This study compared reflexogenic and psychogenic penile responses in men with and without ... studies suggesting that performance-related distractors (i.e.,.
Journal of Consulting and Clinical Psychology 1994, Vol. 62, No. 6, 1222-1228
Copyright 1994 by the American Psychological Association, Inc. 0022-006X/94/J3.00
Visual Stimulation Facilitates Penile Responses to Vibration in Men With and Without Erectile Disorder Erick Janssen, Walter Everaerd, Rik H. W. van Lunsen, and Stefan Oerlemans This study compared reflexogenic and psychogenic penile responses in men with and without erectile disorder. It was hypothesized that men with psychogenic erectile dysfunction respond minimally to vibrotactile stimulation. An enhancement of penile responses was expected when vibration was combined with erotic film. Patients were 50 men with psychogenic erectile dysfunction, 45 men with organic erectile dysfunction, and 50 sexually functional men. The combination of film and vibration resulted in stronger penile responses than the stimuli presented separately. Men with psychogenic erectile dysfunction and sexually functional men did not differ in responses to film and film-andvibration conditions. As predicted, responses of the 2 groups were different in the vibration condition. Interpretations are provided in terms of attention and appraisal. The findings are relevant to the development of psychophysiological diagnostic procedures.
Human penile erection can be elicited by local sensory stimulation of the penis (reflexogenic erection) and by central stimuli received by or generated within the brain (psychogenic erection). This distinction points to two different mechanisms of penile erection: one that is controlled by reflex centers in the spinal cord, and one by cortical centers in the brain (Krane, Goldstein, & de Tejada, 1990). The evidence for the two distinct mechanisms stems mainly from experimental spinal transections in animals (e.g., Sachs & Bitran, 1990) and observations in men with spinal cord injury (e.g., Brindley, 1984; Chapelle, Durand, & Lacert, 1980; Comarr, 1970; Higgins, 1979; Tarabulcy, 1972). To date, no studies have been reported on the two mechanisms of penile erection in neurologically intact men. It is assumed that in neurologically intact men, reflexogenic and psychogenic erectile mechanisms act synergistically in the control of penile erections (de Groat & Steers, 1988; Krane et al., 1990; Weiss, 1972). Although not directly assessed through experimental research, some findings on sexually functional men have been reported that are compatible with this assumption (Rowland & Slob, 1992). Undoubtedly, the stimuli associated with reflexogenic and psychogenic erectile mechanisms (e.g., tactile stimulation and fantasies or visual stimuli) concur in many sexual situations. However, the exact nature of the interactive mechanisms involved in the initiation, and possible (reciprocal) facilitation or inhibition of the two erection systems, is still unclear.
Erick Janssen and Walter Everaerd, Department of Clinical Psychology, Universiteit van Amsterdam; Rik H. W. van Lunsen, Department of Sexology, Academic Medical Center, Universiteit van Amsterdam; Stefan Oerlemans, Department of Urology, Academic Medical Center, Universiteit van Amsterdam. Preparation of this article was supported by Grant 3209 from the Nationaal Fonds voor de Geestelijke Volksgezondheid. Correspondence concerning this article should be addressed to Erick Janssen, Department of Clinical Psychology, Universiteit van Amsterdam, Roetersstraat 15, 1018 WB Amsterdam, The Netherlands.
