Physiologic Review. The Ischiocavernosus and Bulbospongiosus Muscles in Mammalian Penile Rigidity. Markus H. Schmidt and Helmut S.

Transcription

1 Sleep, 16(2): American Sleep Disorders Association and Sleep Research Society Physiologic Review The Ischiocavernosus and Bulbospongiosus Muscles in Mammalian Penile Rigidity Markus H. Schmidt and Helmut S. Schmidt Ohio Sleep Medicine Institute, Dublin, Ohio, U.S.A. Summary: The role of the perineal muscles in erection physiology is currently controversial. Specifically, confusion persists as to the function, if any, the ischiocavernosus (IC) and bulbospongiosus (BS) muscles possess in nonejaculatory erections. An extensive review of the evidence for and against such an erectile role across five orders of mammalian species indicates that the IC muscles create rigidity by producing suprasystolic intracavernous pressures. The BS muscles, on the other hand, are primarily involved in expelling semen during ejaculation. Beckett and coworkers were the first to demonstrate a clear relationship between IC muscle contractions, suprasystolic intracavernous pressures and rigidity. This Beckett model is used to differentiate an erect phase from a rigid erect phase in the erection cycle. The involvement of these muscles in sleep-related erection physiology is also reviewed. Clinical implications and directions for future research are discussed. Key Words: Ischiocavernosus (lc)-bulbospongiosus (BS) - Erection - Sleep - Perineal muscles. Perineal muscle involvement in erection physiology has been debated for more than four centuries. The current view concerning the perineal muscles remains confusing and contradictory. Of the perineal muscles, the ischiocavernosus (IC) and bulbospongiosus (BS) muscles are well documented to be highly active in ejaculation (1,2), but there is no consensus concerning their activity and function in nonejaculatory erection physiology. Some authors attribute an essential role to the Ie muscles in erectile rigidity (3,4). Others report that the Ie and BS muscles are quiescent during normal erections and, therefore, do not play a functional erectile role (5). Finally, some investigators report that these muscles are in fact active during erections, yet still do not ascribe a functional role to them in erection physiology (6). Four major erection models concerning perineal muscle involvement and blood flow have been proposed. In an early theory, Regnier de Graaf in 1668 thought that blood flow to the erectile tissues produced erections (7). De Graaf and a number of authors span- Accepted for publication September Address correspondence and reprint requests to Helmut S. Schmidt, M.D., Ohio Sleep Medicine Institute, 4975 Bradenton Ave., Dublin, Ohio 43614, U.S.A. ning several centuries (8-14) also hypothesized that contractions of the perineal muscles partially constricted penile vessels important for venous drainage, thus restricting venous outflow, It was postulated that venous compression resulting from this perineal muscle activity maintained engorgement of the penis, Other early researchers discounted such a role for these muscles based on anatomical investigations (15-19). In a more recent paradigm, researchers and clinicians for most of this century have considered blood flow to be maintained above the flaccid level throughout all phases of an erection. However, no role is given to any of the perineal muscles in erection physiology. Although these investigators have long debated the presence (20-28) or absence (29-31) of venous outflow restriction in the erection process, all postulate that arterial inflow into the erectile tissues simply maintains erectile engorgement. An essential difference between the "venous occlusion" version of this paradigm and the earlier model proposed by de Graaf that de Graaf identified perineal muscle contractions as the source of venous outflow restriction. A number of other erection models have also been proposed that involve some aspect of perineal muscle activity and penile blood flow. One of the most frequently cited is the work of Karacan et al. (32), who advocate an auxiliary role to the Ie and BS muscles 171

2 172 M. H. SCHMIDT AND H. S. SCHMIDT in erection physiology. These authors hypothesize that the IC and BS muscles act via a pumping action to increase or augment blood flow through the erectile tissues where the maximum theoretically achievable intracavernous pressures would be at or below the systolic level. A fourth major erection model was proposed two decades ago by Beckett (33-39) and Purohit (40). Only recently (after 1986) has this model received some consideration (3,4,41-45). The IC muscles are viewed as playing a critical role in creating rigidity during erections. By compressing the crura of the corpora cavernosa of the penis (CCP), dramatic supra systolic intracavernous pressures and, as a result, rigidity are produced. In addition, once the cavernous sinuses are filled with blood, a state of zero CCP blood flow in the deep arteries of the penis is proposed during the suprasystolic rigid erect state. However, the corpus spongiosum of the penis (CSP) is viewed as essentially an open system even during the rigid erect state. CCP blood flow and perineal muscle involvement in these models are summarized in Table 1. The IC and BS muscles are located at the base of the penis and are closely associated with two separate erectile tissue systems: the paired corpora cavernosa of the penis (CCP) and the single corpus spongiosum TABLE 1. Summary of the four major erection models concerning corpora cavernosa of the penis (CCP) blood flow and perineal muscle involvement Erection Model de Graaf(1668) Blood flow or "cardiogenic" model (20th century) Karacan et al. (1978) Beckett et al. (1972) CCP blood flow during rigidity Yes Yes Y es No Perineal muscle involvement Yes: contractions constrict venous drainage No Yes: increase CCP blood flow by a pumping action Yes: create rigidity and supra systolic CCP pressures of the penis (CSP), which envelops the urethra. The IC muscles surround and insert onto the crura of the CCP (Fig. 1). The paired BS muscles, on the other hand, wrap around and insert onto the midline of the bulb ofthe CSP (Fig. 1). Contractions of these muscles appear to compress the proximal portions of these erectile tissue systems and thereby redistribute intracavernous blood from the proximal into the distal erectile tissues (46). I. r1.'~ -.,, ::.> Deep membranous (Scarpa's) layer of subcutaneous fascia (cut away) lnt~~==l-fi<l~:- ~ ~~'~fg:amellt r -----~---,--Inguinal (poupart's) Deep (Buck's) fascia of penis Superficial inguinal ring External spermatic fascia investing spermatic cord ~~~~. ~~,--- BUl/bC)sponl'JiO,SUS muscle \~~, \-'----ls(;hi(,ccjvemc)sus muscle penis Inferior iascia of urogenital diaphragm Investing (C<lllaunet's) fascia (partially cut awa}') covers muscles of superficial perineal space Superficial transverse perineal muscle Ischial tuberosity Superficial perineal (Colles') fascia (cut edge) f,(,v.~ N"..; l' I ~, Gluteus maximu5 muscle FIG. 1. The ischiocavernosus (IC) muscles surround the crura of the corpora cavernosa penis (CCP). The paired bulbospongiosus (BS) muscles insert onto the midline of the bulb of the corpus spongiosum penis (CSP). Contractions of these muscles compress the proximal portions of the erectile tissues and redistribute intracavernous blood into the distal sinuses. (Copyright 1989 CIBA-GEIGY Corporation. Reproduced with permission from Atlas of Human Anatomy by Frank H. Netter, M.D. All rights reserved.)

