subjects, to r e p r e s e n t t h e t r e n d s for t h e complete curves. FIG. 4 ( b o t t o m p a n e l ) : P l a s m a ACTH levels b e f o r e , d u r i n g , a n d a t s e l e c t e d t i m e p o i n t s a f t e r p r e s e n t a t i o n of a n eroUc film in eight n o r m a l m e n . The post-film time p o i n t s were selected, on the b a s t s of a s s a y of all 15-mln s a m p l e s in two subjects, to r e p r e s e n t t h e t r e n d s for t h e complete curves.

214

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Prolactin

12

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Hours I~o. 5 (top panel): Plasma prolacthn levels belong, during, and at selected ttmepomts ~ ¢ r presentat/on of a n erotic and a neutral fl]m m e ~ t ~ men. The po~,fllm ~ p o i n t s were selected, on the basis of assay of all 15-mln samples m two subjects, to represent the trends for the ~ e : c u r v e s : FIG, 6 (bottom panel): P!a,~ma ~-endorphm ~ e l s before, during, and at selected t ~ e P O / n t s after presentat/on of a n erotic f l l m / n ~ t ~ merL The p o s t ~ tJme points were s ~ t m : l , on the basis at" assay of all 15-m/n ~ in two subjects, to represent the trends for the complete curves:

Er,~OCRISERESOONS~TOEROTICSTmIYL1

215

DISCUSSION The eight subjects in this study all showed evidence of a substantial sexual response to the erotic films in terms of both penile erection and self-ratings of sexual excitement. They did not, however, show any evidence of increased urinary catecholamine excretion in association with this sexual response. This contrasts with the data of Levi (1969), who found significant increases in both urinary adrenaline and noradrenaline. His subjects viewed the explicitly sexual films in a large, mixed-sex group, and this may have influenced their response. Also, Levi's study was carried out more than 20 years ago, when viewing explicit sexual films may have been more arousing to young medical students because of its relative novelty. Nowadays, such experience is more commonplace. It nevertheless seems unlikely from these results that increased urinary catecholamine excretion is a normal component of sexual arousal, and may reflect some other aspect of arousal such as anxiety or embarrassment. We also found little evidence of a neuroendocrine response to sexual stimulation in these men. Although there was a trend towards higher testosterone levels during the erotic condition, there was no clear evidence of a rise in testosterone, or in any other of the hormones measured, following the erotic films. ACTH, cortisol and I~-endorphin all showed a non-significant rise during exposure to the films, but this applied to both neutral and erotic films, and each of these rises was in fact larger during the neutral films. Cortisol was the only hormone to show a significant change during the session, with a rise during the film and a subsequent fall, but this only applied to the neutral condition, and was in part due to a dramatic rise in cortisol at the beginning of the film in one subject. Prolactin was significantly higher during the neutral condition. This raises the interesting possibility that, perhaps by an erotically induced increase in central dopamine, prolactin might be lowered by erotic stimuli. Against this, however, is the fact that prolactin levels were higher during the baseline period of the neutral condition, as well as during the remainder of the session. Also, in the study of Rowland et al. (1987), although different subjects were involved in the two conditions, those subjects viewing the erotic film had higher prolactin levels than those in the neutral condition. It thus seems likely that the observed differences in prolactin are attributable to chance. Previous studies have found a weak association between plasma testosterone levels and erectile response to erotic stimuli in normal men (Rubin et al., 1979; Lange et al., 1980). Rowland et al. (1987) also found some support for such an association. The relevant findings in our study were striking and possibly of considerable interest, though in view of the small number of subjects, they will require replication. It would appear that plasma testosterone, whether assessed during the baseline period, averaged over the whole session, or taken as the maximum reached during the session, did not predict the erectile response to the first 10 rain of erotic film, but did so for the second erotic film, the response to which was significantly less. Is it possible that the initial response reflects the novelty of the stimulus, and as such is independent of testosterone, whereas the second response reflects a more fundamental erectile responsiveness which is androgen dependent and more akin to the spontaneous erections during sleep? In general we have failed to find any evidence of a clear neuroendocrine response accompanying a marked genital and subjective response to erotic stimuli in normal young men tested in laboratory conditions.