One way to explore the interaction between reflexogenic and psychogenic erectile mechanisms is to compare penile response patterns of sexually functional men with those found in men with erectile dysfunction. It may be inferred from the findings on spinal cord injured men that in neurologically intact men, erectile responses to tactile stimulation evolve relatively independent of central nervous system processes (cf. Masters & Johnson, 1966; Money, 1980). However, it has been suggested that in neurologically intact men, reflexogenic erections will be inhibited when psychogenic stimuli such as guilt, hostility (Weiss, 1972), or nonsexual thoughts (Brindley, 1991) are present. Although these assumptions have never been tested systematically, they are consistent with the findings of experimental studies suggesting that performance-related distractors (i.e., sexual worries) inhibit responses to sexual stimuli in sexually dysfunctional men (Barlow, 1986; Everaerd, 1993). In this study, we examined reflexogenic and psychogenic erectile response patterns in men with psychogenic erectile dysfunction, men with organic erectile dysfunction, and sexually functional men, all without spinal cord injury. Penile responses to vibrotactile stimulation of the penis, erotic film presentation, and to a combination of these two stimuli were measured and compared across the three subject groups. The reported data were gathered in a validation study on Waking Erectile Assessment (WEA). This study was designed to compare the use of vibrotactile and visual stimuli in the diagnosis of male erectile dysfunction. A detailed description of the full test procedure and the results of clinical decision analyses are reported elsewhere (Janssen, Everaerd, van Lunsen, & Oerlemans, 1994). We hypothesized that, in comparison to sexually functional men, patients with psychogenic erectile dysfunction will show minimal response to vibration (comparable to patients with organic erectile dysfunction). Second, we expected to find an enhancement of penile responses to vibration when it was combined with erotic film in all groups. We expected to find the most profound enhancement in patients with psychogenic erectile dysfunction. In these subjects, the additional presentation of an erotic film, providing explicit sexual cues, may facilitate
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the appraisal of vibration as sexual and enhance responses by decreasing the attentional capacity for competing sexual worries or nonsexual distracting thoughts (Barlow, 1986; Everaerd, 1993). Method
Subjects One hundred consecutive patients with erectile dysfunction (mean age 53 years, range = 19-78) and 50 sexually functional volunteers (mean age 41 years, range = 19-69) participated in this study. All patients were diagnosed according to DSM-IH-R (Diagnostic and Statistical Manual of Mental Disorders, 3rd edition, revised; American Psychiatric Association, 1987) criteria as having Male Erectile Disorder. The patients, either physician- or self-referred, were first seen in the Sexual Dysfunction Clinic or Urology Department of the Academic Medical Center. Recruitment of sexually functional volunteers was accomplished through announcements in local newspapers. Volunteers were prescreened with an interview and a questionnaire. Information was obtained about sexual problems, general physical functioning, medical history, demographic variables, and psychiatric status. The volunteers were paid $ 15.00 for their participation. Both patients and volunteers submitted written informed consent before participation. Patients were assigned to diagnostic groups on the basis of independent clinical criteria. Although a large number of examination procedures are available for the diagnosis of erectile dysfunction, most of them lack standardization and normative values and show poor reliability (Buvat, Buvat-Herbaut, Lemaire, Marcolin, & Quittelier, 1990; Everaerd, 1993; Mohr & Beutler, 1990). Therefore, any single procedure can be of value only when used in conjunction with other assessments. In accord with the main purpose of this study (i.e., to compare responses of psychogenic patients with responses of sexually functional men), independent examinations were conducted to ensure a conservative criterion for diagnosing patients as having psychogenic erectile disorder. Thus, only those patients who showed a clear presence of psychogenic factors and in whom no indication whatsoever for organic involvement was found were included in the psychogenic patient group. Whenever the examinations led to the suspicion of organic involvement, patients were assigned to the organic patient group. To classify patients, we conducted the following five examination procedures. The clinicians conducting the examinations were not provided with the results of the psychophysiological examination during their diagnostic workup. Structured medical and sexual history interview. The structured interview was conducted by the sexologist (Rik H. W. van Lunsen). The first part of the sexual history interview focused on symptom clarification. A specific description of the primary complaint was followed by questions concerning (a) possible problems in other phases of the sexual response cycle; (b) sexual problems of the partner; (c) the duration, development, course, and degree of the erectile problem; and (d) reactions of the patient and his partner to the sexual problem. The second part of the sexual history interview covered demographic information, psychosexual history, sexual satisfaction, interpersonal factors, and the patient's perception of possible causes and treatment options. The interview was designed to provide the information necessary to determine if relevant psychological factors are present to account for the erectile dysfunction. For example, a patient's report of rigid spontaneous, early morning, or noncoital erections and a patient's own perception of a psychological cause have been found to be strong predictors of psychogenic etiology (e.g., Buvat et al., 1990; Speckens, Hengeveld, Lycklama a Nijeholt, van Hemert, & Hawton, 1993). The medical history interview included questions about general physical functioning, medical history, the use of medications, smoking habits, alcohol consumption, drug abuse, and psychiatric status.