3 IC AND BS MUSCLES IN MAMMALIAN PENILE RIGIDITY 173 The paired CCP, separated by an incomplete septum, essentially function as a single vascular unit in humans (47-49) and are supplied by the deep or cavernous arteries (50). Only rarely are the paired CCP found to be isolated from each other by a complete septum (51,52). The single CSP, however, is a separate vascular system in that it normally does not share any direct vascular communication with the paired CCP (23,52,53). The erectile tissues are composed of smooth muscle bundles that form a framework of collapsed vascular spaces known as cavernous sinuses (54). Blood is prevented from entering these vascular spaces when the penis is flaccid. With appropriate autonomic and local control, smooth muscle cells within the arteries and trabecular framework of the erectile tissues relax, allowing blood to enter the cavernous sinuses (3,55). The penis then becomes engorged and erect as blood expands the spongy erectile tissue. This basic understanding of the erection process is commonly agreed upon. Controversy, however, centers on two points: 1) the involvement and function of the IC and BS muscles that lie at the base of the penis and 2) the extent of blood flow through the CCP during erections. We shall examine evidence against and for an erectile role concerning the IC and BS muscles across major orders of mammalian species, including an evaluation of these muscles in sleep-related erections. Furthermore, to assess the involvement of the perineal muscles on the penile blood flow during erections, we also review relevant blood flow studies. EVIDENCE AGAINST AN ERECTILE ROLE FOR THE PERINEAL MUSCLES For the past three decades, researchers and clinicians have generally discounted perineal muscle involvement in erection physiology. One explanation for this historical view most likely resides in three influential publications: a 1960 publication by Bors and Comarr (56), a 1962 work by Kollberg et al. (57), and a 1964 paper by Newman et al. (31). These works are routinely cited by authors as evidence against a role for the perineal muscles in penile erections (8,29,58-61). Moreover, most prominent authors since these three publications do not even address the IC and BS muscles in erection physiology (1,30,62-67). Because of the impact of these three works on later publications, we shall briefly review their findings. Bors and Comarr (56) examined the impact of various forms of human spinal cord injury on sexual functioning. They also present some of their own findings in regard to the many ailments discussed. In this 30- page paper, only one sentence directly addresses the role of the perineal muscles in erection: It is now generally accepted the erection is the result of active arterial vasodilation and that the striated musculature of the pelvic floor is not essential for a sustained erection; this is confirmed by the fact that patients with lower motor neuron lesions (cauda equina injuries) have erections despite complete denervation and deafferentation of the pelvic floor muscles (p. 212). This conclusion is speculative and based purely on anecdotal data. Erectile functioning was assessed by patient interview only. It is therefore not known what erectile capability the patients actually possessed. Moreover, complete denervation of the pelvic floor musculature was not assessed by objective electromyography. Finally, not only may paraplegics exhibit normal reflex erections (68-70), but animal studies indicate that normal reflex-induced erections involving IC and BS muscle activity may still occur even after complete spinal transection above the lumbosacral level (71,72). Various forms of such sacral reflex control of the IC and BS muscles are well documented (73-75). Kollberg et al. (57) stated that the perineal muscles were involved in ejaculation, but played no role in penile erections. Using electromyography, these authors examined the perineal muscles during erection and ejaculation in human volunteers. However, the IC and BS muscles were not studied. Only the membranous urethral sphincter and the deep transverse perineal muscles were evaluated. Recent electromyographic studies ofthe IC and BS muscles indicate that these muscles are active in erections (32,76-81). In a 1964 review article on erection physiology, Newman et al. (31) briefly stated that the IC and BS muscles are not involved in erection physiology. The authors make this statement without presenting any specific data or cited reference. Like the paper by Bors and Comarr (56), only one sentence directly addresses the perineal muscles in erection physiology (p. 352): "Paraplegics may have satisfactory erection despite complete paralysis of the pelvic muscles". Gerstenberg et al. (5) in a recent (1990) article suggested that the IC and BS muscles are not active during erection and, therefore, cannot play an erectile role. They also cited Bors and Comarr (56) and Kollberg et al. (57) as primary supporting evidence. Gerstenberg and colleagues implanted needle electrodes into the IC and BS muscles. Perineal EMG activity was monitored during erection, masturbation and ejaculation in human volunteers. A "full erection" in the nonmasturbatory phase of the experiment was defined as a penile angle (relative to the body) equal to or greater than 90. It is, therefore, not known whether full rigidity was ever attained in these subjects. Moreover, in a separate phase of the experiment, perineal EMG activity was monitored during masturbation and ejaculation. They provide EMG tracings obtained during

4 174 M. H. SCHMIDT AND H. S. SCHMIDT masturbation where, in fact, the IC and BS muscles are observed to be active in the nonejaculatory erection phase. The authors do not comment on this perineal muscle activity. In an early (1938) study in the cat, Semans and Langworthy (17) concluded that the IC and BS muscles were not important for penile erection. The authors dissected these muscles away from the crura and found that erections still occurred. However, the authors did not differentiate the degree of erection achieved, and specifically whether only a rigid erection was compromised. Indeed, Semans and Langworthy (17) note (p. 844) that "Removing these muscles eliminated only momentary accentuation of erection". In addition, the authors describe that during erections with intact perineal muscles (p. 840), "the ischio- and bulbocavernosus muscles were seen to contract rhythmically". EVIDENCE FOR PERINEAL MUSCLE INVOLVEMENT ACROSS MAMMALIAN ORDERS Whereas the evidence against an erectile role for the IC and BS muscles is largely anecdotal, a large body of literature based on direct experimentation across several orders of mammalian species indicates that these muscles do playa vital role in erection physiology. Indeed, there is evidence to indicate that a common functional role of the IC and BS muscles may exist across mammalian species. For example, in all five mammalian orders examined to date, contractions of the IC muscles have been shown to create suprasystolic intracavernous pressures in the rigidification process of penile erections. Species within the class mammalia are divided into major groups or "orders". These orders diverged from each other at various points in mammalian evolution. A characteristic shared among the orders is considered indicative of having a primitive or common origin. Such knowledge of a common functional role is not only vital for researchers in need of human models, but also provides clues to the evolution of penile erections.we will therefore examine the evidence for an erectile role of the IC and BS muscles across major orders of the class mammalia. Order Perissodactyla Living perissodactyls, or odd-toed ungulates, include the horse and rhinoceros. To our knowledge only two studies have been performed, both on the horse (38,39). In the first study, Beckett et al. (39) implanted silver ring electrodes into the IC and BS muscles. In addition, either a needle-tipped catheter or a subminiature pressure transducer was implanted into the CCP 6000 c. ~ 5000 E EMG of Ie muscles ~ 4000 I l!! '" ~ " "~~~~~~~"~~~~~-- ~ I- 5 Sec. -I Fig. 2. Corpora cavernosa penis (CCP) pressure and electromyographic (EMG) activity of the ischiocavernosus (IC) and bulbospongiosus (BS) muscles during coitus in the stallion. (Reproduced with permission from Beckett et ai., Am J Physio/1973;225: 1073.) for pressure monitoring. A catheter was also implanted into the carotid artery to monitor arterial pressure. After a 2-week recovery period, a receptive mare was introduced to the stallion. Throughout the experiment, four parameters were recorded: 1) carotid arterial pressure, 2) CCP pressure, 3) IC EMG activity and 4) BS EMG activity. During the flaccid state, the mean CCP pressure was 13 mm Hg. When a receptive mare was seen by the stallion, the mean CCP pressure rose to 107 mm Hg. This "mild erection" was thought to be the result of vasodilation of the arteries supplying the cavernous sinuses. The evidence for this view was two-fold. First, the CCP pressure pulsated at the same frequency as the carotid arterial pressure. Second, there was no IC or BS muscle EMG activity during this time. As the stallion became more sexually excited when the mare was brought into close proximity, CCP pressures rose significantly above the systolic level with IC muscle activity. Finally, the mean peak CCP pressure during intromission rose to 6,530 mm Hg. The mean systolic arterial pressure, however, was only 245 mm Hg. Moreover, the troughs of these CCP pressure peaks remained far in excess of 1,000 mm Hg throughout this "full erection" (Fig. 2). The authors concluded that the IC muscles were the source of suprasystolic CCP pressures because CCP pressure peaks correlated with IC EMG muscle activity and not with BS EMG contractions (Fig. 2) and because lidocaine anesthesia of the IC muscles dramatically reduced peak CCP pressures. Complete local anesthesia of the IC muscles was virtually impossible, as indicated by the EMG, because of the variability and deep location in nerve supply to these muscles. Mean CCP pressures in stallions with anesthetized IC muscles dropped to 1,422 mm Hg, with the lowest measurement of 517 mm Hg. Stallions with low intracavernous pressures, although still suprasystolic, were unable to copulate because of insufficient penile rigidity.