Acknowledgements: We are grateful to Dr. A. Scuteri for his help in this study.

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C. CARANIet al. REFERENCES

Bancroft J (1989) Human Sexuality and lts Problems, 2nd Ed. Churchill Livingstone, Edinburgh. Bancroft J, Wu FCW (1983) Changes in erectile responsiveness during androgen therapy. Arch Sex Behav 12: 5966. Del Rio G, Baldini A, Carani C, Della Casa L (1989) Adrenomedullary hyperactivity in type I diabetics before and during continuous subcutaneous insulin treatment. J Clin Endocrinol Metab 68: 555-559. Facchinetti E, Martignoni E, Petraglia F, Sances MG, Nappi G, Genazzani AR (1987) Premenstrual fall of plasma ~-endorphin in patients with premenstrual syndrome. Fertil Steri147: 570-574. Fox CA, Ismail AAA, Love DN, Kirkham KE, Loraine JA (1972) Studies on the relationship between plasma testosterone levels and human sexual activity. J Endocrino152: 51-58. Hellhammer DH, Hubert W, Schiirmeyer T (1985) Changes in saliva testosterone after psychological stimulation in men. Psychoneuroendocrinology 10:77-81. Kwan M, Greenleaf WJ, Mann J, Crapo L, Davidson JM (1983) The nature of androgen action on male sexuality: a combined laboratory and self report study in hypogonadal men. J Clin Endocrinol Metabo157: 557-562. LaFerla J, Anderson D, Schalch D (1978) Psychoendocrine response to sexual arousal in human males. Psychosom Med 40: 166-172. Lange DJ, Brown WA, Wincze JP, Zwick W (1980) Serum testosterone concentration and penile tumescence changes in men. Horm Behav 14: 267-270. Lee R, Jaffe R, Midgley A (1974) Lack of alteration of serum gonadotrophins in men and women following sexual intercourse. Am J Obstet Gynecol 120: 985-987. Levi L (1969) Sympatho-adrenomedullary activity, diuresis and emotional reactions during visual sexual stimulation in human males and females. Psychosom Med 31: 251-268. Lincoln G (1974) Luteinising hormone and testosterone in man. Nature 252: 232-233. O'Carroll R, Shapiro C, Bancroft J (1985) Androgens, behaviour and nocturnal erections in hypogonadal men: the effect of varying the replacement dose. Clin Endocrino123: 527-538. Pirke K, Kockott G, Dittmar F (1974) Psychosexual stimulation and plasma testosterone in man. Arch Sex Behav 3: 577-584. Purvis K, Landgren B, Cekan Z, Diczfalusy E (1976) Endocrine effects of masturbation in men. J Endocrino170: 439-444. Rowland DL, Heiman JR, Gladue BA, Hatch JP, Doering CH, Weiler SJ (1987) Endocrine, psychological and genital response to sexual arousal in men. Psychoneuroendocrinology 12: 149-158. Rubin H, Henson D, Falvo R, High R (1979) The relationship between men's endogenous levels of testosterone and their penile responses to erotic stimuli. Behav Res Ther 17: 305-312. Stearns E, Winter J, Falman C (1973) Effect of coitus on gonadotrophin, prolactin and sex steroid levels in man. J Clin Endocrinol Metab 37:687-691. Winer BJ (1971) Statistical Principles in Experimental Design, 2nd Ed. McGraw Hill, New York.

The endocrine effects of visual erotic stimuli in normal men.

Endocrine responses to erotic stimulation in the laboratory were assessed in eight normal subjects. Each subject was tested on two occasions. On one o...
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