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General physical examination. Also conducted by the sexologist, this procedure included examination of the genitals, secondary sexual characteristics, weight, blood pressure, pulse, and peripheral circulation. Biochemical examination. Laboratory tests included the determination of serum levels of testosterone, follicle-stimulating and luteinizing hormones, prolactin, and glucose. Vascular examination. Conducted by the urologist (Stefan Oerlemans), this examination included the evaluation of penile blood circulation by injections of smooth muscle relaxants (papaverine/phentolamine) in the corpus cavernosum of the penis, and the measurement of penile arterial pressure with calculation of the penile-brachial index (PBI). Following these two examinations, the urologist reviewed the data and decided whether cavernosometry and cavernosography (no rigidity on intracavernous injections of 30 mg papaverine/phentolamine [291 1 ]; n = 20), and duplex Doppler measurements or angiography, or both (no signs of venous leakage on cavernosometry and cavernosography; n = 5) should be performed. Neurophysiological examination. Sensory nerve functioning was evaluated by measuring the pudendal evoked potential (PEP). This examination also included bulbocavernosus and anal reflex testing. For each patient, consensus was reached by the urologist and sexologist on the degree and nature of physiological and psychological involvement. At this stage, they were unaware of the results of the psychophysiological investigation. To structure the process of establishing a diagnosis, a form was designed containing factors indicating psychological and physiological involvement. Overall agreement between the urologist and sexologist wasaccomplished for 93 of the 100 patients. For the remaining 7 patients, some initial disagreement existed on the relative importance of organic and psychogenic factors. For these patients, consensus was established after a more elaborate discussion of the results of the five examination procedures. Of the 100 patients, 50 were diagnosed as having pure psychogenic erectile dysfunction (mean age = 50 years, range = 19-70). In 45 other patients, an organic factor was found (mean age = 58 years, range = 35-78). The remaining five patients had erectile dysfunction of uncertain origin (mean age = 55 years, range = 32-66). The results of these 5 patients are not reported here.
Stimuli The film stimuli consisted of two 3-min erotic videotapes with sound. The stimuli were presented in a fixed order on a color TV monitor. Both a heterosexual version (selected by 137 subjects) and a homosexual version (8 subjects) of the videotape were available. The film stimuli were comparable in intensity, both depicting combinations of petting and foreplay. One film presentation was paired with vibrotactile stimulation of the penis. This vibration-and-film (VF) condition followed a 2-min period of vibrotactile stimulation without film (V). Vibrotactile stimulation was administered by means of a commercially available ring-shaped vibrator with a frequency of approximately 50 Hz. After receiving careful instructions, subjects placed the vibrator just below the coronal ridge. Because an interaction was expected between vibration and film, the presentation of vibrotactile stimulation was counterbalanced across subjects to control for possible order effects. Thus, two order-groups were created: One was first exposed to the vibration conditions V and VF (film 1) followed by the film condition F (film 2); the other group was first exposed to the film condition F (film 1) followed by the vibration conditions V and VF (film 2).
Measures A mechanical penile strain gauge (Barlow, Becker, Leitenberg, & Agras, 1970) was used to assess penile circumference changes. A continuous direct-current signal recorded changes in electrical output
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JANSSEN, EVERAERD, VAN LUNSEN, AND OERLEMANS
caused by expansion of the strain gauge. Before each session, calibration was accomplished by using a 26-step plastic cone with steps ranging from 85 to 160 mm circumference. The strain gauge was positioned two thirds of the way down the shaft of the penis toward the base. The experimenter checked patients for proper placement of this device. Both the strain gauge and the vibrator were sterilized in a solution of Cidexactivated Glutaraldehyde before use (Geer, 1980). A personal history questionnaire (Dekker, Everaerd, & Verhelst, 1985) was administered at the beginning of the psychophysiological session. The questions covered sexual functioning, sexual satisfaction, and frequency of various sexual behaviors and experiences, in reference to a 6-month period before the psychophysiological session.
Procedure Subjects were tested individually. Before being scheduled for the psychophysiological session, each subject received a leaflet with a full description of the psychophysiological procedure. Confidentiality, hygiene, privacy during the psychophysiological session, and the opportunity to withdraw at any time were all assured to the subjects. When each subject arrived at the laboratory, he read and signed an informed consent form and completed the personal history questionnaire. The experimenter (Erick Janssen) then explained the psychophysiological procedure in detail and instructed the subject how to attach the genital devices to the penis. After the experimenter had left the room the subject placed the strain gauge on the penis. Subjects who were first exposed to the vibration conditions also attached the vibrator at this point. When the subject signaled (using a one-way intercom system) that the device (or devices) had been attached, a 5-min adaptation period was started. During this 5-min adaptation period, which included a 2-min baseline period, the subject listened to music. After this period, depending on the order, the erotic film (F) or 2 min of vibrotactile stimulation (V) was presented. The first order group started with the film condition, which was followed by the vibration and the vibration-and-film conditions. Subjects in the second order group received the vibration conditions first and then proceeded with the film condition. Between the two vibration conditions and the film presentation there was a 3-min return-to-baseline interval. At the end of the session, the subject's reactions to the films, the appreciation of the vibrotactile stimulus in terms of pleasantness, and the use of the devices were assessed.