5 IC AND BS MUSCLES IN MAMMALIAN PENILE RIGIDITY en 1j 800 EMGot ~ 700 BS Tuse'es OO01_~'~""~~~~~"~~~~~~~~ ~500 f~_~"ii~~ht~~~iit ~--- ILJOO ~ o t-mounlj INTROMISSION I-EJACULATION--t-olSMOUNTi FIG. 3. Corpus spongiosum penis (CSP) pressure and electromyographic (EMG) activity of the ischiocavernosus (IC) and bulbospongiosus (BS) muscles in the stallion during mounting, intromission, and ejaculation. (Reproduced with permission from Beckett et al., Am J Vet Res 1975;36:432.) In the second study by Beckett et al. (38) under similar experimental conditions, CSP (and not CCP pressure) was examined. The mean CSP pressure rose from 17 mm Hg in the flaccid state to 76 mm Hg when the receptive mare was in view of the stallion. The BS muscles were quiescent at this time. During intromission, the mean peak CSP pressure rose to 762 mm Hg with BS muscle firing. The troughs of these pressure peaks, however, were consistently below systemic systolic pressure (Fig. 3). The BS muscles fired at I-second intervals, and the CSP pressure peaks were found to correlate with these BS muscle bursts and not with IC EMG activity (Fig. 3). In addition, when the BS muscles were anesthetized, the mean peak CSP pressure fell significantly. It was, therefore, determined that the BS muscles were responsible for increasing the CSP pressure. These two studies, therefore, suggest that the IC muscles are important for suprasystolic CCP pressures, whereas the BS muscles are responsible for high CSP pressures. The authors note that the lower peak CSP pressures (762 mm Hg compared to 6,530 mm Hg of the CCP) may be due to greater venous drainage from the CSP. Although suprasystolic CSP pressure peaks are attained, as Fig. 3 indicates, the troughs of these pressure peaks consistently fall below the systolic level. It is hypothesized that only during the transient suprasystolic peaks does CSP blood flow momentarily cease, and that the CSP, unlike the CCP, essentially remains an open system even through the rigid state. According to Beckett, greater venous drainage from the CSP would be important for ejaculatory competence (38). During ejaculation, the BS muscles contract rhythmically (5). These contractions send pressure waves through the CSP to the glans. The pressure waves constrict the urethra as they travel distally and aid in expelling semen during orgasm. To sustain ejaculatory competence, it is vital that these pressure waves be dissipated before subsequent BS muscle contractions. Greater venous drainage from the CSP would, therefore, prevent total urethral constriction by maintaining lower CSP pressures that would allow relatively free urethral passage of semen during ejaculation. Order Artiodactyla The order artiodactyla, or even-toed ungulates, is a large and diverse group. Living members include antelope, giraffe, camel, cervids or deer, bovids such as the bull, and many others. From this order, the IC and BS muscles have been demonstrated to possess an erectile role in the bull (33,34,82,83) and the goat (35-37). Lewis et al. (82) monitored CCP and carotid arterial pressures during erection in bulls. Perineal muscle activity was not monitored in this study. These authors reported CCP pressures in excess of 1,700 mm Hg during natural (noncoital) erections. Systolic arterial pressure, however, did not exceed 200 mm Hg. Although the authors were unable to postulate the source of energy necessary to produce such high pressures, they did note that a closed system, separate from the systemic circulation, would be necessary for CCP pressures to exceed systolic arterial pressure. Beckett et ai. (33) studied the bull in the same manner as they studied the horse. Virtually the same results were reported. Mean CCP pressure during the flaccid state was 16 mm Hg. This pressure rose to 77 mm Hg when the receptive cow was introduced. As in the horse, the CCP pressure pulsated with the same frequency as the carotid arterial pressure at this time. In addition, the electromyogram (EMG) indicated no activity in the IC or BS muscles. During copulation, the mean peak CCP pressure increased to 14,198 mm Hg. These peak pressures were found to correlate with IC muscle activity. Anesthesia of the IC muscles greatly reduced CCP pressures. Although complete anesthesia was not possible, as indicated by the EMG, the bulls with the lowest CCP pressures were unable to copulate because of insufficient erection. Because of the remarkably high CCP pressures monitored in the bull during coitus, Beckett et al. (34) in a separate study experimentally induced CCP rupture to determine what pressures the cavernous system could withstand. Twenty-five isolated penile specimens were obtained. Each was artificially perfused while CCP pressures were monitored. The authors reported that the CCP could withstand pressures over 57,100 mm Hg (1,000 psi) before rupturing. Purohit and Beckett (40), in a similar experiment in the dog, report a mean CCP rupture pressure of 86,615 mm Hg. Beckett and co-workers (35,37) obtained similar results in the goat as in their experiments with the horse and bull. The IC muscles were found to be essential for penile rigidity by creating sustained suprasystolic CCP pressures (35). BS muscle bursts, on the other

6 176 M. H. SCHMIDT AND H. S. SCHMIDT hand, produced only transient supra systolic CSP pressure peaks (37). By anesthetizing the IC muscles, these authors also determined the minimum CCP pressure needed in the goat to accomplish vaginal penetration (35). Only when CCP pressures rose above 300 mm Hg was intromission possible. Moreover, as Beckett et al. (35) note (p. 361): "When effective anesthesia of these muscles was obtained, the CCP pressure increased only up to, or slightly below, the mean arterial pressure. The goat could not copulate because there was insufficient erection for the penis to enter the vagina". To determine whether the CCP becomes a closed system during rigid erections, and where vascular occlusion may occur, Beckett et al. (36) performed serial angiographies on the crus penis of the goat. After erections were produced by an electroejaculator, a contrast medium was injected into the internal pudendal artery. Serial angiographies were made at 0.5-second intervals during erection and detumescence. As long as the IC muscles were contracted and rigidity was maintained, the contrast medium was unable to enter the cavernous sinuses and was shown to be stopped just prior to the origin ofthe deep arteries. The authors concluded that occlusion occurred by mechanical compression of the deep artery either external to or within the tunica albuginea. With cessation of electro stimulation, the IC muscles relaxed and contrast media was able to flow freely into the CCP. Order Carnivora The most common carnivores are, of course, the many species of canids (or dogs) and felids (or cats). Other members include numerous species of fox, hyaena and aquatic carnivores, such as seals, sea lions and walruses. Although minimal work has been performed on cats, extensive studies have been performed on the dog (4,6,11,16,43,46). In a 1976 paper, Purohit and Beckett (40) examined both CCP and CSP pressures in the dog in the same manner as their many earlier studies in the horse, bull and goat. Again, it was shown that IC muscle contractions were responsible for the extremely high CCP pressure peaks (1,300-2,000 mm Hg prior to coitus and 5,000-7,000 mm Hg during coitus). On the other hand, mean peak CSP pressure rose to only 579 mm Hg at this time and was produced by BS muscle activity. Anesthesia of the IC muscles reduced CCP pressures below 200 mm Hg and prevented any of the dogs from accomplishing successful penetration. Lue et al. (84) selectively stimulated the cavernous nerves and pudendal nerves while monitoring CCP pressure in dogs. With cavernous nerve electrostimulation, causing the helicine arteries supplying the cav- ernous sinuses to vasodilate, CCP pressure rose with cavernous filling to approximate systolic arterial pressure. However, with the addition of pudendal nerve stimulation, causing IC muscle contraction, intracavernous pressures then increased to 400 mm Hg. This supra systolic pressure fell to 100 mm Hg as the IC muscles fatigued. Jiinemann et