Data Reduction, Scoring, and Data Analysis All data from the strain gauge output were recorded on a WEKA OEM 821060 thermowriter and simultaneously sampled (10 Hz) by an IBM AT personal computer for off-line analysis. Penile data were scored as millimeters of circumference, based on presession calibration of the strain gauge. Differences between baseline measures and evoked measures provided indexes of change in penile responding. The BMDP 4V program (Dixon, 1990) was used for analyses of variance (ANOVA) and covariance (ANCOVA). Greenhouse-Geisser probability levels are reported for repeated measures ANOVAs to control for possible violations of the homogeneity of variance (Vasey & Thayer, 1987). When required, post hoc contrast analyses (simple mean comparisons) were performed. The BMDP 4F and 6D programs were used for chi-square contingency analyses and Pearson product-moment correlations, respectively.
Results Subject Characteristics The patient groups and the sexually functional volunteers were compared on a number of subject characteristics, listed
in Table 1, using chi-square contingency analyses and one-way ANOVAs (a = .001), and follow-up tests where appropriate. Table 1 also presents information about a comparison group of 95 patients with erectile disorder. These patients were referred to the Sexual Dysfunction Clinic or Urology Department of the Academic Medical Center after completion of the study. Similar to the patients included in this study, patients in the comparison group were referred to the Academic Medical Center in consecutive order. The 95 patients participating in this study and the comparison patient group were comparable on all variables, indicating that the patient sample was representative for the clinic population. Statistical tests on the data of the subjects participating in this study indicated that patients in the organic group were older than either of the two other groups and that the psychogenic patients were older than the sexually functional men. Both patient groups had less years of education than the sexually functional men. Furthermore, both patient groups reported lower frequencies of morning erections, lower quality of sex life, and lower sexual desire than the sexually functional men. Group Comparisons of Genital Responses Figure 1 shows the maximal increases in circumference for the three subject groups in all conditions. A 3 X 2 X 3 (Group X Order X Condition) repeated measures ANOVA, with condition as the within-subjects variable, revealed significant main effects of group, F(2, 128) = 13.94, p < .0001, and condition, F(2,228) = 20.96, p < .0001. No significant main effect of order and no significant interactions were found. Post hoc contrasts on the group effect revealed that the sexually functional men showed higher responses than both the psychogenic, F( 1, 131) = 4.11, p < .04, and the organic, F( 1, 131) = 28.33, p < .0001, patient groups. The pure psychogenic group showed higher responses than the organic group, F(l, 131) = 10.85, p < .001. Post hoc contrasts on the condition effect revealed that the condition with vibration resulted in lower responses than the film condition, F ( l , 128) = 4.62, p < .03, and the vibration-and-film condition, F(l, 128) = 62.15, p < .0001. The film condition resulted in lower responses than the vibration-and-film condition,/^!, 128)= 13.85, p .05; for organics and functionals, p > .3).
Additional Analyses Because vibration was administered for a shorter duration (2 min) than the two film presentations (each for 3 min), the condition effects might be a result of differences in stimulus duration. Therefore, we performed an additional repeated measures ANOVA using the maximum circumference change that occurred during the first 2 min of each condition. Once again, significant main effects were found for group, F(2,128) = 14.08, p < .0001, and condition, F(2, 218) = 16.40, p < .0001. No significant main effect of order and no significant interactions were found. Post hoc contrasts confirmed the pattern of results
revealed by the analyses on the maximal circumference changes when the 3-min film data were used. To investigate whether the response patterns were related to age, correlations were computed between age and genital responses using the data of the three subject groups. For the organic and psychogenic patient groups, correlations in the vibration condition were strongly affected by the responses of one (age 45 years; 52 mm circumference change) and two (ages 19 and 28 years; 49 and 76 mm circumference change) outliers, respectively. Table 2 shows the correlations between genital response and age for all groups, including the correlations for the vibration condition after removal of these outliers. To test whether the differences between the psychogenic patients and the sexually functional men in the vibration condition (the only condition revealing a difference between these two groups) could be attributed to age differences, an ANCOVA was performed on the vibration data of all subjects with age as the covariate. A test of homogeneity of regression slopes revealed that the slopes of the regression lines were the same for all groups, thus legitimizing the use of ANCOVA. Although the ANCOVA revealed a nonsignificant effect of the covariate, F( 1, 135) = 2.43, p > . 12, the p value was close to. 10, indicating that the age differences may have been consequential. The effect of age, however, was found to be both nonsignificant and inconsequential after the data of the three outlying subjects were ex-
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JANSSEN, EVERAERD, VAN LUNSEN, AND OERLEMANS 30 n
during the vibration-and-film condition than psychogenic men with high pleasantness ratings (n = 22), F(l, 45) = 4.94, p < .03. No significant effects were found for the organic patient group, although the pattern of results closely resembled the results of the sexually functional men.