al. (85) recently repeated this experiment and obtained virtually identical results. Lue et al. (84), however, did not comment on a possible importance of the IC muscle-induced suprasystolic pressures or the potential relationship to penile rigidity. In a more recent (1988) review article, Aboseifand Lue (3) do postulate an essential role for the IC muscles in the process of penile rigidity. In this paper, Aboseif and Lue make an important distinction between the erect phase and the rigid erect phase of an erection. Similar phases were also described a year earlier by Hanyu et al. (4) and Jiinemann et al. (86). During the erect phase, CCP pressures attain a steady state approximating the systolic arterial pressure. The IC muscles are inactive at this time. This state is similar to Beckett's "mild erection" phase. The rigid erect phase, in contrast, occurs when the IC muscles compress the crura of the CCP. These contractions produce suprasystolic CCP pressures, a closed cavernous system, and rigidity. This phase is identical to the "full erection" phase described by Beckett. Hanyu et al. (4) describe a series of experiments on the canine penis under general anesthesia. Hanyu et al. selectively perfused the deep artery of the penis, which supplies the CCP at a perfusion pressure of 160 cm H 2 0. Erection was induced by papaverine infusion, and rigidity was maintained by bilateral electrostimulation of the IC muscles with simultaneous monitoring of flow through the deep artery. Perfusion through the deep artery markedly increased with papaverine. However, flow fell below the flaccid level during the erect stage as the CCP pressure approached the 160-cm H 2 0 perfusion pressure. Electrostimulation of the IC muscles produced the rigid stage and an associated sharp suprasystolic rise in CCP pressure. No flow through the deep artery was found during the rigid stage. In fact, when the canula was disconnected from the deep artery and the artery was open to the air in the suprasystolic rigid erect state, no backflow through the open artery was found. Similar results have been reported in more recent investigations (87,88). Vascular casts made during the rigid stage indicated that the deep artery was in fact occluded at the level of the tunica albuginea. In addition, the postcavemous venules that drain the cavernous spaces were found by scanning electron microscopy to be compressed between the expanded sinuses and tunica albuginea in the rigid stage. In the flaccid state, however, these ves- Sleep. Vol. 16. No

7 IC AND BS MUSCLES IN MAMMALIAN PENILE RIGIDITY 177 sels were freely patent. Thus, the authors demonstrated that a closed intracavernous system is accomplished by both venous and arterial occlusion during the rigid stage. Such penile vascular occlusion during rigidity has also been demonstrated by other recent works (43,88-90). By describing an erect stage and rigid stage, these authors appear to have independently divided an erection into separate phases comparable to that of Aboseif and Lue (3). Order Rodentia The IC and BS muscles have long been thought essential for penile erections in rodents (91-98). Unlike the species we have reviewed so far, male rats must lodge their semen as a "seminal plug" into the cervix of a female to enhance fertilization. Interestingly, the male rat also has the ability to dislodge the seminal plug of a previous male from a female and replace it with its own seminal plug. Such an evolutionary divergence in rodents gives rise to interesting implications in the evolution of penile erections, such as sperm competition among males (99). The IC muscles appear to be essential in producing dorsiflexions, or flips, of the penile body in the rat (91,93,98). Such flips of the body are necessary for intromission. Males lacking the IC muscles are generally unable to penetrate because of insufficient erection (19). BS muscle contractions further enhance erections of the glans (93,98). Rats with the BS muscles excised are unable to form intense erections or "cups" of the glans, which are necessary to firmly lodge the seminal plug into the cervix of a receptive female (91). Moreover, excision of the IC or BS muscles greatly reduces a male's ability not only to lodge its seminal plug, but also to dislodge that of a previous male as well (94). McKenna et al. (71), in a recent (1991) publication, simultaneously monitored intracavernous CCP pressure, IC and BS EMG activity, and carotid arterial pressure, as well as several other parameters including pudendal and cavernous nerve activity during penile erections in spinally transected rats. Reflex erections were induced by urethral stimulation. Such stimulations were applied for only seconds until erection was attained. During full erection, the IC and BS muscles were found to contract rhythmically and to coincide directly with suprasystolic CCP pressure peaks as high as 300 mm Hg. These authors reported similar results in an earlier work (72). Unfortunately, they do not specify which muscles, IC or BS, are responsible for producing such high CCP pressures. In addition, a maximum intracavernous pressure of300 mm Hg during IC and BS muscle contractions may be a conservative figure since the pressure transducer used to record CCP pressures saturated at this level (71). Quinlan et al. (100) suggest that the rat is a good human model for penile erection research. Although these authors do not address any potential involvement of the IC and BS muscles in erection physiology, recent developments in neural mapping and neural control of the perineal muscles (lol-lo7), as well as the current ability to measure directly intracavernous CCP pressures in rodents (71,72,108), suggest that this animal model may help delineate the specific involvement of the perineal muscles in human penile rigidity. It should be noted, however, that the role of the IC and BS muscles in seminal plug placement in rodents is unlike that of all other species examined in this review. Order Primates That the IC, BS and surrounding perineal muscles become highly active during human ejaculation is well known and relatively undisputed (1,2,109,110). However, their role in nonejaculatory erection physiology remains in question. Meehan and Goldstein (61) in 1983 devised a noninvasive technique for estimating CCP pressure. Using a sophisticated pressure cuff placed around the penis, human CCP pressure during "strong erections" was found to be 10 times the systolic arterial pressure. This finding was said to necessitate a closed cavernous system. However, the authors ruled out involvement of the IC and BS muscles as the generators of this high pressure and cited Bors and Comarr (56) and Kollberg et al. (57) as their primary supporting evidence. Meehan and Goldstein, without any direct experimental evidence, suggest instead that the supra systolic pressures they observed are the result of smooth muscle contraction of the CCP trabecular walls. Goldstein et al. (66), in an earlier paper, make a similar hypothesis. However, it is now well documented through direct experimentation that the cavernous smooth muscle cells are, in fact, tonically active during flaccidity and quiescent during tumescence and erection (67, ). Michal et al. (117) directly measured CCP pressure during artificially induced erections in human volunteers. During erections, the subjects were asked to voluntarily contract their perineal muscles. Two erection phases were noted by the authors. In the "mild erection" phase, CCP pressure remained at or slightly below systolic arterial pressure. In the "full erection" phase, voluntary contractions of the perineal muscles correlated with mean peak CCP pressures greater than 300 mm Hg. Similar suprasystolic CCP pressure peaks in humans have been reported by others (118,119). Contractions of the IC muscles were thought to com-

8 178 M. H. SCHMIDT AND H. S. SCHMIDT press the crura of the CCP. As a result, blood would be redistributed into the distal sinuses and, as a direct consequence, intracavernous pressure would increase above the systolic level. Lavoisier et al. (118) repeated the Michal et al. (117) experiment and found that intracavernous pressures in excess of 400 mm Hg coincided with voluntary IC muscle contractions. Moreover, duration of IC EMG activity covaried exactly with the duration of CCP pressure peaks. In addition, the peak CCP pressure was found to be a function of the integrated EMG activity, in that greater IC activity resulted in higher CCP pressure peaks. Lavoisier et al. (73,74) later demonstrated that the IC muscles are activated by sacral reflex loops when pressure or electrical stimulations are applied to the glans. It was hypothesized that these reflex loops would be essential in increasing penile rigidity during vaginal penetration and intercourse. Jiinemann et al. (120) studied the physiology of penile erections in six nonhuman primates. While monitoring CCP pressures, the cavernous and pudendal nerves were stimulated in various combinations. The authors state that with cavernous nerve electrostimulation alone, CCP pressures rose to reach up to systolic arterial pressure. They further emphasized that suprasystolic arterial pressures were recorded only with simultaneous cavernosa1 and pudendal nerve stimulation. Activation of the pudendal nerve resulted in IC muscle contractions. The authors suggest that the IC muscles are the energy source responsible for the suprasystolic CCP pressures. PERINEAL MUSCLE INVOLVEMENT IN HUMAN SLEEP-RELATED ERECTIONS The existence of penile erection cycles during sleep was described in the early 1940s (121). These erection cycles in sleep were found to occur approximately every 85 minutes and last about 25 minutes each in duration, identical to the cyclicity and duration of rapid eye movement (REM) sleep, which was discovered a decade later. Fisher et al. (122) and Karacan et al. (123) later demonstrated a strong association between REM sleep and the occurrence of penile erections. Sleeprelated erections in association with other REM sleep parameters have since been used to differentiate psychogenic from organic impotence ( ). Although the IC and BS muscles generally have not been addressed in reviews of the sleep laboratory's role in the diagnosis of impotence (128,129), these perineal muscles appear to possess a significant role in sleep related erection physiology. Karacan et al. (32,76-78) were the first to report perineal muscle activity during sleep-related tumescence. These authors placed bilateral electrodes on the Sleep. Vol. 16, No.2, 1993 perineum, each electrode 2 cm lateral to the midline. This recording montage did not allow the differentiation oflc and BS muscle activity. The terminology of "bulbo-ischiocavernosus" muscle activity is used. They reported spontaneous bulbo-ischiocavernosus muscle bursts occurring during REM sleep-related erections at a frequency of approximately once every 2 minutes. Using a "segmental pulse volume recorder" placed around the penis, Karacan et al. (32,77) also reported blood flow increases with bulbo-ischiocavernosus muscle contractions. Their findings, however, are in direct opposition to the Beckett erection model, which necessitates decreased or zero CCP blood flows during rigid erections in association with IC muscle contractions. The pulse volume recorder used by Karacan et al. (32) is essentially a pressure cuff, i.e. a segmental plethysmograph (130), now commonly used in peripheral vascular laboratories. Transient pressure fluctuations monitored with this recorder are thought to represent transient volume changes. However, this device does not measure blood flow. Karacan et al. (32) even state (p. 180): "Our pulse-volume recorder measured transient changes in the volume of the penis that we can assume were due to changes in blood volume and, by extension, blood flow". From the figures they provide (for example fig. 1 in ref. 32), Karacan and colleagues appear to have recorded two separate physiological events with their pulse volume recorder. When the bulbo-ischiocavernosus muscles are silent, a pulsatile flow pattern is apparent during erection. This is likely a recording of blood flow through the dorsal artery of the penis that lies just beneath this pressure cuff device but external to the tunica albuginea and is not a recording from the deep or cavernous arteries supplying the CCP. Since the dorsal artery of the penis supplies primarily the CSP (50,90), and since the CSP, unlike the CCP, remains essentially an open system throughout the erection (41), it is logical that blood flow should be found in the dorsal artery throughout the erection cycle. With bulbo-ischiocavernosus muscle activity, however, large, artifact-like amplitude increases in the segmental pulse volume recording are shown, and, in our opinion, are erroneously assumed by Karacan and colleagues to represent augmentations in blood flow. These events more likely represent CCP pressure increases in association with IC muscle activity, similar to what Meehan and Goldstein (61) and Lavoisier et al. (81,118) have reported using similar pressure cuff devices. Allen et al. (79,80) also reported spontaneous bulboischiocavernosus muscle activity during sleep related erections. They, like Karacan et al. (32,77), also do not distinguish IC from BS muscle activity. Although the functional role of these muscles was not addressed, Allen and colleagues concluded that impaired perineal

9 IC AND BS MUSCLES IN MAMMALIAN PENILE RIGIDITY 179 TABLE 2. Suprasystolic peak corpora cavernosa o/the penis (CCP) pressures during penile rigidity across mammalian species as reported in the literature Species Stallion Bull Goat Dog Rat Human Human Human Human Human CCP pressures during penile rigidity (mm Hg) 6,530 14,198 7,003 7, a 1, b Investigators Beckett et al. (39)' Beckett et al. (33) Beckett et al. (35) Purohit and Beckett (40) McKenna et ai. (71) Meehan and Goldstein (61) Lavoisier et al. (118) Lavoisier et al. (81) Michal et al. (117) Lue et al. (119) a Probably a conservative value since the pressure transducer saturated at this level. Precise maximum values were not provided. c Numbers inside parentheses are reference numbers for this article. muscle activity is indicative of neurogenic impotence. Allen et al. (79,80) monitored bulbo-ischiocavernosus muscle activity in association with other sleep related tumescence parameters, suggesting that such recordings might help distinguish vasculogenic from neurogenic impotence. Lavoisier et al. (81) simultaneously monitored penile circumference, rigidity and IC muscle activity by electromyography during sleep-related tumescence. Circumference was measured by mercury loop strain gauges and rigidity by a pressure cuff placed around the penis. This specially designed hydraulic pressure cuff was thought to be a good indicator of direct intracavernous pressure measurements (131). The three variables-penile circumference, rigidity and IC muscle activity-were found to peak in unison. In fact, spontaneous IC muscle activity during (REM) sleep-related erections was found to coincide directly with suprasystolic CCP pressure peaks frequently in excess of 300 mm Hg. In comparison with their earlier results during waking-state erections (118), these authors suggested that the involvement of the IC muscles in penile rigidity during sleep-related erections is identical to waking-state erection physiology. Schmidt et al. (132) recently reported that a lack of IC muscle activity during REM sleep is associated with nearly a 95% chance of a diagnosis of organic impotence. Moreover, these authors separately monitored IC and BS EMG activity during sleep-related tumescence by placing bilateral electrodes over the IC muscles with an additional two surface electrodes directly over the BS muscles. Although subjects having absent or markedly diminished BS muscle activity were evenly distributed between the different subgroups of patients, a lack ofic muscle activity was associated with a diagnosis of organic impotence. In addition, using this montage, different patterns of IC and BS muscle activity have been identified. For example, the BS muscles tend to be more tonically active during REM sleep (in contrast to the IC muscles) and exhibit phasic muscle bursts in association with other phasic REM sleep events. The IC muscles, on the other hand, are silent except for intermittent muscle bursts during REM sleep occurring every 30 