Vibralion Film
25 -
Vibration & Film
20 -
Discussion 15-
o £
10 -
5 -
Psychogenic Patients (N=50)
Organic Patients (N=45)
Control Subjects (N=50)
Figure 1. Penile responses to vibration, film, and vibration-and-film conditions of patients with psychogenic or organic erectile disorder and sexually functional men. There were significant differences between the psychogenically dysfunctional and organically dysfunctional men in the film and the vibration-and-film conditions, between the psychogenically dysfunctional and the sexually functional men in the vibration condition, and between the organically dysfunctional and sexually functional men in all conditions. Mm = millimeters.
eluded from analysis: covariate, F( 1, 131) = 0.08, p > .8. Moreover, the ANCOVA using the data of the remaining 142 subjects revealed an even higher significance level for the difference between sexually functional men and psychogenic men in the vibration condition, F(1, 135) = 2.43, p < .0007. In an earlier study on the effects of vibrotactile stimulation in sexually functional men, the rated pleasantness of vibrotactile stimulation was found to interact with the effects of the presented stimuli (Rowland & Slob, 1992). Therefore, we compared penile responses of subjects who gave a low pleasantness rating to the vibrotactile stimuli in the postexperimental interview with those subjects indicating high pleasantness ratings. A 3 X 2 X 2 (Group X Rating X Condition) repeated measures ANOVA with the two vibration conditions as the within-subjects variable, revealed a significant interaction effect of Group X Rating X Condition, F(2, 126) = 4.26, p < .02. An univariate ANOVA revealed no significant effects for the vibration condition. However, a significant interaction effect of Group X Rating was found for the combined vibration-and-film condition, F(2, 127) = 4.99, p < .008 (see Figure 2). Follow-up tests on the data of the vibration-and-film condition revealed a marginally significant effect on the ratings for the sexually functional men. Sexually functional subjects with high pleasantness ratings (n = 23) had higher penile responses than subjects with low pleasantness ratings (n = 23), F(l, 44) = 3.05, p < .09. These results indicate a replication of the findings reported by Rowland and Slob (1992) on sexually functional men. Unexpectedly, we found the reverse effect for the psychogenic patient group: Psychogenic men with low pleasantness ratings (« = 25) showed significantly higher penile responses
The combined presentation of vibrotactile stimulation and erotic film resulted in stronger penile responses than when the stimuli were presented separately. This effect supports the notion that reflexogenic and psychogenic erectile mechanisms act synergistically in the control of penile erections (de Groat & Steers, 1988;Kraneetal., 1990; Weiss, 1972). When the results of the condition with vibrotactile stimulation (V) are considered, a more intricate picture emerges from our data. Although psychogenics and sexually functional subjects did not differ in penile responses to the film and vibration-and-film conditions, responses of these two groups were, as predicted, significantly different in the vibration condition. Vibration initiated substantial penile response in sexually functional men but induced only minimal response in the psychogenic men (comparable to the organic involvement group). It has been assumed that in neurologically intact men, tactile stimulation of the genitalia evokes penile responses in a reflex-like manner (Masters & Johnson, 1966; Money, 1980). Although this may be a correct proposition when considering sexually functional men, the results of the psychogenic patient group clearly suggest that the reflexogenic erectile mechanism is highly susceptible to (central) inhibitory processes. When vibrotactile stimulation is combined with the presentation of an erotic film, the probability of this inhibition decreases drastically. The combination of vibration and film resulted in significantly higher responses than film or vibration alone. A possible explanation for these findings involves changes in the allocation of attention. It may be that when tactile and visual sexual stimuli are presented at the same time to patients with psychogenic erectile dysfunction, inhibition decreases because the attentional capacity for competing sexual worries, distracting thoughts, and so on, is reduced. Thus, inhibition of the reflexogenic response mechanism involved in vibrotactile stimulation disappears in the combined condition. Alternatively, although related to this interpretation, it may be that tactile
Table 2 Correlations Between Age and Genital Response (Maximum Circumference Change in Millimeters) Condition Group
Vibration
Film
Vibration & film
Functional Psychogenics" Organicsb c All(n=145)
-.06 -.35* (-.06) -.22 (-.04) -.26" (-.18*)
-.35** -.19 -.07 -.38**
-.01 -.46** -.29 -.36**
Note. Correlations after the exclusion of 2 subjects', 1 subject6, and the three subjects together" are given in parentheses. *p