seconds to 2 minutes. This frequency ofic muscle activity is similar to what Karacan et al. (32) have reported for "bulbo-ischiocavernosus" activity. Unlike BS muscle activity, IC muscle activity during sleep erections does not appear to be correlated with other phasic phenomena of REM sleep. Ongoing (unpublished) observations suggest that subgroups of impotent patients could be identified in relation to various forms of perineal muscle impairment during (REM) sleep tumescence. SUMMARY Regnier de Graaf (12) in 1668 was the first to hypothesize an erectile role for the IC and BS muscles similar to the Beckett model. In contrast to Beckett, however, de Graaf also ascribed a venous occlusive role to these muscles. Although other such earlier authors (15,83,133) mentioned in passing that the perineal muscles may be important in erection physiology, Beckett and his group demonstrated for the first time a clear relationship between IC muscle contraction, CCP pressure and penile rigidity. This Beckett model has major implications for future clinical research. For example, a subpopulation of impotent patients has been found to possess normal circumference increases during sleep related erections, yet exhibit little or no rigidity (134,135). Future studies need to assess if the lack of rigidity is potentially related to IC muscle failure. From the literature presented, at least two principles have emerged that must be further addressed in future research. First, supra systolic CCP pressures during normal erections have been identified in seven mammalian species, including humans. Such pressures, coinciding with IC muscle contractions, have been found during coital, noncoital and sleep-related erections, and have been documented to effect copulatory capability. Table 2 summarizes the CCP pressures found in various mammalian species during rigid erection phases. Second, a closed and isolated system within the erectile tissues is necessary for pressures within the CCP to exceed that of the rest of the body. This very likely includes both arterial and venous occlusion. Without such vascular occlusion, arterial backflow from the cavernous sinuses into the systemic vascular system would occur during supra systolic CCP pressures. In

10 180 M. H. SCHMIDT AND H. S. SCHMIDT addition, such high pressures within the erectile tissues would not be attainable in an open erectile-systemic system. The Beckett model, which has been refined to specifically identify the erect phase and rigid erect phase, is the only model that adequately explains both the presence of suprasystolic CCP pressures and a state of zero intracavernous CCP blood flow during full rigidity. Relaxation of smooth muscle cells in the supplying arteries and cavernous framework ofthe erectile tissues allow the cavernous sinuses to completely fill with blood. Reflex IC muscle contractions compress the crura of the CCP. Such contractions are said to create rigidity by greatly increasing intracavernous pressures far in excess of the systolic arterial blood pressure. These pressures compress the cavernous vasculature, such as the drainage system at the level of the tunica albuginea, and create a closed cavernous system. It is not clear if humans exhibit sustained suprasystolic CCP pressures as in other nonhuman animals during penile rigidity. Alternatively, repetitive and intermittent IC muscle contractions may create transient supra systolic pressure peaks whose troughs actually fall back down to the systolic level. This would allow for some blood flow through the CCP between IC muscle contractions. The mechanism by which the IC muscles maintain rigidity in human erections requires further investigation. The BS muscles have been shown to be essential for ejaculation. BS muscle contractions compress the bulb of the CSP and create only brief or transient suprasystolic CSP pressure waves. Because the CSP pressures remain far below those of the CCP during rigidity, the CSP, unlike the CCP, essentially remains an open vascular system throughout the erection. To what extent the BS muscles are involved in penile rigidity, however, is not clear. Unfortunately, age-specific normative data ofic and BS muscle activity in sleeping and waking-state erections in humans is totally lacking. This lack of normative data, in combination with misleading conclusions drawn concerning the erectile function of these muscles, has likely led to the general dearth of investigation of the IC and BS muscles in general and, specifically, in sleep-related erection research. Such research may potentially reignite interest in polysomnography with sleep-related erection studies as a useful tool in the diagnosis and treatment of impotence. Each ofthe five mammalian orders examined to date indicate that the IC muscles create suprasystolic intracavernous pressures and rigidity by compressing the proximal portions of the erectile tissues. Further research addressing the Beckett model in these and other species, including humans, is necessary to establish if a common mechanism of rigidity exists among mam- mals. The mammalian orders diverged from each other very early in their evolution. Unless similar erectile physiology evolved independently in each order, it is possible that the role of the IC muscles in penile rigidity may be a primitively shared characteristic and, perhaps, even a general mammalian phenomenon. Acknowledgements: Supported in part by a grant from Riverside Methodist Hospitals, Columbus, Ohio and the Sleep Medicine Research Foundation, Inc., Dublin, Ohio. REFERENCES I. Benson GS, Lipshuitz LI, McConnell J. Mechanisms of human erection, emission, and ejaculation: current clinical concepts. In: von Eschenbach AC, Rodriguez DB, eds. Sexual rehabilitation of the urologic cancer patient. Boston: G.K. Hall Medical Publishers, 1981 : Gerstenberg T, Levin RJ, Wagner G. Correlation of expelled semen volume with the electro myographic activity of the bulbocavernosus and ischiocavernosus muscles during ejaculation in man. J. PhysioI1987;390:137P. 3. Aboseif SR, Lue TF. Hemodynamics of penile erection. Urologic Clinics of North America 1988;15: Hanyu S, Iwanaga T, Kano K, Sato S. Mechanism of penile erection in the dog. Urollnt 1987;42: Gerstenberg TC, Levin RJ, Wagner G. Erection and ejaculation in man. Assessment of the electromyographic activity of the bulbocavernosus and ischiocavernosus muscles. Br J Uro11990; 65: Hart BL. The action of extrinsic penile muscles during copulation in the male dog. Anat Rec 1972; 173: de GraafR. A treatise concerning the generative organs of man. An annotated translation of Tractatus de Virorum Organis Generationi Iservientibus (1668). J Reprod Fert 1972; 17(suppl): Benson GS. Mechanisms of penile erection. Invest Uro11981; 19: Hirsch EW. The so-called arterial valves in the penile arteries. J UroI1931;25: Lindner HH, Feldman SE. Surgical anatomy of the perineum. Surgical Clinics of North America 1962;42(4): II. Christensen Gc. Angioarchitecture of the canine penis and the process of erection. Am J Anat 1954;95: Varolio C. Anatomiae, Sive de Resolutione Corporis Humani ad Caesarem Mediovillanum Libri IIII: a Joan. Mercurialis de Nervis Opticis, Nonnullisque Aliis, Preter Communem Opinionem in Humano Capite Observatis. Francofurti: Apud Joannem Wechelum & Petrum Fischerum consortes, 1591: Gray H. Gray's Anatomy. In: Pick TP, Howden R, eds Edition anatomy, descriptive and surgical. Philadelphia: Running Press, 1974: Wespes E, Nogueira MC, Herbaut AG, Caufriez M, Schulman Cc. Role of the bulbocavernosus muscles on the mechanism of human erection. Eur Uro11990; 18: Henderson VE, Roepke MH. On the mechanism of erection. Am J PhysioI1933;106: Hart BL, Kitchell RL. Penile erection and contraction of penile muscles in the spinal and intact dog. Am J PhysioI1966;210: Semans JH, Langworthy OR. Observations on the neurophysiology of sexual function in the male cat. J UroI1938;40: Kiss F. Anatomisch-histologische Untersuchungen uber die Erection. Zeitschriftfur Anatomie und Entwicklungsgeschichte 1921 ;61 : Cadiat M. Etude sur les muscles du perinee en particulier sur les muscles dits de Wilson et de Guthrie. Journal de I'Anatomie et de la Physiologie Normales et Pathologiques 1877; 13:39-59.

11 IC AND BS MUSCLES IN MAMMALIAN PENILE RIGIDITY Aoki H, Hiroshi T, Banya Y et al. Human penile hemodynamics studied by a polarographic method. J Uro11986; 135: Jiinemann K-P, Lue TF, Fournier GR, Tanagho E. Hemodynamics of papaverine- and phentolamine-induced penile erection. J Urol 1986; 136: Lue TF, Takamura T, Schmidt RA, Palubinskas AJ, Tanagho EA. Hemodynamics of erection in the monkey. J Urol 1983; 130: Aboseif SR, Breza J, Lue TF, Tanagho EA. Penile venous drainage in erectile dysfunction. Anatomical, radiological and functional considerations. Br J UroI1989;64: Conti G. L'erection du penis humain et ses bases morphologico-vasculaires. Acta Anat 1952;14: Fitzpatrick TJ. Venography of the deep dorsal venous and valvular systems. J UroI1974;111: Fitzpatrick TJ, Cooper JF. A cavernosogram study on the valvular competence of the human deep dorsal vein. J Uro11975; 113: Fitzpatrick T. The corpus cavernosum intercommunicating venous drainage system. J Urol 1975; 113: Krane RJ, Goldstein I, Saenz de Tejada I. Impotence. N Engl J Med 1989;321: Weiss HD. The physiology of human penile erection. Ann Intern Med 1972;76: Dorr LD, Brody MJ. Hemodynamic mechanisms of erection in the canine penis. Am J Physiol 1967;213: Newman HF, Northrup JD, Devlin J. Mechanism of human penile erection. Invest UroI1964;1: Karacan I, Hirshkowitz M, Salis PJ, Narter E, Safi MF. Penile blood flow and musculovascular events during sleep-related erections of middle-aged men. J Urol 1987; 138: Beckett SD, Walker DF, Hudson RS, Reynolds TM, Vachon RI. Corpus cavernosum penis pressure and penile muscle activity in the bull during coitus. Am J Vet Res 1974;35: Beckett SD, Reynolds TM, Walker DF, Hudson RS, Purohit RC. Experimentally induced rupture of corpus cavernosum penis of the bull. Am J Vet Res 1974;35: Beckett SD, Hudson RS, Walker DF, Vachon RI, Reynolds TM. Corpus cavernosum penis pressure and external penile muscle activity during erection in the goat. Bioi Reprod 1972; 7: Beckett SD, Reynolds TM, Hudson RS, Holley RS. Serial angiography of the crus penis of the goat during erection. Bioi Reprod 1972;7: Beckett SD, Purohit RC, Reynolds TM. The corpus spongiosum penis pressure and external penile muscle activity in the goat during coitus. Bioi Reprod 1975; 12: Beckett SD, Walker DF, Hudson RS, Reynolds TM, Purohit RC. Corpus spongiosum penis pressure and penile muscle activity in the stallion during coitus. Am J Vet Res 1975;36: Beckett SD, Hudson RS, Walker DF, Reynolds TM, Vachon RI. Blood pressures and penile muscle activity in the stallion during coitus. Am J PhysioI1973;225: Purohit RC, Beckett SD. Penile pressures and muscle activity associated with erection and ejaculation in the dog. Am J Physiol 1976;231: Aboseif SR, Lue TF. Fundamentals and hemodynamics of penile erection. Cardiovasc Intervent Radio11988; II: Nelson RP, Lue TF. Physiology, hemodynamics and pharmacology of penile erection. Archivio Italiano di Urologia Nefrologia e Andrologia 1988;60: Hanyu S. Morphological changes in penile vessels during erection: the mechanism of obstruction of arteries and veins at the tunica albuginea in dog corpora cavernosa. UrolInt 1988;43: Schmidt HS, Schmidt MH. Current physiology of erectile mechanisms: basis for five phases of penile erection. Sleep Res 1991;21: Schmidt MH, Schmidt HS. Penile rigidity and the perineal musculature in mammals: a review. Sleep Res 1991;21: Colleen S, Holmquist B, Olin T. An angiographic study of erection in the dog. Urol Res 1981 ;9: Wagner G. Erection: anatomy. In: Wagner G, Green R, eds. Impotence. New York: Plenum Press, 1981: Banya Y, Ushiki T, Takagane H, et al. Two circulatory routes within the human corpus cavernosum penis: a scanning electron microscopic study of corrosion casts. J Urol 1989; 142: Lierse W. Blood vessels and nerves of the human penis. Urol Int 1982;37: Breza J, AboseifSR, Orvis BR, Lue TF, Tanagho EA. Detailed anatomy of penile neurovascular structures: surgical significance. J UroI1989;141: Keogh EJ. Absent cross-circulation between corpora cavernosa. J UroI1989;142:l Kolbenstvedt A, Egge T, Klevmark B, Talseth T. Isolated cavernous bodies. J UroI1990;143: Benoit G, Delmas V, Gillot C, Jardin A. The anatomy of erection. Surg Radiol Anat 1987;9: Goldstein AMB, Padma-Nathan H. The microarchitecture of the intracavernosal smooth muscle and the cavernosal fibrous skeleton. J UroI1990;144: Lue TF, Zeineh SJ, Schmidt RA, Tanagho EA. Physiology of penile erection. World J UroI1983;1: Bors E, Comarr AE. Neurological disturbances of sexual function with special reference to 529 patients with spinal cord injury. Urological Survey 1960;10: Kollberg S, Petersen I, Stener I. Preliminary results of an e1ectromyographic study of ejaculation. Acta Chir Scand 1962; 123: Newman HF, Northup JD. Mechanism of human penile erection: an overview. Urology 1981 ;27: Van Arsdalen KN, Malloy TR, Wein AJ. Erectile physiology, dysfunction and evaluation. Part I: physiology of erection. Monographs in Urology 1983: Newman HF. Physiology of erection: anatomic considerations. In: Krane RJ, Siroky MB, Goldstein I, eds. Male sexual dysfunction. Boston: Little Brown & Co., 1983: Meehan JP, Goldstein AMB. High pressure within corpus cavernosum in man during erection: its probable mechanism. Urology 1983;21: Virag R. Arterial and venous hemodynamics in male impotence. In: Bennett AH, ed. Management of male impotence. Baltimore: The Williams & Wilkins Co., 1982: Wagner G. Erection: physiology and endocrinology. In: Wagner G, Green R, eds. Impotence. New York: Plenum Press, 1981 : Newman HF, Reiss H. Artificial perfusion in impotence. Urology 1984;24(5): Conti G, Virag R, Von Niederhausern W. The morphological basis for the polster theory of penile vascular regulation. Acta Anat 1988;133: Goldstein AMB, Meehan JP, Zakhary R, Buckley PA, Rogers FA. New observations on microarchitecture of corpora cavernosa in man and possible relationship to mechanism of erection. Urology 1982;20: Lue TF, Takamura T, Umraiya M, Schmidt RA, Tanagho EA. Hemodynamics of canine corpora cavernosa during erection. Urology 1984;24: Kellett JM. Sexual expression in paraplegia. Br Med J 1990; 301: Sachs BD, Bitran D. Spinal block reveals roles for brain and spinal cord in the mediation of reflexive penile erections in rats. Brain Res 1990;528: Biering-Sorensen F, Sonksen J. Penile erection in men with spinal cord or cauda equina lesions. Seminars in Neurology 1992;12: McKenna KE, Chung SK, McVary KT. A model for the study of sexual function in anesthetized male and female rats. Am J PhysioI1991;261:RI Chung SK, McVary KT, McKenna KE. Sexual reflexes in male and female rats. Neurosci Let 1988;94: Lavoisier P, Proulx J, Courtois F, Reflex contractions of the

12 182 M. H. SCHMIDT AND H. S. SCHMIDT ischiocavernosus muscles following electrical and pressure stimulations. J UroI1988;139: Lavoisier P, Proulx J, Courtois F, de Carufel F. Bulbocavernosus reflex: its validity as a diagnostic test of neurogenic impotence. J UroI1989;141: Blaivas JG, O'Donnell TF, Gottlieb P, Labib KB. Measurement of bulbocavernosus reflex latency time as part ofa comprehensive evaluation of impotence. In: Zorgniotti A W, Rossi G, eds. Vasculogenic impotence. Springfield, Illinois: Charles C. Thomas, 1980: Karacan I, LaIis PJ, Williams RL. The role of the sleep laboratory in diagnosis and treatment of impotence. In: Williams RL, Karacan I, Frazier SH, eds. Sleep disorders: diagnosis and treatment. New York: John Wiley and Sons, 1978: Karacan I, AsIan C, Hirshkowitz M. Erectile mechanisms in man. Science 1983;220: Karacan I, Salis PJ, Hirshkowitz M, Borreson RE, Narter E, Williams RL. Erectile dysfunction in hypertensive men: sleeprelated erections, penile blood flow and musculovascular events. J UroI1989;142: Allen RP, Smolev JK. Bulbo-ischio-cavernosus muscle activity in determining etiology for organic impotence. In: Virag R, Virag H, eds. Proceedings of the First World Meeting on Impotence. Paris: CERI, 1984: Allen RP, Brendler CB. Nocturnal penile tumescence predicting response to intracorporeal pharmacological erection testing. J Uro/1988;140: Lavoisier P, Proulx J, Courtois F, de Carufel F, Durand L-G. Relationship between perineal muscle contractions, penile tumescence, and penile rigidity during nocturnal erections. J Urol 1988; 139: Lewis JE, Walker OF, Beckett SO, Vachon RI. Blood pressure within the corpus cavernosum penis of the bull. J Reprod Fert 1968; 17: Watson JW. Mechanism of erection and ejaculation in the bull and ram. Nature 1960;204: Lue TF, Umraiya M, Takamura T, Schmidt RA, Tanagho EA. Animal models for penile erection studies. Neurourol Urodyn 1983;2: JUnemann K-P, Persson-Jiinemann C, Tanagho EA, AIken P. Neurophysiology of penile erection. Urol Res 1989; 17: Jiinemann K-P, Lue TF, Melchior H. Die Physiologie der penilen erektion I. Hamodynamik der penilen Erektion. Urologe fa} 1987;26: Hanyu S, Iwanaga T, Tamaki M, Kano K, Sato S. Increase in venous outflow from the corpora cavernosa during mild erection in dogs. UrolInt 1992;48: Tamaki M. Mechanism preventing backflow from the canine corpora cavernosa to arteries in the rigid phase of penile erection. UrolInt 1992;48: Fournier GR, Jiinemann K-P, Lue TF, Tanagho EA. Mechanisms of venous occlusion during canine penile erection: an anatomic demonstration. J UroI1987;137: Kano K-I, Hanyu S, Iwanaga T, Sato S. Scanning electron microscope observation of penile vascular casts in the dog: an inquiry into the possible mechanism of erection based on the findings. Biomed Res 1987;8: Sachs BD. Role of striated muscles in penile reflexes, copulation, and induction of pregnancy in the rat. J Reprod Fert 1982;66: Elmore LA, Sachs BD. Role of the bulbospongiosus muscles in sexual behavior and fertility in the house mouse. Pysiol Behav 1988;44: Hart BL, Melese d'hospital PY. Penile mechanisms and the role of the striated penile muscles in penile reflexes. Physiol Behav 1983;31: Wallach SJR, Hart BL. The role of the striated penile muscles of the male rat in seminal plug dislodgement and deposition. Physiol Behav 1983;31 : Holmes G, Chapple W, Leipheimer R, Sachs B. Electromyographic analysis of male rat perineal muscles during copulation and reflexive erections. Physiol Behav 1991 ;49: Holmes GM, Sachs BD. Ejaculatory reflex in copulating rats: normal bulbospongiosus activity without apparent urethral stimulation. Neurosci Let 1991; 125: , Sachs BD, Meisel RL. The physiology of male sexual behavior. In: Knobi1 E, Neill J, et ai., eds. The physiology of reproduction. New York: Raven Press, Ltd., 1988: Sachs BD. Potency and fertility: Hormonal and mechanical causes and effects of penile actions in rats. In: Balthazart J, Prove E, Gilles R, eds. Hormones and behaviour in higher vertebrates. Berlin: Springer-Verlag, 1983: Hart BL. Role of testosterone secretion and penile reflexes in sexual behavior and sperm competition in male rats: a theoretical contribution. Physiol Behav 1983;31: Quinlan OM, Nelson RJ, Partin AW, Mostwin JL, Walsh Pc. The rat as a model for the study of penile erection. J Uro11989; 141: Sasaki M, Arnold AP, Androgenic regulation of dendritic trees of motoneurons in the spinal nucleus of the bulbocavernosus: reconstruction after intracellular iontophoresis of horseradish peroxidase. J Comp NeuroI1991;308:11-27, 102. Monaghan EP, Breedlove SM. Brain sites projecting to the spinal nucleus of the bulbocavernosus. J Comp Neuro11991; 307: , Collins WF, Erichsen JT, Rose RD, Pudendal motor and premotor neurons in the male rat: a WGA transneuronal study. J Comp Neurol 1991 ;308: Vercelli A, Cracco C. Effects of prepubertal castration on the spinal motor nucleus of the ischiocavernosus muscle of the rat. Cell Tissue Res 1990;262: Pascual 11, Insausti R, Gonzalo LM. Pudendal nerve topography in the rat spinal cord projections studied with the axonal tracer wheat germ agglutinin conjugated-horseradish peroxidase. J UroI1992;147: Marson L, McKenna KE. The identification of a brainstem site controlling spinal sexual reflexes in male rats, Brain Res 1990;515: Marson L, McKenna KE. A role for 5-hydroxytryptamine in descending inhibition of spinal sexual reflexes. Exp Brain Res 1992;88: Chen K-K, Chan JYH, Chang LS, Chen M-T, Chan SHH. Intracavernous pressure as an experimental index in a rat model for the evaluation of penile erection. J UroI1992;147: Petersen I, Stener I. An electromyographical study of the striated urethral sphincter, the striated anal sphincter, and the levator ani muscle during ejaculation. Electromyography 1970; 10: Kadefors R, Petersen I. Spectral analysis of myo-electric signals from muscles of the pelvic floor during voluntary contraction and during reflex contractions connected with ejaculation. Electromyography 1970; 1 0: Saenz de Tejada I, Goldstein I, Krane RJ. Local control of penile erection. Urologic Clinics of North America 1988; 15: Wagner G, Gerstenberg T, Levin RJ. Electrical activity of corpus cavernosum during flaccidity and erection of the human penis: a new diagnostic method? J UroI1989;142: Jiinemann K-P, Luo J-A, Lue TF, Tanagho EA. Further evidence of venous outflow restriction during erection. Br J Urol 1986;58: StiefCG, Thon WF, Djamilian M, et ai. Single potential analysis of cavernous electrical activity. Urol Res 1991; 19: Rafjer J, Aronson WJ, Bush PA, Dorey FJ, Ignarro LJ. Nitric oxide as a mediator of relaxation of the corpus cavernosum in response to nonadrenergic, noncholinergic neurotransmission. N Engl J Med 1992;326: StiefCG, Thon WF, Djamilian M, AllhoffEP, Jonas U. Transcutaneous registration of cavernous smooth muscle electrical activity: noninvasive diagnosis of neurogenic autonomic impotence. J UroI1992;147: Michal V, Simana J, Rehak J, Masin J. Haemodynamics of erection in man. Physiol Bohemoslov 1983;32: Lavoisier P, Courtois F, Barres 0, Blanchard M. Correlation between intracavernous pressure and contraction of the ischiocavernosus muscle in man. J UroI1986;136:936-9.